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Archive for the ‘Regenerative Medicine’ Category

Stem Cells Applications in Regenerative Medicine and Disease …

Friday, December 6th, 2024

Abstract

Regenerative medicine, the most recent and emerging branch of medical science, deals with functional restoration of tissues or organs for the patient suffering from severe injuries or chronic disease. The spectacular progress in the field of stem cell research has laid the foundation for cell based therapies of disease which cannot be cured by conventional medicines. The indefinite self-renewal and potential to differentiate into other types of cells represent stem cells as frontiers of regenerative medicine. The transdifferentiating potential of stem cells varies with source and according to that regenerative applications also change. Advancements in gene editing and tissue engineering technology have endorsed the ex vivo remodelling of stem cells grown into 3D organoids and tissue structures for personalized applications. This review outlines the most recent advancement in transplantation and tissue engineering technologies of ESCs, TSPSCs, MSCs, UCSCs, BMSCs, and iPSCs in regenerative medicine. Additionally, this review also discusses stem cells regenerative application in wildlife conservation.

Regenerative medicine, the most recent and emerging branch of medical science, deals with functional restoration of specific tissue and/or organ of the patients suffering with severe injuries or chronic disease conditions, in the state where bodies own regenerative responses do not suffice [1]. In the present scenario donated tissues and organs cannot meet the transplantation demands of aged and diseased populations that have driven the thrust for search for the alternatives. Stem cells are endorsed with indefinite cell division potential, can transdifferentiate into other types of cells, and have emerged as frontline regenerative medicine source in recent time, for reparation of tissues and organs anomalies occurring due to congenital defects, disease, and age associated effects [1]. Stem cells pave foundation for all tissue and organ system of the body and mediates diverse role in disease progression, development, and tissue repair processes in host. On the basis of transdifferentiation potential, stem cells are of four types, that is, (1) unipotent, (2) multipotent, (3) pluripotent, and (4) totipotent [2]. Zygote, the only totipotent stem cell in human body, can give rise to whole organism through the process of transdifferentiation, while cells from inner cells mass (ICM) of embryo are pluripotent in their nature and can differentiate into cells representing three germ layers but do not differentiate into cells of extraembryonic tissue [2]. Stemness and transdifferentiation potential of the embryonic, extraembryonic, fetal, or adult stem cells depend on functional status of pluripotency factors like OCT4, cMYC, KLF44, NANOG, SOX2, and so forth [35]. Ectopic expression or functional restoration of endogenous pluripotency factors epigenetically transforms terminally differentiated cells into ESCs-like cells [3], known as induced pluripotent stem cells (iPSCs) [3, 4]. On the basis of regenerative applications, stem cells can be categorized as embryonic stem cells (ESCs), tissue specific progenitor stem cells (TSPSCs), mesenchymal stem cells (MSCs), umbilical cord stem cells (UCSCs), bone marrow stem cells (BMSCs), and iPSCs (Figure 1; Table 1). The transplantation of stem cells can be autologous, allogenic, and syngeneic for induction of tissue regeneration and immunolysis of pathogen or malignant cells. For avoiding the consequences of host-versus-graft rejections, tissue typing of human leucocyte antigens (HLA) for tissue and organ transplant as well as use of immune suppressant is recommended [6]. Stem cells express major histocompatibility complex (MHC) receptor in low and secret chemokine that recruitment of endothelial and immune cells is enabling tissue tolerance at graft site [6]. The current stem cell regenerative medicine approaches are founded onto tissue engineering technologies that combine the principles of cell transplantation, material science, and microengineering for development of organoid; those can be used for physiological restoration of damaged tissue and organs. The tissue engineering technology generates nascent tissue on biodegradable 3D-scaffolds [7, 8]. The ideal scaffolds support cell adhesion and ingrowths, mimic mechanics of target tissue, support angiogenesis and neovascularisation for appropriate tissue perfusion, and, being nonimmunogenic to host, do not require systemic immune suppressant [9]. Stem cells number in tissue transplant impacts upon regenerative outcome [10]; in that case prior ex vivo expansion of transplantable stem cells is required [11]. For successful regenerative outcomes, transplanted stem cells must survive, proliferate, and differentiate in site specific manner and integrate into host circulatory system [12]. This review provides framework of most recent (Table 1; Figures 18) advancement in transplantation and tissue engineering technologies of ESCs, TSPSCs, MSCs, UCSCs, BMSCs, and iPSCs in regenerative medicine. Additionally, this review also discusses stem cells as the tool of regenerative applications in wildlife conservation.

Promises of stem cells in regenerative medicine: the six classes of stem cells, that is, embryonic stem cells (ESCs), tissue specific progenitor stem cells (TSPSCs), mesenchymal stem cells (MSCs), umbilical cord stem cells (UCSCs), bone marrow stem cells (BMSCs), and induced pluripotent stem cells (iPSCs), have many promises in regenerative medicine and disease therapeutics.

Application of stem cells in regenerative medicine: stem cells (ESCs, TSPSCs, MSCs, UCSCs, BMSCs, and iPSCs) have diverse applications in tissue regeneration and disease therapeutics.

ESCs in regenerative medicine: ESCs, sourced from ICM of gastrula, have tremendous promises in regenerative medicine. These cells can differentiate into more than 200 types of cells representing three germ layers. With defined culture conditions, ESCs can be transformed into hepatocytes, retinal ganglion cells, chondrocytes, pancreatic progenitor cells, cone cells, cardiomyocytes, pacemaker cells, eggs, and sperms which can be used in regeneration of tissue and treatment of disease in tissue specific manner.

TSPSCs in regenerative medicine: tissue specific stem and progenitor cells have potential to differentiate into other cells of the tissue. Characteristically inner ear stem cells can be transformed into auditory hair cells, skin progenitors into vascular smooth muscle cells, mesoangioblasts into tibialis anterior muscles, and dental pulp stem cells into serotonin cells. The 3D-culture of TSPSCs in complex biomaterial gives rise to tissue organoids, such as pancreatic organoid from pancreatic progenitor, intestinal tissue organoids from intestinal progenitor cells, and fallopian tube organoids from fallopian tube epithelial cells. Transplantation of TSPSCs regenerates targets tissue such as regeneration of tibialis muscles from mesoangioblasts, cardiac tissue from AdSCs, and corneal tissue from limbal stem cells. Cell growth and transformation factors secreted by TSPSCs can change cells fate to become other types of cell, such that SSCs coculture with skin, prostate, and intestine mesenchyme transforms these cells from MSCs into epithelial cells fate.

MSCs in regenerative medicine: mesenchymal stem cells are CD73+, CD90+, CD105+, CD34, CD45, CD11b, CD14, CD19, and CD79a cells, also known as stromal cells. These bodily MSCs represented here do not account for MSCs of bone marrow and umbilical cord. Upon transplantation and transdifferentiation these bodily MSCs regenerate into cartilage, bones, and muscles tissue. Heart scar formed after heart attack and liver cirrhosis can be treated from MSCs. ECM coating provides the niche environment for MSCs to regenerate into hair follicle, stimulating hair growth.

UCSCs in regenerative medicine: umbilical cord, the readily available source of stem cells, has emerged as futuristic source for personalized stem cell therapy. Transplantation of UCSCs to Krabbe's disease patients regenerates myelin tissue and recovers neuroblastoma patients through restoring tissue homeostasis. The UCSCs organoids are readily available tissue source for treatment of neurodegenerative disease. Peritoneal fibrosis caused by long term dialysis, tendon tissue degeneration, and defective hyaline cartilage can be regenerated by UCSCs. Intravenous injection of UCSCs enables treatment of diabetes, spinal myelitis, systemic lupus erythematosus, Hodgkin's lymphoma, and congenital neuropathies. Cord blood stem cells banking avails long lasting source of stem cells for personalized therapy and regenerative medicine.

BMSCs in regenerative medicine: bone marrow, the soft sponge bone tissue that consisted of stromal, hematopoietic, and mesenchymal and progenitor stem cells, is responsible for blood formation. Even halo-HLA matched BMSCs can cure from disease and regenerate tissue. BMSCs can regenerate craniofacial tissue, brain tissue, diaphragm tissue, and liver tissue and restore erectile function and transdifferentiation monocytes. These multipotent stem cells can cure host from cancer and infection of HIV and HCV.

iPSCs in regenerative medicine: using the edge of iPSCs technology, skin fibroblasts and other adult tissues derived, terminally differentiated cells can be transformed into ESCs-like cells. It is possible that adult cells can be transformed into cells of distinct lineages bypassing the phase of pluripotency. The tissue specific defined culture can transform skin cells to become trophoblast, heart valve cells, photoreceptor cells, immune cells, melanocytes, and so forth. ECM complexation with iPSCs enables generation of tissue organoids for lung, kidney, brain, and other organs of the body. Similar to ESCs, iPSCs also can be transformed into cells representing three germ layers such as pacemaker cells and serotonin cells.

Stem cells in wildlife conservation: tissue biopsies obtained from dead and live wild animals can be either cryopreserved or transdifferentiated to other types of cells, through culture in defined culture medium or in vivo maturation. Stem cells and adult tissue derived iPSCs have great potential of regenerative medicine and disease therapeutics. Gonadal tissue procured from dead wild animals can be matured, ex vivo and in vivo for generation of sperm and egg, which can be used for assistive reproductive technology oriented captive breeding of wild animals or even for resurrection of wildlife.

For the first time in 1998, Thomson isolated human ESCs (hESCs) [13]. ESCs are pluripotent in their nature and can give rise to more than 200 types of cells and promises for the treatment of any kinds of disease [13]. The pluripotency fate of ESCs is governed by functional dynamics of transcription factors OCT4, SOX2, NANOG, and so forth, which are termed as pluripotency factors. The two alleles of the OCT4 are held apart in pluripotency state in ESCs; phase through homologues pairing during embryogenesis and transdifferentiation processes [14] has been considered as critical regulatory switch for lineage commitment of ESCs. The diverse lineage commitment potential represents ESCs as ideal model for regenerative therapeutics of disease and tissue anomalies. This section of review on ESCs discusses transplantation and transdifferentiation of ESCs into retinal ganglion, hepatocytes, cardiomyocytes, pancreatic progenitors, chondrocytes, cones, egg sperm, and pacemaker cells (Figure 2; Table 1). Infection, cancer treatment, and accidents can cause spinal cord injuries (SCIs). The transplantation of hESCs to paraplegic or quadriplegic SCI patients improves body control, balance, sensation, and limbal movements [15], where transplanted stem cells do homing to injury sites. By birth, humans have fixed numbers of cone cells; degeneration of retinal pigment epithelium (RPE) of macula in central retina causes age-related macular degeneration (ARMD). The genomic incorporation of COCO gene (expressed during embryogenesis) in the developing embryo leads lineage commitment of ESCs into cone cells, through suppression of TGF, BMP, and Wnt signalling pathways. Transplantation of these cone cells to eye recovers individual from ARMD phenomenon, where transplanted cone cells migrate and form sheet-like structure in host retina [16]. However, establishment of missing neuronal connection of retinal ganglion cells (RGCs), cones, and PRE is the most challenging aspect of ARMD therapeutics. Recently, Donald Z Jacks group at John Hopkins University School of Medicine has generated RGCs from CRISPER-Cas9-m-Cherry reporter ESCs [17]. During ESCs transdifferentiation process, CRIPER-Cas9 directs the knock-in of m-Cherry reporter into 3UTR of BRN3B gene, which is specifically expressed in RGCs and can be used for purification of generated RGCs from other cells [17]. Furthermore, incorporation of forskolin in transdifferentiation regime boosts generation of RGCs. Coaxing of these RGCs into biomaterial scaffolds directs axonal differentiation of RGCs. Further modification in RGCs generation regime and composition of biomaterial scaffolds might enable restoration of vision for ARMD and glaucoma patients [17]. Globally, especially in India, cardiovascular problems are a more common cause of human death, where biomedical therapeutics require immediate restoration of heart functions for the very survival of the patient. Regeneration of cardiac tissue can be achieved by transplantation of cardiomyocytes, ESCs-derived cardiovascular progenitors, and bone marrow derived mononuclear cells (BMDMNCs); however healing by cardiomyocytes and progenitor cells is superior to BMDMNCs but mature cardiomyocytes have higher tissue healing potential, suppress heart arrhythmias, couple electromagnetically into hearts functions, and provide mechanical and electrical repair without any associated tumorigenic effects [18, 19]. Like CM differentiation, ESCs derived liver stem cells can be transformed into Cytp450-hepatocytes, mediating chemical modification and catabolism of toxic xenobiotic drugs [20]. Even today, availability and variability of functional hepatocytes are a major a challenge for testing drug toxicity [20]. Stimulation of ESCs and ex vivo VitK12 and lithocholic acid (a by-product of intestinal flora regulating drug metabolism during infancy) activates pregnane X receptor (PXR), CYP3A4, and CYP2C9, which leads to differentiation of ESCs into hepatocytes; those are functionally similar to primary hepatocytes, for their ability to produce albumin and apolipoprotein B100 [20]. These hepatocytes are excellent source for the endpoint screening of drugs for accurate prediction of clinical outcomes [20]. Generation of hepatic cells from ESCs can be achieved in multiple ways, as serum-free differentiation [21], chemical approaches [20, 22], and genetic transformation [23, 24]. These ESCs-derived hepatocytes are long lasting source for treatment of liver injuries and high throughput screening of drugs [20, 23, 24]. Transplantation of the inert biomaterial encapsulated hESCs-derived pancreatic progenitors (CD24+, CD49+, and CD133+) differentiates into -cells, minimizing high fat diet induced glycemic and obesity effects in mice [25] (Table 1). Addition of antidiabetic drugs into transdifferentiation regime can boost ESCs conservation into -cells [25], which theoretically can cure T2DM permanently [25]. ESCs can be differentiated directly into insulin secreting -cells (marked with GLUT2, INS1, GCK, and PDX1) which can be achieved through PDX1 mediated epigenetic reprogramming [26]. Globally, osteoarthritis affects millions of people and occurs when cartilage at joints wears away, causing stiffness of the joints. The available therapeutics for arthritis relieve symptoms but do not initiate reverse generation of cartilage. For young individuals and athletes replacement of joints is not feasible like old populations; in that case transplantation of stem cells represents an alternative for healing cartilage injuries [27]. Chondrocytes, the cartilage forming cells derived from hESC, embedded in fibrin gel effectively heal defective cartilage within 12 weeks, when transplanted to focal cartilage defects of knee joints in mice without any negative effect [27]. Transplanted chondrocytes form cell aggregates, positive for SOX9 and collagen II, and defined chondrocytes are active for more than 12wks at transplantation site, advocating clinical suitability of chondrocytes for treatment of cartilage lesions [27]. The integrity of ESCs to integrate and differentiate into electrophysiologically active cells provides a means for natural regulation of heart rhythm as biological pacemaker. Coaxing of ESCs into inert biomaterial as well as propagation in defined culture conditions leads to transdifferentiation of ESCs to become sinoatrial node (SAN) pacemaker cells (PCs) [28]. Genomic incorporation TBox3 into ESCs ex vivo leads to generation of PCs-like cells; those express activated leukocyte cells adhesion molecules (ALCAM) and exhibit similarity to PCs for gene expression and immune functions [28]. Transplantation of PCs can restore pacemaker functions of the ailing heart [28]. In summary, ESCs can be transdifferentiated into any kinds of cells representing three germ layers of the body, being most promising source of regenerative medicine for tissue regeneration and disease therapy (Table 1). Ethical concerns limit the applications of ESCs, where set guidelines need to be followed; in that case TSPSCs, MSCs, UCSCs, BMSCs, and iPSCs can be explored as alternatives.

TSPSCs maintain tissue homeostasis through continuous cell division, but, unlike ESCs, TSPSCs retain stem cells plasticity and differentiation in tissue specific manner, giving rise to few types of cells (Table 1). The number of TSPSCs population to total cells population is too low; in that case their harvesting as well as in vitro manipulation is really a tricky task [29], to explore them for therapeutic scale. Human body has foundation from various types of TSPSCs; discussing the therapeutic application for all types is not feasible. This section of review discusses therapeutic application of pancreatic progenitor cells (PPCs), dental pulp stem cells (DPSCs), inner ear stem cells (IESCs), intestinal progenitor cells (IPCs), limbal progenitor stem cells (LPSCs), epithelial progenitor stem cells (EPSCs), mesoangioblasts (MABs), spermatogonial stem cells (SSCs), the skin derived precursors (SKPs), and adipose derived stem cells (AdSCs) (Figure 3; Table 1). During embryogenesis PPCs give rise to insulin-producing -cells. The differentiation of PPCs to become -cells is negatively regulated by insulin [30]. PPCs require active FGF and Notch signalling; growing more rapidly in community than in single cell populations advocates the functional importance of niche effect in self-renewal and transdifferentiation processes. In 3D-scaffold culture system, mice embryo derived PPCs grow into hollow organoid spheres; those finally differentiate into insulin-producing -cell clusters [29]. The DSPSCs, responsible for maintenance of teeth health status, can be sourced from apical papilla, deciduous teeth, dental follicle, and periodontal ligaments, have emerged as regenerative medicine candidate, and might be explored for treatment of various kinds of disease including restoration neurogenic functions in teeth [31, 32]. Expansion of DSPSCs in chemically defined neuronal culture medium transforms them into a mixed population of cholinergic, GABAergic, and glutaminergic neurons; those are known to respond towards acetylcholine, GABA, and glutamine stimulations in vivo. These transformed neuronal cells express nestin, glial fibrillary acidic protein (GFAP), III-tubulin, and voltage gated L-type Ca2+ channels [32]. However, absence of Na+ and K+ channels does not support spontaneous action potential generation, necessary for response generation against environmental stimulus. All together, these primordial neuronal stem cells have possible therapeutic potential for treatment of neurodental problems [32]. Sometimes, brain tumor chemotherapy can cause neurodegeneration mediated cognitive impairment, a condition known as chemobrain [33]. The intrahippocampal transplantation of human derived neuronal stem cells to cyclophosphamide behavioural decremented mice restores cognitive functions in a month time. Here the transplanted stem cells differentiate into neuronal and astroglial lineage, reduce neuroinflammation, and restore microglial functions [33]. Furthermore, transplantation of stem cells, followed by chemotherapy, directs pyramidal and granule-cell neurons of the gyrus and CA1 subfields of hippocampus which leads to reduction in spine and dendritic cell density in the brain. These findings suggest that transplantation of stem cells to cranium restores cognitive functions of the chemobrain [33]. The hair cells of the auditory system produced during development are not postmitotic; loss of hair cells cannot be replaced by inner ear stem cells, due to active state of the Notch signalling [34]. Stimulation of inner ear progenitors with -secretase inhibitor (LY411575) abrogates Notch signalling through activation of transcription factor atonal homologue 1 (Atoh1) and directs transdifferentiation of progenitors into cochlear hair cells [34]. Transplantation of in vitro generated hair cells restores acoustic functions in mice, which can be the potential regenerative medicine candidates for the treatment of deafness [34]. Generation of the hair cells also can be achieved through overexpression of -catenin and Atoh1 in Lrg5+ cells in vivo [35]. Similar to ear progenitors, intestine of the digestive tract also has its own tissue specific progenitor stem cells, mediating regeneration of the intestinal tissue [34, 36]. Dysregulation of the common stem cells signalling pathways, Notch/BMP/TGF-/Wnt, in the intestinal tissue leads to disease. Information on these signalling pathways [37] is critically important in designing therapeutics. Coaxing of the intestinal tissue specific progenitors with immune cells (macrophages), connective tissue cells (myofibroblasts), and probiotic bacteria into 3D-scaffolds of inert biomaterial, crafting biological environment, is suitable for differentiation of progenitors to occupy the crypt-villi structures into these scaffolds [36]. Omental implementation of these crypt-villi structures to dogs enhances intestinal mucosa through regeneration of goblet cells containing intestinal tissue [36]. These intestinal scaffolds are close approach for generation of implantable intestinal tissue, divested by infection, trauma, cancer, necrotizing enterocolitis (NEC), and so forth [36]. In vitro culture conditions cause differentiation of intestinal stem cells to become other types of cells, whereas incorporation of valproic acid and CHIR-99021 in culture conditions avoids differentiation of intestinal stem cells, enabling generation of indefinite pool of stem cells to be used for regenerative applications [38]. The limbal stem cells of the basal limbal epithelium, marked with ABCB5, are essential for regeneration and maintenance of corneal tissue [39]. Functional status of ABCB5 is critical for survival and functional integrity of limbal stem cells, protecting them from apoptotic cell death [39]. Limbal stem cells deficiency leads to replacement of corneal epithelium with visually dead conjunctival tissue, which can be contributed by burns, inflammation, and genetic factors [40]. Transplanted human cornea stem cells to mice regrown into fully functional human cornea, possibly supported by blood eye barrier phenomena, can be used for treatment of eye diseases, where regeneration of corneal tissue is critically required for vision restoration [39]. Muscle degenerative disease like duchenne muscular dystrophy (DMD) can cause extensive thrashing of muscle tissue, where tissue engineering technology can be deployed for functional restoration of tissue through regeneration [41]. Encapsulation of mouse or human derived MABs (engineered to express placental derived growth factor (PDGF)) into polyethylene glycol (PEG) fibrinogen hydrogel and their transplantation beneath the skin at ablated tibialis anterior form artificial muscles, which are functionally similar to those of normal tibialis anterior muscles [41]. The PDGF attracts various cell types of vasculogenic and neurogenic potential to the site of transplantation, supporting transdifferentiation of mesoangioblasts to become muscle fibrils [41]. The therapeutic application of MABs in skeletal muscle regeneration and other therapeutic outcomes has been reviewed by others [42]. One of the most important tissue specific stem cells, the male germline stem cells or spermatogonial stem cells (SSCs), produces spermatogenic lineage through mesenchymal and epithets cells [43] which itself creates niche effect on other cells. In vivo transplantation of SSCs with prostate, skin, and uterine mesenchyme leads to differentiation of these cells to become epithelia of the tissue of origin [43]. These newly formed tissues exhibit all physical and physiological characteristics of prostate and skin and the physical characteristics of prostate, skin, and uterus, express tissue specific markers, and suggest that factors secreted from SSCs lead to lineage conservation which defines the importance of niche effect in regenerative medicine [43]. According to an estimate, more than 100 million people are suffering from the condition of diabetic retinopathy, a progressive dropout of vascularisation in retina that leads to loss of vision [44]. The intravitreal injection of adipose derived stem cells (AdSCs) to the eye restores microvascular capillary bed in mice. The AdSCs from healthy donor produce higher amounts of vasoprotective factors compared to glycemic mice, enabling superior vascularisation [44]. However use of AdSCs for disease therapeutics needs further standardization for cell counts in dose of transplant and monitoring of therapeutic outcomes at population scale [44]. Apart from AdSCs, other kinds of stem cells also have therapeutic potential in regenerative medicine for treatment of eye defects, which has been reviewed by others [45]. Fallopian tubes, connecting ovaries to uterus, are the sites where fertilization of the egg takes place. Infection in fallopian tubes can lead to inflammation, tissue scarring, and closure of the fallopian tube which often leads to infertility and ectopic pregnancies. Fallopian is also the site where onset of ovarian cancer takes place. The studies on origin and etiology of ovarian cancer are restricted due to lack of technical advancement for culture of epithelial cells. The in vitro 3D organoid culture of clinically obtained fallopian tube epithelial cells retains their tissue specificity, keeps cells alive, which differentiate into typical ciliated and secretory cells of fallopian tube, and advocates that ectopic examination of fallopian tube in organoid culture settings might be the ideal approach for screening of cancer [46]. The sustained growth and differentiation of fallopian TSPSCs into fallopian tube organoid depend both on the active state of the Wnt and on paracrine Notch signalling [46]. Similar to fallopian tube stem cells, subcutaneous visceral tissue specific cardiac adipose (CA) derived stem cells (AdSCs) have the potential of differentiation into cardiovascular tissue [47]. Systemic infusion of CA-AdSCs into ischemic myocardium of mice regenerates heart tissue and improves cardiac function through differentiation to endothelial cells, vascular smooth cells, and cardiomyocytes and vascular smooth cells. The differentiation and heart regeneration potential of CA-AdSCs are higher than AdSCs [48], representing CA-AdSCs as potent regenerative medicine candidates for myocardial ischemic therapy [47]. The skin derived precursors (SKPs), the progenitors of dermal papilla/hair/hair sheath, give rise to multiple tissues of mesodermal and/or ectodermal origin such as neurons, Schwann cells, adipocytes, chondrocytes, and vascular smooth muscle cells (VSMCs). VSMCs mediate wound healing and angiogenesis process can be derived from human foreskin progenitor SKPs, suggesting that SKPs derived VSMCs are potential regenerative medicine candidates for wound healing and vasculature injuries treatments [49]. In summary, TSPSCs are potentiated with tissue regeneration, where advancement in organoid culture (Figure 3; Table 1) technologies defines the importance of niche effect in tissue regeneration and therapeutic outcomes of ex vivo expanded stem cells.

MSCs, the multilineage stem cells, differentiate only to tissue of mesodermal origin, which includes tendons, bone, cartilage, ligaments, muscles, and neurons [50]. MSCs are the cells which express combination of markers: CD73+, CD90+, CD105+, CD11b, CD14, CD19, CD34, CD45, CD79a, and HLA-DR, reviewed elsewhere [50]. The application of MSCs in regenerative medicine can be generalized from ongoing clinical trials, phasing through different state of completions, reviewed elsewhere [90]. This section of review outlines the most recent representative applications of MSCs (Figure 4; Table 1). The anatomical and physiological characteristics of both donor and receiver have equal impact on therapeutic outcomes. The bone marrow derived MSCs (BMDMSCs) from baboon are morphologically and phenotypically similar to those of bladder stem cells and can be used in regeneration of bladder tissue. The BMDMSCs (CD105+, CD73+, CD34, and CD45), expressing GFP reporter, coaxed with small intestinal submucosa (SIS) scaffolds, augment healing of degenerated bladder tissue within 10wks of the transplantation [51]. The combinatorial CD characterized MACs are functionally active at transplantation site, which suggests that CD characterization of donor MSCs yields superior regenerative outcomes [51]. MSCs also have potential to regenerate liver tissue and treat liver cirrhosis, reviewed elsewhere [91]. The regenerative medicinal application of MSCs utilizes cells in two formats as direct transplantation or first transdifferentiation and then transplantation; ex vivo transdifferentiation of MSCs deploys retroviral delivery system that can cause oncogenic effect on cells. Nonviral, NanoScript technology, comprising utility of transcription factors (TFs) functionalized gold nanoparticles, can target specific regulatory site in the genome effectively and direct differentiation of MSCs into another cell fate, depending on regime of TFs. For example, myogenic regulatory factor containing NanoScript-MRF differentiates the adipose tissue derived MSCs into muscle cells [92]. The multipotency characteristics represent MSCs as promising candidate for obtaining stable tissue constructs through coaxed 3D organoid culture; however heterogeneous distribution of MSCs slows down cell proliferation, rendering therapeutic applications of MSCs. Adopting two-step culture system for MSCs can yield homogeneous distribution of MSCs in biomaterial scaffolds. For example, fetal-MSCs coaxed in biomaterial when cultured first in rotating bioreactor followed with static culture lead to homogeneous distribution of MSCs in ECM components [7]. Occurrence of dental carries, periodontal disease, and tooth injury can impact individual's health, where bioengineering of teeth can be the alternative option. Coaxing of epithelial-MSCs with dental stem cells into synthetic polymer gives rise to mature teeth unit, which consisted of mature teeth and oral tissue, offering multiple regenerative therapeutics, reviewed elsewhere [52]. Like the tooth decay, both human and animals are prone to orthopedic injuries, affecting bones, joint, tendon, muscles, cartilage, and so forth. Although natural healing potential of bone is sufficient to heal the common injuries, severe trauma and tumor-recession can abrogate germinal potential of bone-forming stem cells. In vitro chondrogenic, osteogenic, and adipogenic potential of MSCs advocates therapeutic applications of MSCs in orthopedic injuries [53]. Seeding of MSCs, coaxed into biomaterial scaffolds, at defective bone tissue, regenerates defective bone tissues, within fourwks of transplantation; by the end of 32wks newly formed tissues integrate into old bone [54]. Osteoblasts, the bone-forming cells, have lesser actin cytoskeleton compared to adipocytes and MSCs. Treatment of MSCs with cytochalasin-D causes rapid transportation of G-actin, leading to osteogenic transformation of MSCs. Furthermore, injection of cytochalasin-D to mice tibia also promotes bone formation within a wk time frame [55]. The bone formation processes in mice, dog, and human are fundamentally similar, so outcomes of research on mice and dogs can be directional for regenerative application to human. Injection of MSCs to femur head of Legg-Calve-Perthes suffering dog heals the bone very fast and reduces the injury associated pain [55]. Degeneration of skeletal muscle and muscle cramps are very common to sledge dogs, animals, and individuals involved in adventurous athletics activities. Direct injection of adipose tissue derived MSCs to tear-site of semitendinosus muscle in dogs heals injuries much faster than traditional therapies [56]. Damage effect treatment for heart muscle regeneration is much more complex than regeneration of skeletal muscles, which needs high grade fine-tuned coordination of neurons with muscles. Coaxing of MSCs into alginate gel increases cell retention time that leads to releasing of tissue repairing factors in controlled manner. Transplantation of alginate encapsulated cells to mice heart reduces scar size and increases vascularisation, which leads to restoration of heart functions. Furthermore, transplanted MSCs face host inhospitable inflammatory immune responses and other mechanical forces at transplantation site, where encapsulation of cells keeps them away from all sorts of mechanical forces and enables sensing of host tissue microenvironment, and respond accordingly [57]. Ageing, disease, and medicine consumption can cause hair loss, known as alopecia. Although alopecia has no life threatening effects, emotional catchments can lead to psychological disturbance. The available treatments for alopecia include hair transplantation and use of drugs, where drugs are expensive to afford and generation of new hair follicle is challenging. Dermal papillary cells (DPCs), the specialized MSCs localized in hair follicle, are responsible for morphogenesis of hair follicle and hair cycling. The layer-by-layer coating of DPCs, called GAG coating, consists of coating of geletin as outer layer, middle layer of fibroblast growth factor 2 (FGF2) loaded alginate, and innermost layer of geletin. GAG coating creates tissue microenvironment for DPCs that can sustain immunological and mechanical obstacles, supporting generation of hair follicle. Transplantation of GAG-coated DPCs leads to abundant hair growth and maturation of hair follicle, where GAG coating serves as ECM, enhancing intrinsic therapeutic potential of DPCs [58]. During infection, the inflammatory cytokines secreted from host immune cells attract MSCs to the site of inflammation, which modulates inflammatory responses, representing MSCs as key candidate of regenerative medicine for infectious disease therapeutics. Coculture of macrophages (M) and adipose derived MSCs from Leishmania major (LM) susceptible and resistant mice demonstrates that AD-MSCs educate M against LM infection, differentially inducing M1 and M2 phenotype that represents AD-MSC as therapeutic agent for leishmanial therapy [93]. In summary, the multilineage differentiation potential of MSCs, as well as adoption of next-generation organoid culture system, avails MSCs as ideal regenerative medicine candidate.

Umbilical cord, generally thrown at the time of child birth, is the best known source for stem cells, procured in noninvasive manner, having lesser ethical constraints than ESCs. Umbilical cord is rich source of hematopoietic stem cells (HSCs) and MSCs, which possess enormous regeneration potential [94] (Figure 5; Table 1). The HSCs of cord blood are responsible for constant renewal of all types of blood cells and protective immune cells. The proliferation of HSCs is regulated by Musashi-2 protein mediated attenuation of Aryl hydrocarbon receptor (AHR) signalling in stem cells [95]. UCSCs can be cryopreserved at stem cells banks (Figure 5; Table 1), in operation by both private and public sector organization. Public stem cells banks operate on donation formats and perform rigorous screening for HLA typing and donated UCSCs remain available to anyone in need, whereas private stem cell banks operation is more personalized, availing cells according to donor consent. Stem cell banking is not so common, even in developed countries. Survey studies find that educated women are more eager to donate UCSCs, but willingness for donation decreases with subsequent deliveries, due to associated cost and safety concerns for preservation [96]. FDA has approved five HSCs for treatment of blood and other immunological complications [97]. The amniotic fluid, drawn during pregnancy for standard diagnostic purposes, is generally discarded without considering its vasculogenic potential. UCSCs are the best alternatives for those patients who lack donors with fully matched HLA typing for peripheral blood and PBMCs and bone marrow [98]. One major issue with UCSCs is number of cells in transplant, fewer cells in transplant require more time for engraftment to mature, and there are also risks of infection and mortality; in that case ex vivo propagation of UCSCs can meet the demand of desired outcomes. There are diverse protocols, available for ex vivo expansion of UCSCs, reviewed elsewhere [99]. Amniotic fluid stem cells (AFSCs), coaxed to fibrin (required for blood clotting, ECM interactions, wound healing, and angiogenesis) hydrogel and PEG supplemented with vascular endothelial growth factor (VEGF), give rise to vascularised tissue, when grafted to mice, suggesting that organoid cultures of UCSCs have promise for generation of biocompatible tissue patches, for treating infants born with congenital heart defects [59]. Retroviral integration of OCT4, KLF4, cMYC, and SOX2 transforms AFSCs into pluripotency stem cells known as AFiPSCs which can be directed to differentiate into extraembryonic trophoblast by BMP2 and BMP4 stimulation, which can be used for regeneration of placental tissues [60]. Wharton's jelly (WJ), the gelatinous substance inside umbilical cord, is rich in mucopolysaccharides, fibroblast, macrophages, and stem cells. The stem cells from UCB and WJ can be transdifferentiated into -cells. Homogeneous nature of WJ-SCs enables better differentiation into -cells; transplantation of these cells to streptozotocin induced diabetic mice efficiently brings glucose level to normal [7]. Easy access and expansion potential and plasticity to differentiate into multiple cell lineages represent WJ as an ideal candidate for regenerative medicine but cells viability changes with passages with maximum viable population at 5th-6th passages. So it is suggested to perform controlled expansion of WJ-MSCS for desired regenerative outcomes [9]. Study suggests that CD34+ expression leads to the best regenerative outcomes, with less chance of host-versus-graft rejection. In vitro expansion of UCSCs, in presence of StemRegenin-1 (SR-1), conditionally expands CD34+ cells [61]. In type I diabetic mellitus (T1DM), T-cell mediated autoimmune destruction of pancreatic -cells occurs, which has been considered as tough to treat. Transplantation of WJ-SCs to recent onset-T1DM patients restores pancreatic function, suggesting that WJ-MSCs are effective in regeneration of pancreatic tissue anomalies [62]. WJ-MSCs also have therapeutic importance for treatment of T2DM. A non-placebo controlled phase I/II clinical trial demonstrates that intravenous and intrapancreatic endovascular injection of WJ-MSCs to T2DM patients controls fasting glucose and glycated haemoglobin through improvement of -cells functions, evidenced by enhanced c-peptides and reduced inflammatory cytokines (IL-1 and IL-6) and T-cells counts [63]. Like diabetes, systematic lupus erythematosus (SLE) also can be treated with WJ-MSCs transplantation. During progression of SLE host immune system targets its own tissue leading to degeneration of renal, cardiovascular, neuronal, and musculoskeletal tissues. A non-placebo controlled follow-up study on 40 SLE patients demonstrates that intravenous infusion of WJ-MSC improves renal functions and decreases systematic lupus erythematosus disease activity index (SLEDAI) and British Isles Lupus Assessment Group (BILAG), and repeated infusion of WJ-MSCs protects the patient from relapse of the disease [64]. Sometimes, host inflammatory immune responses can be detrimental for HSCs transplantation and blood transfusion procedures. Infusion of WJ-MSC to patients, who had allogenic HSCs transplantation, reduces haemorrhage inflammation (HI) of bladder, suggesting that WJ-MSCs are potential stem cells adjuvant in HSCs transplantation and blood transfusion based therapies [100]. Apart from WJ, umbilical cord perivascular space and cord vein are also rich source for obtaining MSCs. The perivascular MSCs of umbilical cord are more primitive than WJ-MSCs and other MSCs from cord suggest that perivascular MSCs might be used as alternatives for WJ-MSCs for regenerative therapeutics outcome [101]. Based on origin, MSCs exhibit differential in vitro and in vivo properties and advocate functional characterization of MSCs, prior to regenerative applications. Emerging evidence suggests that UCSCs can heal brain injuries, caused by neurodegenerative diseases like Alzheimer's, Krabbe's disease, and so forth. Krabbe's disease, the infantile lysosomal storage disease, occurs due to deficiency of myelin synthesizing enzyme (MSE), affecting brain development and cognitive functions. Progression of neurodegeneration finally leads to death of babies aged two. Investigation shows that healing of peripheral nervous system (PNS) and central nervous system (CNS) tissues with Krabbe's disease can be achieved by allogenic UCSCs. UCSCs transplantation to asymptomatic infants with subsequent monitoring for 46 years reveals that UCSCs recover babies from MSE deficiency, improving myelination and cognitive functions, compared to those of symptomatic babies. The survival rate of transplanted UCSCs in asymptomatic and symptomatic infants was 100% and 43%, respectively, suggesting that early diagnosis and timely treatment are critical for UCSCs acceptance for desired therapeutic outcomes. UCSCs are more primitive than BMSCs, so perfect HLA typing is not critically required, representing UCSCs as an excellent source for treatment of all the diseases involving lysosomal defects, like Krabbe's disease, hurler syndrome, adrenoleukodystrophy (ALD), metachromatic leukodystrophy (MLD), Tay-Sachs disease (TSD), and Sandhoff disease [65]. Brain injuries often lead to cavities formation, which can be treated from neuronal parenchyma, generated ex vivo from UCSCs. Coaxing of UCSCs into human originated biodegradable matrix scaffold and in vitro expansion of cells in defined culture conditions lead to formation of neuronal organoids, within threewks' time frame. These organoids structurally resemble brain tissue and consisted of neuroblasts (GFAP+, Nestin+, and Ki67+) and immature stem cells (OCT4+ and SOX2+). The neuroblasts of these organoids further can be differentiated into mature neurons (MAP2+ and TUJ1+) [66]. Administration of high dose of drugs in divesting neuroblastoma therapeutics requires immediate restoration of hematopoiesis. Although BMSCs had been promising in restoration of hematopoiesis UCSCs are sparely used in clinical settings. A case study demonstrates that neuroblastoma patients who received autologous UCSCs survive without any associated side effects [12]. During radiation therapy of neoplasm, spinal cord myelitis can occur, although occurrence of myelitis is a rare event and usually such neurodegenerative complication of spinal cord occurs 624 years after exposure to radiations. Transplantation of allogenic UC-MSCs in laryngeal patients undergoing radiation therapy restores myelination [102]. For treatment of neurodegenerative disease like Alzheimer's disease (AD), amyotrophic lateral sclerosis (ALS), traumatic brain injuries (TBI), Parkinson's, SCI, stroke, and so forth, distribution of transplanted UCSCs is critical for therapeutic outcomes. In mice and rat, injection of UCSCs and subsequent MRI scanning show that transplanted UCSCs migrate to CNS and multiple peripheral organs [67]. For immunomodulation of tumor cells disease recovery, transplantation of allogenic DCs is required. The CD11c+DCs, derived from UCB, are morphologically and phenotypically similar to those of peripheral blood derived CTLs-DCs, suggesting that UCB-DCs can be used for personalized medicine of cancer patient, in need for DCs transplantation [103]. Coculture of UCSCs with radiation exposed human lung fibroblast stops their transdifferentiation, which suggests that factors secreted from UCSCs may restore niche identity of fibroblast, if they are transplanted to lung after radiation therapy [104]. Tearing of shoulder cuff tendon can cause severe pain and functional disability, whereas ultrasound guided transplantation of UCB-MSCs in rabbit regenerates subscapularis tendon in fourwks' time frame, suggesting that UCB-MSCs are effective enough to treat tendons injuries when injected to focal points of tear-site [68]. Furthermore, transplantation of UCB-MSCs to chondral cartilage injuries site in pig knee along with HA hydrogel composite regenerates hyaline cartilage [69], suggesting that UCB-MSCs are effective regenerative medicine candidate for treating cartilage and ligament injuries. Physiologically circulatory systems of brain, placenta, and lungs are similar. Infusion of UCB-MSCs to preeclampsia (PE) induced hypertension mice reduces the endotoxic effect, suggesting that UC-MSCs are potential source for treatment of endotoxin induced hypertension during pregnancy, drug abuse, and other kinds of inflammatory shocks [105]. Transplantation of UCSCs to severe congenital neutropenia (SCN) patients restores neutrophils count from donor cells without any side effect, representing UCSCs as potential alternative for SCN therapy, when HLA matched bone marrow donors are not accessible [106]. In clinical settings, the success of myocardial infarction (MI) treatment depends on ageing, systemic inflammation in host, and processing of cells for infusion. Infusion of human hyaluronan hydrogel coaxed UCSCs in pigs induces angiogenesis, decreases scar area, improves cardiac function at preclinical level, and suggests that the same strategy might be effective for human [107]. In stem cells therapeutics, UCSCs transplantation can be either autologous or allogenic. Sometimes, the autologous UCSCs transplants cannot combat over tumor relapse, observed in Hodgkin's lymphoma (HL), which might require second dose transplantation of allogenic stem cells, but efficacy and tolerance of stem cells transplant need to be addressed, where tumor replace occurs. A case study demonstrates that second dose allogenic transplants of UCSCs effective for HL patients, who had heavy dose in prior transplant, increase the long term survival chances by 30% [10]. Patients undergoing long term peritoneal renal dialysis are prone to peritoneal fibrosis and can change peritoneal structure and failure of ultrafiltration processes. The intraperitoneal (IP) injection of WJ-MSCs prevents methylglyoxal induced programmed cell death and peritoneal wall thickening and fibrosis, suggesting that WJ-MSCs are effective in therapeutics of encapsulating peritoneal fibrosis [70]. In summary, UCB-HSCs, WJ-MSCs, perivascular MSCs, and UCB-MSCs have tissue regeneration potential.

Bone marrow found in soft spongy bones is responsible for formation of all peripheral blood and comprises hematopoietic stem cells (producing blood cells) and stromal cells (producing fat, cartilage, and bones) [108] (Figure 6; Table 1). Visually bone marrow has two types, red marrow (myeloid tissue; producing RBC, platelets, and most of WBC) and yellow marrow (producing fat cells and some WBC) [108]. Imbalance in marrow composition can culminate to the diseased condition. Since 1980, bone marrow transplantation is widely accepted for cancer therapeutics [109]. In order to avoid graft rejection, HLA typing of donors is a must, but completely matched donors are limited to family members, which hampers allogenic transplantation applications. Since matching of all HLA antigens is not critically required, in that case defining the critical antigens for haploidentical allogenic donor for patients, who cannot find fully matched donor, might relieve from donor constraints. Two-step administration of lymphoid and myeloid BMSCs from haploidentical donor to the patients of aplastic anaemia and haematological malignancies reconstructs host immune system and the outcomes are almost similar to fully matched transplants, which recommends that profiling of critically important HLA is sufficient for successful outcomes of BMSCs transplantation. Haploidentical HLA matching protocol is the major process for minorities and others who do not have access to matched donor [71]. Furthermore, antigen profiling is not the sole concern for BMSCs based therapeutics. For example, restriction of HIV1 (human immune deficiency virus) infection is not feasible through BMSCs transplantation because HIV1 infection is mediated through CD4+ receptors, chemokine CXC motif receptor 4 (CXCR4), and chemokine receptor 5 (CCR5) for infecting and propagating into T helper (Th), monocytes, macrophages, and dendritic cells (DCs). Genetic variation in CCR2 and CCR5 receptors is also a contributory factor; mediating protection against infection has been reviewed elsewhere [110]. Engineering of hematopoietic stem and progenitor cells (HSPCs) derived CD4+ cells to express HIV1 antagonistic RNA, specifically designed for targeting HIV1 genome, can restrict HIV1 infection, through immune elimination of latently infected CD4+ cells. A single dose infusion of genetically modified (GM), HIV1 resistant HSPCs can be the alternative of HIV1 retroviral therapy. In the present scenario stem cells source, patient selection, transplantation-conditioning regimen, and postinfusion follow-up studies are the major factors, which can limit application of HIV1 resistant GM-HSPCs (CD4+) cells application in AIDS therapy [72, 73]. Platelets, essential for blood clotting, are formed from megakaryocytes inside the bone marrow [74]. Due to infection, trauma, and cancer, there are chances of bone marrow failure. To an extent, spongy bone marrow microenvironment responsible for lineage commitment can be reconstructed ex vivo [75]. The ex vivo constructed 3D-scaffolds consisted of microtubule and silk sponge, flooded with chemically defined organ culture medium, which mimics bone marrow environment. The coculture of megakaryocytes and embryonic stem cells (ESCs) in this microenvironment leads to generation of functional platelets from megakaryocytes [75]. The ex vivo 3D-scaffolds of bone microenvironment can stride the path for generation of platelets in therapeutic quantities for regenerative medication of burns [75] and blood clotting associated defects. Accidents, traumatic injuries, and brain stroke can deplete neuronal stem cells (NSCs), responsible for generation of neurons, astrocytes, and oligodendrocytes. Brain does not repopulate NSCs and heal traumatic injuries itself and transplantation of BMSCs also can heal neurodegeneration alone. Lipoic acid (LA), a known pharmacological antioxidant compound used in treatment of diabetic and multiple sclerosis neuropathy when combined with BMSCs, induces neovascularisation at focal cerebral injuries, within 8wks of transplantation. Vascularisation further attracts microglia and induces their colonization into scaffold, which leads to differentiation of BMSCs to become brain tissue, within 16wks of transplantation. In this approach, healing of tissue directly depends on number of BMSCs in transplantation dose [76]. Dental caries and periodontal disease are common craniofacial disease, often requiring jaw bone reconstruction after removal of the teeth. Traditional therapy focuses on functional and structural restoration of oral tissue, bone, and teeth rather than biological restoration, but BMSCs based therapies promise for regeneration of craniofacial bone defects, enabling replacement of missing teeth in restored bones with dental implants. Bone marrow derived CD14+ and CD90+ stem and progenitor cells, termed as tissue repair cells (TRC), accelerate alveolar bone regeneration and reconstruction of jaw bone when transplanted in damaged craniofacial tissue, earlier to oral implants. Hence, TRC therapy reduces the need of secondary bone grafts, best suited for severe defects in oral bone, skin, and gum, resulting from trauma, disease, or birth defects [77]. Overall, HSCs have great value in regenerative medicine, where stem cells transplantation strategies explore importance of niche in tissue regeneration. Prior to transplantation of BMSCs, clearance of original niche from target tissue is necessary for generation of organoid and organs without host-versus-graft rejection events. Some genetic defects can lead to disorganization of niche, leading to developmental errors. Complementation with human blastocyst derived primary cells can restore niche function of pancreas in pigs and rats, which defines the concept for generation of clinical grade human pancreas in mice and pigs [111]. Similar to other organs, diaphragm also has its own niche. Congenital defects in diaphragm can affect diaphragm functions. In the present scenario functional restoration of congenital diaphragm defects by surgical repair has risk of reoccurrence of defects or incomplete restoration [8]. Decellularization of donor derived diaphragm offers a way for reconstruction of new and functionally compatible diaphragm through niche modulation. Tissue engineering technology based decellularization of diaphragm and simultaneous perfusion of bone marrow mesenchymal stem cells (BM-MSCs) facilitates regeneration of functional scaffolds of diaphragm tissues [8]. In vivo replacement of hemidiaphragm in rats with reseeded scaffolds possesses similar myography and spirometry as it has in vivo in donor rats. These scaffolds retaining natural architecture are devoid of immune cells, retaining intact extracellular matrix that supports adhesion, proliferation, and differentiation of seeded cells [8]. These findings suggest that cadaver obtained diaphragm, seeded with BM-MSCs, can be used for curing patients in need for restoration of diaphragm functions (Figure 6; Table 1). However, BMSCs are heterogeneous population, which might result in differential outcomes in clinical settings; however clonal expansion of BMSCs yields homogenous cells population for therapeutic application [8]. One study also finds that intracavernous delivery of single clone BMSCs can restore erectile function in diabetic mice [112] and the same strategy might be explored for adult human individuals. The infection of hepatitis C virus (HCV) can cause liver cirrhosis and degeneration of hepatic tissue. The intraparenchymal transplantation of bone marrow mononuclear cells (BMMNCs) into liver tissue decreases aspartate aminotransferase (AST), alanine transaminase (ALT), bilirubin, CD34, and -SMA, suggesting that transplanted BMSCs restore hepatic functions through regeneration of hepatic tissues [113]. In order to meet the growing demand for stem cells transplantation therapy, donor encouragement is always required [8]. The stem cells donation procedure is very simple; with consent donor gets an injection of granulocyte-colony stimulating factor (G-CSF) that increases BMSCs population. Bone marrow collection is done from hip bone using syringe in 4-5hrs, requiring local anaesthesia and within a wk time frame donor gets recovered donation associated weakness.

The field of iPSCs technology and research is new to all other stem cells research, emerging in 2006 when, for the first time, Takahashi and Yamanaka generated ESCs-like cells through genetic incorporation of four factors, Sox2, Oct3/4, Klf4, and c-Myc, into skin fibroblast [3]. Due to extensive nuclear reprogramming, generated iPSCs are indistinguishable from ESCs, for their transcriptome profiling, epigenetic markings, and functional competence [3], but use of retrovirus in transdifferentiation approach has questioned iPSCs technology. Technological advancement has enabled generation of iPSCs from various kinds of adult cells phasing through ESCs or direct transdifferentiation. This section of review outlines most recent advancement in iPSC technology and regenerative applications (Figure 7; Table 1). Using the new edge of iPSCs technology, terminally differentiated skin cells directly can be transformed into kidney organoids [114], which are functionally and structurally similar to those of kidney tissue in vivo. Up to certain extent kidneys heal themselves; however natural regeneration potential cannot meet healing for severe injuries. During kidneys healing process, a progenitor stem cell needs to become 20 types of cells, required for waste excretion, pH regulation, and restoration of water and electrolytic ions. The procedure for generation of kidney organoids ex vivo, containing functional nephrons, has been identified for human. These ex vivo kidney organoids are similar to fetal first-trimester kidneys for their structure and physiology. Such kidney organoids can serve as model for nephrotoxicity screening of drugs, disease modelling, and organ transplantation. However generation of fully functional kidneys is a far seen event with today's scientific technologies [114]. Loss of neurons in age-related macular degeneration (ARMD) is the common cause of blindness. At preclinical level, transplantation of iPSCs derived neuronal progenitor cells (NPCs) in rat limits progression of disease through generation of 5-6 layers of photoreceptor nuclei, restoring visual acuity [78]. The various approaches of iPSCs mediated retinal regeneration including ARMD have been reviewed elsewhere [79]. Placenta, the cordial connection between mother and developing fetus, gets degenerated in certain pathophysiological conditions. Nuclear programming of OCT4 knock-out (KO) and wild type (WT) mice fibroblast through transient expression of GATA3, EOMES, TFAP2C, and +/ cMYC generates transgene independent trophoblast stem-like cells (iTSCs), which are highly similar to blastocyst derived TSCs for DNA methylation, H3K7ac, nucleosome deposition of H2A.X, and other epigenetic markings. Chimeric differentiation of iTSCs specifically gives rise to haemorrhagic lineages and placental tissue, bypassing pluripotency phase, opening an avenue for generation of fully functional placenta for human [115]. Neurodegenerative disease like Alzheimer's and obstinate epilepsies can degenerate cerebrum, controlling excitatory and inhibitory signals of the brain. The inhibitory tones in cerebral cortex and hippocampus are accounted by -amino butyric acid secreting (GABAergic) interneurons (INs). Loss of these neurons often leads to progressive neurodegeneration. Genomic integration of Ascl1, Dlx5, Foxg1, and Lhx6 to mice and human fibroblast transforms these adult cells into GABAergic-INs (iGABA-INs). These cells have molecular signature of telencephalic INs, release GABA, and show inhibition to host granule neuronal activity [81]. Transplantation of these INs in developing embryo cures from genetic and acquired seizures, where transplanted cells disperse and mature into functional neuronal circuits as local INs [82]. Dorsomorphin and SB-431542 mediated inhibition of TGF- and BMP signalling direct transformation of human iPSCs into cortical spheroids. These cortical spheroids consisted of both peripheral and cortical neurons, surrounded by astrocytes, displaying transcription profiling and electrophysiology similarity with developing fetal brain and mature neurons, respectively [83]. The underlying complex biology and lack of clear etiology and genetic reprogramming and difficulty in recapitulation of brain development have barred understanding of pathophysiology of autism spectrum disorder (ASD) and schizophrenia. 3D organoid cultures of ASD patient derived iPSC generate miniature brain organoid, resembling fetal brain few months after gestation. The idiopathic conditions of these organoids are similar with brain of ASD patients; both possess higher inhibitory GABAergic neurons with imbalanced neuronal connection. Furthermore these organoids express forkhead Box G1 (FOXG1) much higher than normal brain tissue, which explains that FOXG1 might be the leading cause of ASD [84]. Degeneration of other organs and tissues also has been reported, like degeneration of lungs which might occur due to tuberculosis infection, fibrosis, and cancer. The underlying etiology for lung degeneration can be explained through organoid culture. Coaxing of iPSC into inert biomaterial and defined culture leads to formation of lung organoids that consisted of epithelial and mesenchymal cells, which can survive in culture for months. These organoids are miniature lung, resemble tissues of large airways and alveoli, and can be used for lung developmental studies and screening of antituberculosis and anticancer drugs [87]. The conventional multistep reprogramming for iPSCs consumes months of time, while CRISPER-Cas9 system based episomal reprogramming system that combines two steps together enables generation of ESCs-like cells in less than twowks, reducing the chances of culture associated genetic abrasions and unwanted epigenetic [80]. This approach can yield single step ESCs-like cells in more personalized way from adults with retinal degradation and infants with severe immunodeficiency, involving correction for genetic mutation of OCT4 and DNMT3B [80]. The iPSCs expressing anti-CCR5-RNA, which can be differentiated into HIV1 resistant macrophages, have applications in AIDS therapeutics [88]. The diversified immunotherapeutic application of iPSCs has been reviewed elsewhere [89]. The -1 antitrypsin deficiency (A1AD) encoded by serpin peptidase inhibitor clade A member 1 (SERPINA1) protein synthesized in liver protects lungs from neutrophils elastase, the enzyme causing disruption of lungs connective tissue. A1AD deficiency is common cause of both lung and liver disease like chronic obstructive pulmonary disease (COPD) and liver cirrhosis. Patient specific iPSCs from lung and liver cells might explain pathophysiology of A1AD deficiency. COPD patient derived iPSCs show sensitivity to toxic drugs which explains that actual patient might be sensitive in similar fashion. It is known that A1AD deficiency is caused by single base pair mutation and correction of this mutation fixes the A1AD deficiency in hepatic-iPSCs [85]. The high order brain functions, like emotions, anxiety, sleep, depression, appetite, breathing heartbeats, and so forth, are regulated by serotonin neurons. Generation of serotonin neurons occurs prior to birth, which are postmitotic in their nature. Any sort of developmental defect and degeneration of serotonin neurons might lead to neuronal disorders like bipolar disorder, depression, and schizophrenia-like psychiatric conditions. Manipulation of Wnt signalling in human iPSCs in defined culture conditions leads to an in vitro differentiation of iPSCs to serotonin-like neurons. These iPSCs-neurons primarily localize to rhombomere 2-3 segment of rostral raphe nucleus, exhibit electrophysiological properties similar to serotonin neurons, express hydroxylase 2, the developmental marker, and release serotonin in dose and time dependent manner. Transplantation of these neurons might cure from schizophrenia, bipolar disorder, and other neuropathological conditions [116]. The iPSCs technology mediated somatic cell reprogramming of ventricular monocytes results in generation of cells, similar in morphology and functionality with PCs. SA note transplantation of PCs to large animals improves rhythmic heart functions. Pacemaker needs very reliable and robust performance so understanding of transformation process and site of transplantation are the critical aspect for therapeutic validation of iPSCs derived PCs [28]. Diabetes is a major health concern in modern world, and generation of -cells from adult tissue is challenging. Direct reprogramming of skin cells into pancreatic cells, bypassing pluripotency phase, can yield clinical grade -cells. This reprogramming strategy involves transformation of skin cells into definitive endodermal progenitors (cDE) and foregut like progenitor cells (cPF) intermediates and subsequent in vitro expansion of these intermediates to become pancreatic -cells (cPB). The first step is chemically complex and can be understood as nonepisomal reprogramming on day one with pluripotency factors (OCT4, SOX2, KLF4, and hair pin RNA against p53), then supplementation with GFs and chemical supplements on day seven (EGF, bFGF, CHIR, NECA, NaB, Par, and RG), and two weeks later (Activin-A, CHIR, NECA, NaB, and RG) yielding DE and cPF [86]. Transplantation of cPB yields into glucose stimulated secretion of insulin in diabetic mice defines that such cells can be explored for treatment of T1DM and T2DM in more personalized manner [86]. iPSCs represent underrated opportunities for drug industries and clinical research laboratories for development of therapeutics, but safety concerns might limit transplantation applications (Figure 7; Table 1) [117]. Transplantation of human iPSCs into mice gastrula leads to colonization and differentiation of cells into three germ layers, evidenced with clinical developmental fat measurements. The acceptance of human iPSCs by mice gastrula suggests that correct timing and appropriate reprogramming regime might delimit human mice species barrier. Using this fact of species barrier, generation of human organs in closely associated primates might be possible, which can be used for treatment of genetic factors governed disease at embryo level itself [118]. In summary, iPSCs are safe and effective for treatment of regenerative medicine.

The unstable growth of human population threatens the existence of wildlife, through overexploitation of natural habitats and illegal killing of wild animals, leading many species to face the fate of being endangered and go for extinction. For wildlife conservation, the concept of creation of frozen zoo involves preservation of gene pool and germ plasm from threatened and endangered species (Figure 8). The frozen zoo tissue samples collection from dead or live animal can be DNA, sperms, eggs, embryos, gonads, skin, or any other tissue of the body [119]. Preserved tissue can be reprogrammed or transdifferentiated to become other types of tissues and cells, which opens an avenue for conservation of endangered species and resurrection of life (Figure 8). The gonadal tissue from young individuals harbouring immature tissue can be matured in vivo and ex vivo for generation of functional gametes. Transplantation of SSCs to testis of male from the same different species can give rise to spermatozoa of donor cells [120], which might be used for IVF based captive breeding of wild animals. The most dangerous fact in wildlife conservation is low genetic diversity, too few reproductively capable animals which cannot maintain adequate genetic diversity in wild or captivity. Using the edge of iPSC technology, pluripotent stem cells can be generated from skin cells. For endangered drill, Mandrillus leucophaeus, and nearly extinct white rhinoceros, Ceratotherium simum cottoni, iPSC has been generated in 2011 [121]. The endangered animal drill (Mandrillus leucophaeus) is genetically very close to human and often suffers from diabetes, while rhinos are genetically far removed from other primates. The progress in iPSCs, from the human point of view, might be transformed for animal research for recapturing reproductive potential and health in wild animals. However, stem cells based interventions in wild animals are much more complex than classical conservation planning and biomedical research has to face. Conversion of iPSC into egg or sperm can open the door for generation of IVF based embryo; those might be transplanted in womb of live counterparts for propagation of population. Recently, iPSCs have been generated for snow leopard (Panthera uncia), native to mountain ranges of central Asia, which belongs to cat family; this breakthrough has raised the possibilities for cryopreservation of genetic material for future cloning and other assisted reproductive technology (ART) applications, for the conservation of cat species and biodiversity. Generation of leopard iPSCs has been achieved through retroviral-system based genomic integration of OCT4, SOX2, KLF4, cMYC, and NANOG. These iPSCs from snow leopard also open an avenue for further transformation of iPSCs into gametes [122]. The in vivo maturation of grafted tissue depends both on age and on hormonal status of donor tissue. These facts are equally applicable to accepting host. Ectopic xenografts of cryopreserved testis tissue from Indian spotted deer (Moschiola indica) to nude mice yielded generation of spermatocytes [123], suggesting that one-day procurement of functional sperm from premature tissue might become a general technique in wildlife conservation. In summary, tissue biopsies from dead or live animals can be used for generation of iPSCs and functional gametes; those can be used in assisted reproductive technology (ART) for wildlife conservation.

The spectacular progress in the field of stem cells research represents great scope of stem cells regenerative therapeutics. It can be estimated that by 2020 or so we will be able to produce wide array of tissue, organoid, and organs from adult stem cells. Inductions of pluripotency phenotypes in terminally differentiated adult cells have better therapeutic future than ESCs, due to least ethical constraints with adult cells. In the coming future, there might be new pharmaceutical compounds; those can activate tissue specific stem cells, promote stem cells to migrate to the side of tissue injury, and promote their differentiation to tissue specific cells. Except few countries, the ongoing financial and ethical hindrance on ESCs application in regenerative medicine have more chance for funding agencies to distribute funding for the least risky projects on UCSCs, BMSCs, and TSPSCs from biopsies. The existing stem cells therapeutics advancements are more experimental and high in cost; due to that application on broad scale is not feasible in current scenario. In the near future, the advancements of medical science presume using stem cells to treat cancer, muscles damage, autoimmune disease, and spinal cord injuries among a number of impairments and diseases. It is expected that stem cells therapies will bring considerable benefits to the patients suffering from wide range of injuries and disease. There is high optimism for use of BMSCs, TSPSCs, and iPSCs for treatment of various diseases to overcome the contradictions associated with ESCs. For advancement of translational application of stem cells, there is a need of clinical trials, which needs funding rejoinder from both public and private organizations. The critical evaluation of regulatory guidelines at each phase of clinical trial is a must to comprehend the success and efficacy in time frame.

Dr. Anuradha Reddy from Centre for Cellular and Molecular Biology Hyderabad and Mrs. Sarita Kumari from Department of Yoga Science, BU, Bhopal, India, are acknowledged for their critical suggestions and comments on paper.

Embryonic stem cells

Tissue specific progenitor stem cells

Umbilical cord stem cells

Bone marrow stem cells

Induced pluripotent stem cells

Mesenchymal stem cells

Wharton's jelly mesenchymal stem cells

Hematopoietic stem cells

Retinal ganglion cells

Type I diabetes mellitus

Type 2 diabetes mellitus

-1 antitrypsin deficiency

Chronic obstructive pulmonary disease

Human leukocyte antigen

Major histocompatibility complex

Three-dimensional

Spinal cord injury

Age-related macular degeneration

Retinal pigment epithelium

Pregnane X receptor

Dental pulp stem cells

Glial fibrillary acidic protein

Activation of transcription factor atonal homologue 1

Necrotizing enterocolitis

Duchene muscular dystrophy

Placental derived growth factor

Polyethylene glycol

Spermatogonial stem cells

Adipose derived stem cells

Hematopoietic stem cells

Amniotic fluid stem cells

Vascular endothelial growth factor

Umbilical cord blood

Systematic lupus erythematosus (SLE) disease activity index

Human immunodeficiency virus-1

Genetically modified hematopoietic stem and progenitor cells

T helper

Lipoic acid

Tissue repair cells

Bone marrow mesenchymal stem cells

Peripheral blood stem cells

Granulocyte-colony stimulating factor

Serpin peptidase inhibitor clade A member 1

Autism spectrum disorder

Interneurons

-amino butyric acid secreting

Neuronal progenitor cells

Independent trophoblast stem-like cells

Human cortical spheroids

Cardiomyocytes

Adrenoleukodystrophy

Metachromatic leukodystrophy

Tay-Sachs disease

Amyotrophic lateral sclerosis

Traumatic brain injuries

Alzheimer's disease

Neuronal stem cells

Severe immune deficiency.

There are no competing interests associated with this paper.

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Navigating the hope and hype of regenerative medicine

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March 27, 2020

Regenerative medicine is the process of creating living, functional tissues to repair or replace tissue or organ function that is lost due to age, disease, damage or congenital defects. Mayo Clinic is careful to give patients a realistic picture of what they can expect from regenerative medicine treatments for orthopedic conditions.

Before patients receive orthobiologics at Mayo Clinic in Jacksonville, Florida, they visit the Regenerative Medicine Consult Service, part of the Mayo Clinic Center for Regenerative Biotherapeutics. There they meet with a clinical consultant who has expertise in regenerative medicine and the patients' specific conditions.

"We explain which orthobiologics we use, what the science shows about them and what outcomes we are seeing. We tell patients to please understand that regenerative medicine treatments aren't necessarily cures or substitutes for surgery," says Shane A. Shapiro, M.D., a medical orthopedist and medical director of the Regenerative Medicine Therapeutics Program at Mayo Clinic's campus in Florida. "When we educate patients, they are better able to make decisions that are right for them and their orthopedic conditions."

This effort exemplifies Mayo's commitment to evidence-based care at a time when orthobiologics are aggressively marketed to consumers and health care providers.

"Unfortunately, the field has proliferated in a way that is not always backed up by science," Dr. Shapiro says. "The excitement around regenerative medicine and stem cells has consumed both the public and even care providers who don't have the background in molecular or stem cell biology to understand what is real and what is entirely false or misleading about these therapies."

Patients' visits to the Regenerative Medicine Consult Service include medical evaluations to determine whether orthobiologics are appropriate. Misinformation about the unapproved stem cell therapy marketplace also can be corrected.

"For some patients this is an eye-opening experience, as they have received inaccurate information from websites and other sources," Dr. Shapiro says. "Infomercials disguised as educational seminars for the public are widespread. In our meetings with patients, we take care not to overemphasize the medical benefits and also to acknowledge any risks of orthobiologics."

Patients who qualify and opt for orthobiologics are treated in the Regenerative Medicine Suites, a novel, multidisciplinary surgical hybrid procedure facility for cell therapy applications. The suites are equipped for regulatory-compliant cell harvest, application, storage, receiving and quality oversight. Mayo Clinic offers procedures that involve the patient's own cells from blood, adipose tissue or bone marrow which are minimally processed and returned to the patient within the same surgical procedure. All clinical trials using orthobiologics are monitored by the FDA.

"Patients may experience relief of pain and improvement in function for up to a year or longer. But most procedures should not be considered a cure," Dr. Shapiro says. "All would likely need to be repeated over time with some exceptions, such as procedures in younger patients with tendinopathies, in which cures are certainly possible." Biologic therapy is also regularly combined with best practices such as activity modification, bracing and physical therapy.

Close

Illustration shows the injection of platelet-rich plasma, one of the biologic therapies offered at Mayo Clinic.

Among the orthobiologics offered at Mayo Clinic is platelet-rich plasma, which uses the patient's own platelets and growth factors to promote musculoskeletal healing. In recent years the protocols for this therapy have been refined and standardized, leading to more consistently positive results.

"We are seeing a significant clinically beneficial effect to using platelet-rich plasma in tendinopathies, as a surgical adjunct to rotator cuff repair and as pain relief for knee arthritis," Dr. Shapiro says.

Mayo Clinic also offers newer treatments using cells derived from patients' adipose tissue or bone marrow. Notably, bone marrow aspirate concentrate therapy achieved positive results in a Mayo Clinic study of patients with osteonecrosis of the femoral head. As described in the February 2018 issue of Clinical Orthopaedics and Related Research, patients with corticosteroid-induced osteonecrosis had bone marrow-derived stem cells and platelet-rich plasma injected into the femoral head after hip decompression. More than 90% of the 35 hips treated in the preliminary series avoided collapse at a minimum of two years after surgery.

"We don't necessarily view any of these first-generation orthobiologics blood, adipose tissue or bone marrow as definitely better than standard-of-care orthopedic surgery," Dr. Shapiro says. "For example, patients with severe knee arthritis are probably still best served with knee replacement surgery. But for patients who aren't good candidates for knee replacements, and haven't responded to physical therapy or to steroid or hyaluronic acid injections, orthobiologics can fill that treatment gap."

Photograph shows the outcomes registry tablet used by Mayo Clinic patients to track their self-reported outcomes after visits to the Regenerative Medicine Therapeutics Program.

After visiting the Regenerative Medicine Consult Service, about 10% of patients opt for a cell-based therapy, 25% choose platelet-rich plasma therapy, and the remaining 65% stick with standard-of-care steroid injection, physical therapy or surgery. Whichever approach patients choose, Mayo Clinic tracks treatment outcomes using validated patient-reported measures.

Additional research is underway to refine orthobiologic treatments. Dr. Shapiro is conducting a randomized clinical trial comparing therapy with adipose-derived stromal vascular fraction cells to a saline placebo for the treatment of knee arthritis. That trial builds on previously conducted randomized controlled trials, including a study published in the October 2019 issue of Cartilage. Orthopedic surgeons at Mayo Clinic in Rochester, Minnesota, have undertaken a trial of a stem cell technique, known as RECLAIM, to repair knee cartilage.

"We recognize that our first-generation orthobiologics just scratch the surface in terms of using cells to treat orthopedic disease. The future of orthopedic cell therapy is going to require much more sophisticated versions of these cell therapies," Dr. Shapiro says. "Treatment using orthobiologics that's not based in sound orthopedic science is not likely to help people. Mayo Clinic is committed to advancing the science of regenerative medicine, to harness its potential and to provide evidence-based treatments for patients."

Houdek MT, et al. Stem cells combined with platelet-rich plasma effectively treat corticosteroid-induced osteonecrosis of the hip: A prospective study. Clinical Orthopaedics and Related Research. 2018;476:388.

Shapiro SA, et al. Quantitative T2 MRI mapping and 12-month follow-up in a randomized, blinded, placebo controlled trial of bone marrow aspiration and concentration for osteoarthritis of the knees. Cartilage. 2019;10:432.

Originally posted here:
Navigating the hope and hype of regenerative medicine

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Cell and Gene Therapy Investment Ticks Up After Hard Few Years – BioSpace

Monday, October 14th, 2024

Cell and Gene Therapy Investment Ticks Up After Hard Few Years  BioSpace

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Cell and Gene Therapy Investment Ticks Up After Hard Few Years - BioSpace

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Crackdowns on Unproven Stem Cell Therapies Worked Abroad – Medpage Today

Monday, October 14th, 2024

Crackdowns on Unproven Stem Cell Therapies Worked Abroad  Medpage Today

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Crackdowns on Unproven Stem Cell Therapies Worked Abroad - Medpage Today

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How Regenerative Medicine can help you get out of pain without surgery – WJLA

Monday, October 14th, 2024

How Regenerative Medicine can help you get out of pain without surgery  WJLA

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How Regenerative Medicine can help you get out of pain without surgery - WJLA

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Regenity Biosciences Receives 510(k) Clearance for RejuvaKnee, a Groundbreaking Regenerative Meniscus Implant Device to Redefine the Standard of Care…

Monday, October 14th, 2024

Regenity Biosciences Receives 510(k) Clearance for RejuvaKnee, a Groundbreaking Regenerative Meniscus Implant Device to Redefine the Standard of Care  OrthoSpineNews

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Regenity Biosciences Receives 510(k) Clearance for RejuvaKnee, a Groundbreaking Regenerative Meniscus Implant Device to Redefine the Standard of Care...

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Buy, Sell, Hold: Cell and Gene Therapy – BioPharm International

Monday, October 14th, 2024

Buy, Sell, Hold: Cell and Gene Therapy  BioPharm International

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Buy, Sell, Hold: Cell and Gene Therapy - BioPharm International

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Mayo Clinic offers unique regenerative medicine procedure for knee and …

Friday, September 13th, 2024

Aug. 29, 2023

This Q&A features Daniel B. F. Saris, M.D., Ph.D., an orthopedic surgeon specializing in knee surgery with a focus on cell-based surgical regenerative medicine at Mayo Clinic's campus in Minnesota. Here, he explains a regenerative medicine procedure for joint restoration that he believes addresses an unmet need. Dr. Saris discusses its background and future, and appropriate referral candidates.

A team of Mayo Clinic orthopedic and regenerative medicine researchers has continued development and testing of a knee joint restoration procedure, called recycled cartilage auto/allo implantation (RECLAIM). I brought RECLAIM with me from the University Medical Center Utrecht in the Netherlands, where we developed this procedure and called it IMPACT.

In this procedure, we debride the patient's knee defect. We remove cartilage from the knee or hip, mincing these pieces into smaller fragments and extracting cartilage cells through chemical digestion to the level of the chondron. We combine these recycled autologous chondrons with allogeneic donor mesenchymal stem cells (MSCs). The mixture of 10% to 20% of the patient's cells with 80% to 90% MSCs is placed into fibrin glue, which allows the surgeon to inject them into the patient's knee defect. This procedure enables the patient's body to repair the cartilage defect, something it otherwise would be unable to do.

RECLAIM is a one-stage innovative procedure for hip and knee that enables tissue growth and restoration of cartilage in the patient's joint. Within one year, the defect is filled. DNA analysis has shown this to be patient-derived new cartilage tissue without donor DNA remaining. I see it as the MSCs providing both immune modulatory signals as well as growth factor, reminding the cartilage to grow. Ultimately, RECLAIM may help preserve the joint by filling the "pothole" for a better "drive."

We have learned that combining native cartilage cells and allogeneic MSCs can be a good partnership. We consider the transplant successful if the joint is still viable in 13 to 20 years.

A depiction of the steps in the process of recycled cartilage auto/allo implantation (RECLAIM) knee cartilage regeneration.

[This animation shows RECLAIM knee cartilage regeneration. It is playing with no audio.]

RECLAIM for hip and knee is performed under FDA scrutiny as an investigational new drug in a phase 1 trial I led with a team of Mayo Clinic investigators, and it is not yet widely available. The trial began in September 2018 and ends in September 2024.

Indications for this therapy are precise. The patient must meet the following criteria:

Often, these cartilage defects are from trauma or athletic injury.

One of my biggest drivers is improving quality of life. People need to move in their lives and they need their joints to work. Patients' alternatives are usually to deal with discomfort or quit sports. We want to help them return to sports or their pre-injury lifestyles.

I am also passionate about helping patients with arthritis, one of the biggest quality-of-life threats.

My research team specifically is seeking solutions to treat defects in young patients with active lifestyles. This is a growing group, and age limits are changing. Someday, if people live to age 120, we need joint preservation solutions for individuals ages 30 to 60 and older.

We hope it will work with other joints, but that has not been studied yet. The need seems greatest for hip and knee, but we would like to explore hand, ankle, elbow and others.

We also hope RECLAIM will apply to the meniscus. We have a Ph.D. program working on that potential application.

Aaron J. Krych, M.D., an orthopedic surgeon at Mayo Clinic in Minnesota, is leading a phase 1 RECLAIM study in the hip joint. It's open for patient enrollment. We are doing a randomized controlled trial in the Netherlands for permission to enter this as standard of care.

Lucienne Vonk, Ph.D., and I developed the idea from the first experiments through completing the initial human trials. Dr. Vonk serves as a senior researcher in the Department of Orthopaedics, University Medical Center Utrecht, the Netherlands, and director of musculoskeletal diseases at Xintela AB, a biomedical company in Sweden. As we were working with RECLAIM in the Netherlands, evidence and international enthusiasm grew. It was showing promise. Mayo Clinic orthopedic and regenerative medicine leadership gave us the opportunity to continue developing RECLAIM using Mayo Clinic's stem cell bank and conduct U.S. RECLAIM clinical trials.

Also important to me was that Mayo Clinic had orthopedic surgeons who could perform the RECLAIM procedure and that Mayo had the brand respect needed to make a clinical trial happen in the U.S.

First, we will take good care of your patients. Second, it is a cell-based cartilage repair in a single surgical procedure and only available at Mayo Clinic in Minnesota in the U.S. Outside of the United States, it's also available at University Medical Center Utrecht.

If patients have cartilage defects, say, in the knee, they often have pain and swelling clinically, and the defect can be visible on MRI. Mayo Clinic has a specialized cartilage clinic. In the knee clinic, we jointly analyze those injuries with the whole team to develop one-visit solutions.

Mayo Clinic also has world leaders in orthopedic injectable therapy if our experts deem injectables best for patients' injuries.

We also have significant multidisciplinary expertise available at Mayo Clinic and have numerous clinical trials to offer.

If you have a question regarding sending a patient to Mayo Clinic, contact knee@mayo.edu or cartilage@mayo.edu.

We attempted a moonshot effort to put all elements of this procedure into one arthroscopic surgery, an important goal for our team. To now see that come to fruition after some years is exciting and rewarding for the team, and hopefully it is a valuable improvement for our patients.

Ultimately, we want RECLAIM to be available widely for many patients and to be able to apply this cell-cell combination for other joint challenges and even other organs.

Clinical trials: REcycled CartiLage Auto/Allo Implantation. Mayo Clinic.

Refer a patient to Mayo Clinic.

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Mayo Clinic offers unique regenerative medicine procedure for knee and ...

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Regenerative Medicine to the Rescue – Cleveland Clinic

Friday, September 13th, 2024

For Kevin Kelley, the bad news came out of nowhere. I woke up one morning, he recalls, and it felt like somebody had stuffed half a banana under the left side of my jaw. The IT data security analyst from the Cleveland suburb of Rocky River, Ohio, considered himself to be in good health, aside from the hypertension that ran in his family and a recent pulmonary embolism that was successfully treated. A competitive swimmer, he swam a couple of miles almost every day, either in Lake Erie or in a pool.

A biopsy of Kelleys swollen gland revealed an aggressive form of non-Hodgkins lymphoma, a malignant cancer that originates in the lymphatic system, a network of vessels, tissues and organs that helps remove toxins and waste from our bodies.

To fight the disease, Kelley and his oncologist, Brian Hill, MD, PhD, of Cleveland Clinic, turned to regenerative medicine not once, but twice. His case is compelling because it highlights where regenerative medicine has been and where regenerative medicine is heading, says Dr. Hill, Director of the Lymphoid Malignancies Program in Taussig Cancer Institute.

Kelley received a bone marrow transplant and CAR-T cell therapy. Bone marrow transplants, which have been used for decades, transfer healthy blood-forming cells into a person with blood cancer. CAR-T cell therapy, which the Food and Drug Administration initially approved in 2017, modifies a patients own immune cells to kill cancer cells.

First, though, Kelley underwent six cycles of chemotherapy. Through it all, he continued to swim as often as he could. His care team even timed the treatments so he and his new bride, Karen, could enjoy a Grand Cayman honeymoon.

Unfortunately, a few months later, a biopsy showed that Kelley wasnt cancer-free. The next step was a bone marrow transplant, immediately preceded by more chemotherapy. Very high doses of chemotherapy are delivered with the intention of eliminating the lymphoma, Dr. Hill says. In the process, though, the patients bone marrow is eradicated, too. So you have to collect their bone marrow ahead of time and then give it back to them after the chemotherapy.

In Kelleys case, the transplant was autologous, meaning he was his own donor. (Allogeneic transplants entail a matched donor.) During the transplant, more than 100 million hematopoietic stem cells were delivered directly into his bloodstream through a special type of IV. For good measure, a chaplain blessed the cells beforehand, at Kelleys request. I figured every little bit helps, he says.

Like salmon swimming upstream to spawn, the cells knew where to go and what to do when they got there, regenerating healthy marrow in the bones.

For Kelley, the road to recovery included a three-week stay in the hospital. After another month of rest at home, he began swimming again, slowly but surely regaining strength. He was declared in remission, although the respite was short-lived. Less than a year after the bone marrow transplant, a scan showed new activity. A lymph node biopsy confirmed it: The lymphoma was back.

Kelley didnt hesitate when Dr. Hill recommended a new line of attack: CAR-T cell therapy. To get the ball rolling, T cells which are white blood cells were collected from Kelley through a procedure called leukapheresis. The T cells were then shipped off to a lab, where they were genetically altered. New chimeric antigen receptors (CAR for short) on the surface of the T cells would allow them to carry out a seek-and-destroy mission against cancer cells. In the meantime, Kelley had another course of chemotherapy. When the manufactured CAR-T cells were ready, hundreds of millions of them were infused into his bloodstream. After a week in the hospital, he was back home and on the mend.

With CAR-T cell therapy, instead of just hammering away at the cancer cells with traditional chemotherapy drugs that poison the cells, the idea is to invoke the power of the bodys own immune response to attack the cancer, Dr. Hill says.

By way of an explanation, Kelley offers an analogy that any fan of old-school video games will appreciate: Suddenly, your body is playing Pac-Man. Once those manufactured T cells are put in you, theyre on the hunt. When they find a cancer cell, they destroy it. Theyre just gobbling it up.

CAR-T cell therapy isnt without side effects, which can include flu-like symptoms as well as neurologic events that can result in confusion. Nonetheless, this particular form of regenerative medicine shows great promise. Im very optimistic for the future of this treatment approach, Dr. Hill says.

As for Kelley, hes back in remission. He plans to swim in a couple of upcoming 8-mile, open-water races: one in the Florida Keys and one around Mackinac Island in Michigan. The latter will be a fundraiser for the Leukemia & Lymphoma Society.

I feel great, Kelley says. Now its time to go have some fun.

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Regenerative Medicine to the Rescue - Cleveland Clinic

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Regenerative medicine applications: An overview of clinical trials

Friday, September 13th, 2024

Abstract

Insights into the use of cellular therapeutics, extracellular vesicles (EVs), and tissue engineering strategies for regenerative medicine applications are continually emerging with a focus on personalized, patient-specific treatments. Multiple pre-clinical and clinical trials have demonstrated the strong potential of cellular therapies, such as stem cells, immune cells, and EVs, to modulate inflammatory immune responses and promote neoangiogenic regeneration in diseased organs, damaged grafts, and inflammatory diseases, including COVID-19. Over 5,000 registered clinical trials on ClinicalTrials.gov involve stem cell therapies across various organs such as lung, kidney, heart, and liver, among other applications. A vast majority of stem cell clinical trials have been focused on these therapies safety and effectiveness. Advances in our understanding of stem cell heterogeneity, dosage specificity, and ex vivo manipulation of stem cell activity have shed light on the potential benefits of cellular therapies and supported expansion into clinical indications such as optimizing organ preservation before transplantation. Standardization of manufacturing protocols of tissue-engineered grafts is a critical first step towards the ultimate goal of whole organ engineering. Although various challenges and uncertainties are present in applying cellular and tissue engineering therapies, these fields prospect remains promising for customized patient-specific treatments. Here we will review novel regenerative medicine applications involving cellular therapies, EVs, and tissue-engineered constructs currently investigated in the clinic to mitigate diseases and possible use of cellular therapeutics for solid organ transplantation. We will discuss how these strategies may help advance the therapeutic potential of regenerative and transplant medicine.

Keywords: regenerative medicine, stem cells, extracellular vesicles, COVID-19, tissue engineering, transplantation, bioengineering

Regenerative medicine focuses on replenishing and repairing tissue or organs impaired by disease, trauma, or congenital issues. Cellular therapies, conditioned media, extracellular vesicles (EVs), and seeded cellular patches are promising therapeutic tools to combat various inflammatory conditions and diseases. A large body of pre-clinical research has shown that stem cell therapies can delay disease onset within multiple organs such as the kidney (Sedrakyan et al., 2012; Urt-Filho et al., 2016; Frank and Petrosyan, 2020), lung (Mei et al., 2007; Zhen et al., 2008, 2010; Garcia et al., 2013; Xu et al., 2018), heart (Wang et al., 2015; Galipeau et al., 2016; Miteva et al., 2017), and liver (Gilsanz et al., 2017; Tsuchiya et al., 2019) through immunomodulatory and paracrine mechanisms. Conditioned media and EVs derived from stem cells also demonstrate similar characteristics (Lener et al., 2015; Nassar et al., 2016; Bruno et al., 2017; Riazifar et al., 2017; Sedrakyan et al., 2017; Grange et al., 2019). Mesenchymal stromal cells (mesenchymal stem cells; MSCs), which are used mainly in clinical trials, have a potent self-renewal and differentiation capacity into multi-lineages and may be isolated from various adult tissues such as bone marrow (BM), adipose tissue, and fetal specimens (amniotic fluid and umbilical cord). Cellular therapies are also investigated for transplant medicine with the hopes of repairing marginal organs, minimizing ischemia-reperfusion injury (IRI), and inducing immune tolerance in solid organ transplantation (Leventhal et al., 2016; Sawitzki et al., 2020). In addition to stem cell therapies, immune cell therapies that specifically isolate and enrich anti-inflammatory immune cells are also investigated as a promising regenerative medicine tool towards treating inflammation, promoting tissue regeneration, and enhancing transplant tolerance (Zwang and Leventhal, 2017). Currently, clinicians and scientists have begun providing novel insights into optimizing cellular therapy in the clinical setting to provide a more deliverable, sustained, and impactful clinical benefit to patients (Okano and Sipp, 2020). However, further studies with larger patient cohorts are needed to show the efficacy of cellular therapies, conditioned media, extracellular vesicles (EVs), and seeded cellular patches for regenerative medicine. Here we will review results obtained from current clinical trials and novel cellular therapeutic options investigated towards clinical use. We will discuss how these findings and current novel techniques may help advance the potential therapeutic effects of cellular transplantations, EVs, and tissue-engineered constructs for regenerative medicine and transplantation.

Promising pre-clinical research studies have shown the potential of multipotent mesenchymal stem cells (MSCs) transplantation as a regenerative medicine therapy option (Vu et al., 2014; Wang et al., 2021). Currently, the U.S. Food and Drug Administration (FDA) has approved a small set of therapies for clinical use (). Clinical trials have focused on using MSCs immunomodulatory, immunosuppressive, and regenerative potentials with hopes of treating chronic diseases and immune resetting of autoimmune disorders (). MSCs immunoregulatory properties are attributed to their secretion of numerous cytokines (anti-inflammatory factors: iNOS, IDO, PGE2, TSG6, HO1 and galectins, cytokines: TGF, IL-10, CCL2, IL-6 and IL-7, chemokines: IL-6, CXCR3, CCR5, CCL5, CXCL9-11) and putative angiogenic proteins (VEGF, PDGF, TGF) (Shi et al., 2018). The Mesenchymal and Tissue Stem Cell Committee of the International Society for Cellular Therapy (ISCT) has set standards to define multipotent mesenchymal stromal cells (MSC) for both laboratory-based scientific investigations and pre-clinical studies (Dominici et al., 2006). Three guidelines must be met for the designation of MSC. Firstly, MSC must be plastic-adherent (tissue culture flasks) in cultured under standard conditions. Secondly, MSC (measured by flow cytometry) must have specific surface antigen (Ag) expression (95% expression of CD105, CD73 and CD90, with absence (5/2%) in expression of CD45, CD34, CD14 or CD11b, CD79a or CD19 and HLA class II). Thirdly, MSC must exhibit differentiation capabilities towards osteoblasts, adipocytes, and chondroblasts under standard in vitro differentiating conditions. Not all published clinical trials have adhered to these guidelines, limiting our ability to compare and contrast study outcomes and hindering the fields progression ().

A list of cellular and tissue engineered products with the proposed treatments currently FDA approved. All of the approved cellular products are hematopoietic progenitor cell derived from Cord Blood approved for disorders affecting the hematopoietic system. The tissue engineered scaffolds are allowed for the treatment of mucogingival conditions, cartilage defects of the knee, and thermal burns.

A list of clinical trials using regenerative medicine applications. Each trial is identified by disease reference, patient gender, method of treatment, outcome, and International Society for Cellular Therapy Criteria Check (1, 2, 3). 1) MSC must be plastic-adherent when maintained in standard culture conditions. 2) MSC must express CD105, CD73 and CD90, and lack expression of CD45, CD34, CD14 or CD11b, CD79alpha or CD19 and HLA-DR surface molecules. 3) MSC must differentiate to osteoblasts, adipocytes and chondroblasts in vitro. Most clinical trials using MSC appeared to have the 1st and 2nd criteria mentioned, and a large difference was noted between the trials regarding cell number, type, from of transplantation, and culture conditions. Such variation allows for the identification of different forms of effect per experimental group but shows little consistency in the trials performed. Thus, it would be beneficial if clinical trials followed a clearer guideline with minor changes per experimental group to understand better the applicability and efficacy of cellular and tissue engineered therapies.

In current clinical trials, similar to pre-clinical data, clinical administration of cellular therapies has shown angiogenic properties (active secretion of proangiogenic factors) and anti-inflammatory effects (reduced expression of pro-inflammatory markers and T cell proliferation) (Saad et al., 2017; Ye et al., 2017; Zhang et al., 2017). The angiogenic properties of autologous adipose tissue-derived MSCs are attributed to significantly increasing renal tissue oxygenation, cortical blood flow, and stabilizing glomerular filtration rates (GFR) up to 3months in patients with the atherosclerotic renovascular disease (RVD) (Saad et al., 2017). The anti-inflammatory effects of autologous hematopoietic stem cells are predicted to be beneficial for patients with type 1 diabetes mellitus by lowering the proportion of white blood cells, lymphocytes, T-cell proliferation, and pro-inflammatory cytokine production (Ye et al., 2017). Similarly, anti-inflammatory properties of allogeneic umbilical cord-derived MSCs, show improvements in patients with systemic sclerosis-associated, with better skin thickness scores, lung function, significantly decrease in anti-Scl70 autoantibody titers, and reduction of pro-inflammatory cytokine levels (including transforming growth factor- (TGF-) and vascular endothelial growth factor (VEGF) levels in serum) (Zhang et al., 2017). Although clinical trials show promising results for MSC use in the clinic, there are limitations in MSCs scalability, interdonor variability, clinical trial outcomes inconsistency, low engraftment rates, variation in immunomodulatory response, and potential regenerative limitations (Tanavde et al., 2015). Recently, induced pluripotent stem cells (iPSCs) derived MSCs (CPY-001) are shown to be safe and well-tolerated in a limited number of patients with steroid-resistant acute graft versus host disease (Bloor et al., 2020). This trial demonstrates for the first time, the possible applicability of iPSC-derived MSCs for a range of other clinical targets that may overcome the fundamental limitations of conventional, donor-derived MSC production processes. Although current clinical trials exhibit similar and limited anti-inflammatory beneficial effects with MSC treatments like previous pre-clinical trials, there is a large variation between each trial. Variations such as cell culture conditions, cell number transplantation, from of transplantation, cell type, and characterization limited the interpretation of each trial. Additional studies with larger cohorts are also needed to address the efficacy of cellular therapeutics in regenerative medicine.

MSCs preconditioned with either recombinant proteins, drugs, or ex-vivo cell culture conditions and techniques are also investigated to enhance their therapeutic potential before transplantation (). One form of enhancement strategy applied for cardiac regenerative cell therapy is using a guided cardiopoiesis approach to deliver BM-MSCs expanded and processed for lineage specification to derive cardiopoietic cells. In a Phase III Congestive Heart Failure Cardiopoietic Regenerative Therapy (CHART-1) clinical trial, cardiopoietic stem cells were delivered via the endomyocardial route with a retention-enhanced catheter to patients with ischemic heart failure (Bartunek et al., 2017). However, after thirty-nine weeks, the primary outcome was neutral, except for a subset of patients with severe heart enlargement that appeared to have had a consistent beneficial effect. The results suggest that cardiopoietic cell treatment beneficial outcomes may vary depending on the type of cardiac damage present in patients. Another alternative method used to enhance MSC regenerative potential aside from preconditioning the cells with recombinant growth factors, cytokines, or drugs is the use of environmental stimuli, such as hypoxia. Preconditioned MSCs under chronic hypoxic conditions (itMSC) show enhanced immunomodulatory properties when transplanted in non-ischemic cardiomyopathy patients (Butler et al., 2017). After 90 days, the administration of itMSCs was associated with a reduced number of natural killer cells, and the magnitude of this reduction was correlated with improved left ventricular ejection fraction (Butler et al., 2017). However, a single injection of itMSC was not efficient in promoting significant cardiac structural or functional improvements, highlighting the need to investigate the efficacy of serial dosing of intravenously administered itMSCs to promote a sustained immunomodulatory effect along with structural and functional improvements in the clinic. Thus, clinicians have also carried out studies identifying how different dosages of stem cells and numbers of injections (transplants) may dictate their therapeutic potential. In the TRIDENT Study, Florea et al. have demonstrated in patients with ischemic cardiomyopathy that there are different beneficial outcomes when patients are administered either 20 million or 100 million allogeneic MSC via transendocardial injection (Florea et al., 2017). Both groups showed improvement in scar formation; however, improved ejection fraction was noted only in patients receiving 100 million cells. The authors stated that although the two doses of allogeneic MSC are safe for patients, it is crucial to design trials to evaluate optimal dosing for cell-based therapies. Clinical trials have also begun to understand how different cell types produce better results than single-cell transplantation. In pre-clinical studies (Park K.-S. et al., 2019), have recently demonstrated that delivering both cardiomyocytes derived from human induced pluripotent stem cells (hiPSC-CMs) and human mesenchymal stem cell-loaded patch (hMSC-PA) to rats with myocardial infractions can amplify cardiac repair with enhanced vascular regeneration and improved cellular retention and engraftment (Park S.-J. et al., 2019). The combinatory cell delivery can also be applied to organ transplantations to enhance/preserve newly transplanted partial organ engraftment. Benomar et al. demonstrated that patients who were transplanted with pancreatic tissue comprising more than 50% of non-islet cells (likely enriched in ductal, acinar, and MSCs) had a statistically significant lower level of hemoglobin A1c and lower daily requirement of insulin even 5years after transplantation, compared to those who received islet transplant with more than 50% tissue purity (Benomar et al., 2018); thus, suggesting that non-endocrine cells have a beneficial effect on long-term islet graft metabolic function. The authors identified elevated expression of CA19-9 generally synthesized by pancreatic ductal cells and hypothesized that ductal cells must have been transplanted and continued to proliferate and contributed to the beneficial outcomes. These findings bring forth an important concept, the need to transplant multiple cell types for better long-term engraftment and function. These results suggest and warrant further investigation into the understanding and application of methods to enhance the therapeutic potential of MSC, either through improved cell culture techniques, the route of delivery, dosage specificity, or a combination of various cell types to further amplify their regenerative potential.

Current therapies are also designed to mobilize patients tissue-specific progenitor cells using various bioactive molecules such as growth factors, cytokines, and hormones to enhance endogenous regeneration. Activation of endogenous stem cells to promote regeneration or repair holds great promise for the future of translational medicine (Xia et al., 2018). Ansheles et al. demonstrated that using statins (Atorvastatin therapy) in patients with coronary heart disease could significantly increase the pool of endothelial progenitor cells by 72% in 3months (Ansheles et al., 2017). Patients also displayed a significant decrease in VEGF expression and various metabolic markers such as C-reactive protein, total cholesterol, LDL cholesterol, and triglycerides. Pantin et al. also investigated how to enhance endothelial cell mobilization from patients following allogeneic transplantation to sustain donor-derived hematopoiesis (Pantin et al., 2017). They identified that a high-dose (480mg/kg) Plerixafor is safe and effective in mobilizing CD31 expressing cells in healthy donors. These studies highlight the use of molecules to enhance tissue regeneration and restoration in disease by activating endogenous resident cells without the need for exogenous cellular infusions.

Cell-to-cell communication is vital to control wound healing and modulate chronic and acute diseases via paracrine signaling. Cells communicate via the secretion of numerous extracellular vesicles (EVs) which are a heterogeneous population and ranging from 40nm to a few mm in size under physiological and pathophysiological conditions. EV populations most widely studied and characterized are exosomes (derived from intracellular endosomal compartments and range from 30 to 120nm in diameter), microvesicles (also known as shedding vesicles are non-apoptotic EVs that originate from the plasma membrane and range from 50 to 1,000nm in diameter), and apoptotic bodies (originate from cells undergoing apoptosis and range from 50 to 2,000nm). Multiple pre-clinical studies have demonstrated that conditioned media of cultured stem cells and stem cell EVs show beneficial effects on various diseases (Lener et al., 2015; Bruno et al., 2017; Riazifar et al., 2017; Nguyen et al., 2020). The discovery of exosomes, microvesicles, and apoptotic bodies within the conditioned media has led to a new avenue of research exploring EVs for clinical use. Using EVs, most of the therapeutic effects of stem cells can be achieved with a reduced risk associated with live-cell injection late effects, such as neoplastic transformation and immune response activation (Nassar et al., 2016; Wang et al., 2017; Guo et al., 2020). A limited number of clinical trials have investigated EVs therapeutic potential in patients with cancer (Morse et al., 2005; Dai et al., 2008) and disease (Nassar et al., 2016). In chronic kidney disease patients (), EVs isolated from umbilical cord MSCs were shown to be safe and potentially effective in modulating the inflammatory immune reaction (Nassar et al., 2016). Patients who were given two doses of MSC-EVs showed improved eGFR, serum creatinine level, blood urea, and urinary albumin-creatinine ratio, possibly due to a significant plasma level increase in TGF-1 and IL-10 with a decrease in plasma levels of inflammatory cytokine, TNF-. Although patients saw a vast improvement after two dosages of therapy at 8weeks to 9months, the improvements were not sustained after 9months, and an additional administration of the EV might be needed (Nassar et al., 2016).

Further studies are also necessary to clarify fundamental questions regarding the generation, origin of isolation (body fluids: plasma, serum, blood, amniotic fluid, cell lines: MSCs, progenitor cells, IPSCs distribution, tissue derived) (Crescitelli et al., 2021) and uptake of EVs and how to scale up to cGMP manufacturing and improve associated quality control and batch tracking methods for the clinic (Riazifar et al., 2017). Another issue brought forth by the International Society for Extracellular Vesicles is the general lack of proper characterization of the different forms of EVs used in pre-clinical and clinical trials as each type contains different cargos and may promote different effects (Thry et al., 2018). There are currently multiple clinical trials initiated and recruiting patients to investigate EVs application in various diseased organs such as lung, liver, kidney, and heart. The potential use of EVs as a regenerative medicine therapeutic option is vast and promising. There are currently no FDA-approved EV products.

Cellular therapeutics have also been applied ex vivo to improve and recondition donor organ quality before transplantations. Thompson et al. show how ex vivo delivery of multipotent adult progenitor cells via normothermic machine perfusion in kidneys deemed un-transplantable prompted improved clinically relevant parameters (urine output, decreased expression of injury biomarker NGAL, improved microvascular perfusion) and decreased neutrophil recruitment and pro-inflammatory cytokines (downregulation of interleukin (IL)-1, upregulation of IL-10 and Indolamine-2, 3-dioxygenase) (Thompson et al., 2020). Brasile et al. also show how 24h ex vivo perfusion of MSC in an Exsanguinous Metabolic Support tissue-engineering can accelerate the repair of ischemic damage in human kidneys. Promoting regeneration identified by the increased synthesis of ATP (both in the renal cortex and medulla), a reduced inflammatory response (TNF-, RANTES, IL1-B, IL6), increased synthesis of growth factors (EGF, FGF-2, and TGF-), normalization of the cytoskeleton (ZO-1 expressed exclusively at the plasma membrane) and increased cellular proliferation (higher expression of PCNA and mitosis) (Brasile et al., 2019). The authors suggest a more prolonged warm reperfusion of a donors kidney may further improve and repair tubule damages attained from severe ischemic insult. The potential of MSCs to prevent or decrease injuries due to ischemia-reperfusion to further improve organ preservation has also been shown in various organs such as the lung (La Francesca et al., 2014; Lu et al., 2015), liver (Laing et al., 2020), and heart (Yano et al., 2018). Thus, these techniques involving reperfusion using various cell types provide a new avenue to significantly expanding donor criteria to offset current donor shortages. Future studies directed towards identifying the precise reperfusion media, the extent of reperfusion time, and the most suitable cell source can further enhance these techniques applicability in the clinic.

COVID-19, the disease attributed to the novel SARS-CoV-2 coronavirus, has given rise to a global pandemic. Although many patients do well, some present fever, dyspnea, hypoxia, and even exhibit moderate-to-severe acute respiratory distress syndrome (ARDS). This group of patients typically require intubation, which is associated with high mortality rates (up to 67%94%) (King et al., 2020). The detrimental effect of COVID-19 that causes multiple organ failure and even death is correlated with the presentation of a cytokine storm, which is identified as a maladaptive release of cytokines (Brodin, 2021). Elevated expression of inflammatory cytokines such as IL-1B, IFN-, IP-10, and monocyte chemoattractant protein 1 (MCP-1) detected in patients with COVID-19 is linked with Th1 cell response (Ye et al., 2020). Currently, MSC and their EVs are considered as a potential therapeutic option against COVID-19 (). MSC has the innate capacity to promote anti-inflammatory and immune regulatory functions by directly inhibiting abnormal activation of T lymphocytes and macrophages, pro-inflammatory cytokines, and secreting anti-inflammatory cytokines and growth factors such as IL-10 and VEGF to stimulate regeneration and repair. There are currently 16 clinical trials completed with over one thousand studies listed on ClinicalTrials.gov on the use of stem cells or stem cell exosomes to treat coronavirus-related injuries, such as acute kidney and lung injury and various inflammatory processes. Non-randomized case studies, phase 1 and phase 2 clinical trials have shown that human umbilical cord-derived mesenchymal stem cell (UC-MSCs) infusions in patients with moderate and severe COVID-19 pulmonary disease is safe and well-tolerated (Liang et al., 2020; Meng et al., 2020; Shu et al., 2020; Hashemian et al., 2021; Shi et al., 2021). A phase 1 and phase 2 clinical trial with limited patients shows that administration of UC-MSCs or clinical-grade MSCs may help reduce inflammatory cytokines (TNF-, IFN-, IL6, IL8, C-reactive protein) and promote lung recovery in surviving patients (Liang et al., 2020; Hashemian et al., 2021; Shi et al., 2021). Intravenous injection of clinical-grade MSCs (lacking ACE-2 receptor and TMPRSS2) led to increased levels of anti-inflammatory cytokine IL-10, and the normalized presence of immune cells. The patients presented an increase of peripheral lymphocytes, a decrease in C-reactive protein (CRP), a reduced activated cytokine-secreting immune cells (CXCR3+CD4+T-cells, CXCR3+CD8+Tcells, and CXCR3+NK-cells), and a restored levels of regulatory DC cell population (CD14+CD11c+CD11bmodregulatory DC cell) (Leng et al., 2020). The use of MSC with the absence of ACE-2 receptor and TMPRSS2 to prevent infection with SARS-Cov-2 may have enhanced the therapeutic effects of MSCs.

There are currently multiple studies listed on ClinicalTrials.gov on the use of EVs to treat COVID-19. Sengupta et al. show that a single dose of intravenous infusion of exosomes derived from BM-MSC (ExoFloTM) in patients presenting moderate-to-severe ARDS helps restore oxygenation, reduces the cytokine storm, to bring back a healthy immune system with no adverse effects (Sengupta et al., 2020). The authors state that exosomes may be used as a preventative measure against progression to invasive oxygen support and mechanical ventilation, which is associated with a high mortality rate. Further studies with randomized controlled trials (RCTs) are warranted to prove efficacy and address what type of EVs and what dosage of EVs are needed to treat COVID-19 patients. A short-term (84days) Phase 1 clinical trial of twenty-seven COVID-19 patients with pulmonary fibrosis treated with human embryonic stem cell-derived immunity and matrix-regulatory cells, which poses high expression of proliferative, immunomodulatory and anti-fibrotic genes, also show improvements in clinical symptoms (Wu et al., 2020). Additional multicenter randomized placebo-controlled Phase 2/3 trials are underway for further proof. Although these findings are promising, additional studies with larger cohorts are needed to assess the efficacy of MSCs and EVs therapeutic potential to treat and prevent the progression of COVID-19 related injuries in patients. While many clinical trials are listed, not all have begun, and only a few have been completed. Additionally, the completed trials consist of a small sample size, various cellular products, different culture methodology, and need more time for result interpretation. Leading to a discouraging notion that COVID-19 treatment with cellular therapies may not be available soon to treat a significant number of patients. COVID-19 clinical trial moving forward should focus on clear identification of cellular products used and improve quality of study design to further the future of cellular therapies in treatment of COVID-19.

Aside from using stem cells, the field of regenerative medicine also investigates the potential isolation and enrichment of specific anti-inflammatory immune cells to treat inflammation, promote tissue regeneration and transplant tolerance (). In non-acute stroke patients, administration of autologous M2 macrophages is shown to be safe and can modulate inflammatory responses, contributing to angiogenesis and tissue repair (Chernykh et al., 2016). However, the treatment appeared to be more effective in patients with lower endogenous immunosuppressive mechanisms (IL-10, FGF-, PDGF, VEGF) and increased pro-inflammatory activity (IL-1, TNF-, IFN-, IL-6). Infusion of autologous Treg cells has also been investigated for kidney transplantation patients to promote transplant tolerance in hopes of avoiding long-term use of toxic immunosuppressive agents that cause increased morbidity/mortality (Mathew et al., 2018). The administration of transplanted polyclonal Tregs (CD4+CD25+ T cells) derived from the thymus or peripheral tissues of the recipients and expanded in vitro into living donor kidney transplant recipients showed a reduction of total CD4+T and CD8+ T cells and a 520 fold increased circulating Tregs levels after 90 days. The authors aim to move into a phase II clinical trial to test Treg infusions efficacy for tolerance induction or drug minimization (Mathew et al., 2018). Chimeric antigen receptor transduced natural killer (CAR-NK) therapy (Liu et al., 2020), and pluripotent stem cell-derived immunosuppressive cells (macrophages) (Tsuji et al., 2020) are also investigated for use in solid organ transplantation as an alternative method of posttransplant management to improve allograft survival and minimize secondary complications. Recently, Tsuji et al. showed the successful generation of immunosuppressive cells from non-human primate ESCs that expressed several immunosuppressive molecules and significantly inhibited allogeneic mixed lymphocyte reaction (Tsuji et al., 2020). The future goal is to move into pre-clinical trials and demonstrate their potential to suppress allogeneic immune reactions against grafts derived from the same donor in transplantation models. Although advancements in surgical technique and immunosuppression regimens have progressed in transplant medicine, many limitations still exist. The chronic use of immunosuppression in transplant medicine promotes several side effects and increases the relative risk of infections, malignancy, cardiovascular morbidity, and organ damage (e.g., liver toxicity, nephrotoxicity, neurotoxicity, and diabetes mellitus). Thus, to further improve solid organ transplantation outcomes, discovering a novel immunoregulating strategy in regenerative medicine using pluripotent stem cells and engineered immune cells to enhance organ survival and tolerance is vital for the growth of transplant medicine.

In tissue engineering, a combination of cells, a scaffold, and biologically active molecules are used to reconstruct or regenerate damaged tissues or whole organs. The success of tissue engineering relies on the interplay between multiple scientific disciplines such as cell biology, biomedical engineering, and material science. The identification of proper scaffolds, bioreactors, cell sources, and biomolecules such as growth factors and chemokines are needed to reconstruct or regenerate organs correctly. Currently, contrary to 2D planar tissues, bioengineering solid organs for transplantation is still challenging. Advances have been made towards identifying novel scaffolds, biomolecules, and cells, but protocols towards combining the mixture for solid organs de novo reconstruction are still a limiting factor. Although scientific thinking and approaches towards fully realizing the exciting potential of whole organ engineering are still in their early phases, there have been advances in using novel technology with cell therapy to enhance tissue regeneration and function in the clinic ().

Tissue engineering is currently applied to creating alternative materials for the reconstruction of multiple organs. Ram-Liebig et al. show that manufactured tissue-engineered oral mucosa graft is safe and efficient in urethroplasty in male patients with surgically unsuccessful pretreated urethral stricture (Ram-Liebig et al., 2017). The procedure involves harvesting a small oral biopsy from the patients and sending it out to a Good Manufacturing Practice (GMP) laboratory manufacturing company, MukoCell, where the sample is used to create a tissue-engineered oral mucosa graft for the urethroplasty. The transplant success rate was 67.3% at 12 and 58.2% at 24 months and the authors hypothesize that the success rate may be higher if the patients are initially treated with the graft from the beginning. Nonetheless, the authors show that the bulbar and penile urethra reconstruction is feasible, safe, and efficacious in a heavily pretreated population using a tissue-engineered oral mucosa graft. This study demonstrates how current tissue engineering therapies could be successfully standardized and manufactured in a company to provide a constant viable product tailored to everyone.

Clinical studies are also exploring the mechanisms of how tissue-engineered constructs cross-communicate with the diseased milieu to promote healing of a chronic wound. Stone et al. used transcriptomics to understand mechanistically how an FDA-approved bilayer living cell construct (BLCC) promotes the healing of chronic non-healing venous leg ulcers (Stone et al., 2017). BLCC consists of a layer of the human foreskinderived neonatal fibroblasts in a bovine type I collagen matrix under a layer of the human foreskinderived neonatal epidermal keratinocytes. The authors identified that BLCC provides bioactive signals after transplant to the damaged tissue site to promote wound healing via modulation of inflammatory and growth factor signaling, keratinocyte activation, and attenuation Wnt/-catenin signaling. This study identifies mechanistically how tissue-engineered constructs can communicate at the site of injury to promote healing (Stone et al., 2017). The use of a cardiac patch has also garnered much attention, which provides cells a proper microenvironment for tissue development and maturation (Menasch et al., 2018). Bayes-Genis et al. have shown that autologous pericardial adipose graft transplanted within patients treated with coronary artery bypass graft surgery promotes a noticeable improvement in reducing the necrotic mass-sized ventricular volumes after 1year (Bayes-Genis et al., 2016). The authors used an autologous pericardial adipose graft directly obtained from the patients and surgical glued it in place over the necrotic zone after the coronary artery bypass. The surgeons harnessed the biological regenerative capacity of adipose tissue for patients with a chronic myocardial scar. However, no statistically significant difference was noted in necrosis size, possibly due to the limited patient numbers and the need to refine the surgical procedure (Bayes-Genis et al., 2016). Cardiac patches are also used to address the limitation in the retention and need of large cell numbers for cardiac regenerative therapy. In a phase I clinical trial, Menasche et al. assessed the safety and efficacy of transplanting human embryonic stem cell (hESC)-derived cardiovascular progenitors embedded in a fibrin patch in severe ischemic left ventricular dysfunction patients receiving a coronary artery bypass procedure (Menasch et al., 2018). The cardiac fibrin patch showed no evidence of tumor formation or arrhythmias during the 18 months follow-up. Although the feasibility of producing clinical-grade hESC-CM for transplantation was demonstrated, clinical trials assessing efficacy were not yet conducted due to the small sample size, lack of blinded assessment, and confounding effect of the associated coronary artery bypass grafting. Based on these results, there is still a need to identify the best source of stem or progenitor cells and extracellular matrix or biomaterial to promote tissue regeneration and repair in efficacy and safe manner.

Researchers have identified how stem cell heterogeneity, due to differences in source and donor to donor variations, may limit their clinical effectiveness. Autologous (isolated from and transplanted back into the same patient) and allogeneic (isolated from a different patient) stem cells have a different beneficial therapeutic potential based on disease and organ model. Hare et al. demonstrate that although transplantation of both autologous and allogeneic BM-MSCs is safe, feasible, and beneficial when applied in chronic non-ischemic dilated cardiomyopathy (NIDCM), there are slight differences in their beneficial outcomes (Hare et al., 2017). Allogeneic BM-MSCs transplants promote a more significant improvement in functional tests like Ejection Fraction (EF), Minnesota Living with Heart Failure Questionnaire (MLHFQ), Six Minute Walk Test (6MWT), along with the better functional restoration of endothelium and reduction of pro-inflammatory cytokines (TNF-) 6 months after transplantation compared to autologous BM-MSCs. Similarly, Bhansali et al. also show that autologous bone-marrow or mononuclear cells (MNCs) transplanted in patients with type 2 diabetes mellitus effectively reduce the need for insulin after a year (Bhansali et al., 2017). However, patients with MNC transplants showed a significant increase in second-phase C-peptide response during the hyperglycemic clamp indicating insulin production, while MSC transplanted patients had a significant improvement in insulin sensitivity index and an increase in insulin receptor substrate-1 gene expression. Thus, demonstrating the need for more informative studies to distinguish the differential beneficial effects of different cell cellular therapies. Xiao et al. also compared the efficacy of intracoronary administration of BM-MNCs or BM-MSCs for patients with dilated cardiomyopathy (DCM) (Xiao et al., 2017). After 3months, both injections showed an improvement in New York Heart Association (NYHA) functional class and left ventricular ejection fraction (LVEF) in patients. However, after 12 months, BM-MSCs transplanted patients continued to significantly improve LVEF and NYHA, unlike BM-MNCs transplanted patients who showed a decrease in LVEF compared to their 3months follow-up. These results suggest that BM-MNCs provided a temporary improvement in LVEF and NYHA class and only accelerate cardiac function recovery while the improvement observed following BM-MSC therapy is sustained (Xiao et al., 2017). These studies provide novel insights and a comprehensive understanding of how various cell sources and cell types may deliver different therapeutic effects based on disease. Additionally, they highlight the need to tailor stem cell therapies specific to each patients need to enhance their regenerative potential. Further conformational studies with large, randomized, placebo-controlled clinical trials are needed to clarify the complexity of MSCs (based on origin and application) and their interaction with host tissue.

Although advancements are being made daily in cellular therapy, there are still many challenges in translating pre-clinical results regarding cellular therapy efficacy to promote tissue healing, reduce excessive inflammation, and improve the clinics survival (Galipeau et al., 2016; Chinnadurai et al., 2018). It has been shown that not all stem cell therapies are initially beneficial. Makhlough et al. show the safety and tolerability of autologous BM-MSC transplanted into six autosomal dominant polycystic kidney disease patients but with no physiological improvement detected after 1year (Makhlough et al., 2017). Patients exhibited a continuous decrease of GFR with a significant increase in serum creatinine levels. The study was limited to only six patients, and only a single cell transplant was administered, which may partially explain the limited beneficial effects detected (Makhlough et al., 2017). Stem cell therapys effectiveness may also be limited by the extent of chronic inflammation and fibrosis already present within the patients damaged tissue. In patients with decompensated (severe) alcoholic liver disease, transplantation of BM-MSCs showed no modification of the diseases progression after 4weeks (Lanthier et al., 2017) to 8weeks (Rajaram et al., 2017). Although patients showed an elevation of liver macrophages and upregulation of regenerative liver markers (SPINK1 and HGF), no difference was detected regarding proliferative hepatocyte numbers (Lanthier et al., 2017). There are also potential safety concerns with cellular therapy, such as the potential for malignant transformation of MSCs (Steinemann et al., 2013). A long-term follow-up study of patients with decompensated (severe) alcoholic liver disease transplanted with autologous BM-derived mononuclear cells showed improved liver function and decreased collagen levels in patients liver transiently 6months post-transplantation (Kim et al., 2017). Patients also displayed improved biochemical parameters, CP class, and increased liver volume, indicating liver regeneration. Although improved liver function was still evident at the five-year follow-up, patients who had received cell transplantation had an alarming increased risk of developing hepatocellular carcinoma (HCC). This relatively high incidence of HCC within 2years after autologous bone marrow cell infusion warrants further investigation (Kim et al., 2017). Other studies have also shown that a small group of hematopoietic cell transplant survivors may suffer from not only solid tumors but also from other significant late effects such as diseases of the cardiovascular, pulmonary, and endocrine systems, dysfunction of the thyroid gland, gonads, liver and kidneys, infertility, iron overload, bone diseases, infection, and neuropsychological effects (Inamoto and Lee, 2017). The leading cause of mortality in adult patients who had received hematopoietic cell transplants includes recurrent malignancy, lung diseases, infection, secondary cancers, and chronic graft-versus-host disease. Thus, long-term risk assessment studies of patients receiving stem cell transplantation are needed to understand the risk of developing cancer and other harmful late effects versus the long-term benefits of stem cell therapy. Another limitation preventing comparison of current clinical trials and their outcomes, is that not all clinical trials adhered to ISCT criteria in defining the cellular treatments. Moving forward, improved methodological quality, increased sample size, and extended trial duration are needed for a better comparison of clinical trial data and results amongst each study. Cossu et al. and others also emphasized the need for better science, funding models, governance, public and patient engagement to enhance cellular therapys efficacy and safety in the clinic (Cossu et al., 2018). Regulatory limitations are another hurdle for the application of cell therapies or new technologies. With growing innovations made in regenerative medicine, outdated regulations may not adequately address new challenges posed as technology advances. Thus, new regulations must be designed to protect the patients from unnecessary risk while encouraging investigators, funding bodies, and investors to support research and development and market commercialization of novel products.

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Regenerative medicine applications: An overview of clinical trials

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The Progression of Regenerative Medicine and its Impact on Therapy …

Friday, September 13th, 2024

Clin Transl Sci. 2020 May; 13(3): 440450.

1Division of Cardiac Surgery, University of Ottawa Heart Institute, OttawaOntario, Canada

2School of Human Kinetics, University of Ottawa, OttawaCanada

1Division of Cardiac Surgery, University of Ottawa Heart Institute, OttawaOntario, Canada

3Department of Cellular & Molecular Medicine, University of Ottawa, OttawaCanada

1Division of Cardiac Surgery, University of Ottawa Heart Institute, OttawaOntario, Canada

2School of Human Kinetics, University of Ottawa, OttawaCanada

3Department of Cellular & Molecular Medicine, University of Ottawa, OttawaCanada

Received 2019 Nov 6; Accepted 2019 Nov 7.

Despite regenerative medicine (RM) being one of the hottest topics in biotechnology for the past 3decades, it is generally acknowledged that the fields performance at the bedside has been somewhat disappointing. This may be linked to the novelty of these technologies and their disruptive nature, which has brought an increasing level of complexity to translation. Therefore, we look at how the historical development of the RM field has changed the translational strategy. Specifically, we explore how the pursuit of such novel regenerative therapies has changed the way experts aim to translate their ideas into clinical applications, and then identify areas that need to be corrected or reinforced in order for these therapies to eventually be incorporated into the standardofcare. This is then linked to a discussion of the preclinical and postclinical challenges remaining today, which offer insights that can contribute to the future progression of RM.

In 1954, Dr. Joseph Murray performed the first transplant in a human when he transferred a kidney from one identical twin to another.1 This successful procedure, which would go on to have a profound impact on medical history, was the culmination of >50years of transplantation and grafting research. In the following years, organ replacement became more widespread but also led to a plateau in terms of landmark successes.1 The technology was working, but limitations were already being encountered; the most prominent of them being the lack of organ availability and the increasing need from the aging population.2 During the same time period, chronic diseases were on the rise and the associated process of tissue degeneration was becoming evident. Additionally, the available clinical interventions were merely capable of treating symptoms, rather than curing the disease, and, therefore, once a loss of tissue function occurred, it was nearly impossible to regain.3 Overall, the coupling of all these factors that took place in the 1960s and 1970s created urgency for disruptive technologies and led to the creation of tissue engineering (TE).

TE can be described as a field that applies the principles of engineering and life sciences toward the development of biological substitutes that restore, maintain, or improve tissue function or a whole organ.4 TE is considered to be under the umbrella of regenerative medicine (RM) and, according to Dr. Heather Greenwood et al., regenerative medicine is an emerging interdisciplinary field of research and clinical applications focused on the repair, replacement or regeneration of cells, tissues or organs to restore impaired function resulting from any cause, including congenital defects, diseases, trauma and aging.5 It uses a combination of technological approaches that moves it beyond traditional transplantation and replacement therapies. These approaches may include, but are not limited to, the use of soluble molecules, gene therapy, stem cell transplantation, tissue engineering, and the reprogramming of cell and tissue types.3, 6, 7 A summary of the recent history of RM is presented in Figure.

A summary timeline of the recent history of regenerative medicine (RM). Selected milestones in the development of RM are presented starting from the 1950s all the way up to the present day.

Although RM may have seemed novel, the principles of regeneration are as old as humanity and are found in its many cultures.8 A common example used is the tale of Prometheus that appeared in 8th century BCE. Prometheus, an immortal Titan in Greek mythology, stole fire and gave it to humanity for them to use, defying the gods in consequence. As punishment, Zeus decreed that he was to be bound to a rock where an eagle would feast on his liver every day and said liver would regenerate itself every night, leading to a continuous loop of torture.9 RM came about at the time it did, not only because of the combining factors mentioned above, but also because researchers had been successfully keeping tissue alive in vitro and understanding the biological processes involved in regeneration and degeneration. Consequently, possible therapeutic outcomes came into fruition. Since the arrival of TE and RM, strides made on the benchside have been ever increasing with now >280,000 search results on PubMed relating to regeneration. Discoveries and advances made by cell/molecular biologists, engineers, clinicians, and many more led to a paradigm shift from treatmentbased to curebased therapies.10 In addition to Greenwoods definition, RMs arsenal now contains controlled release matrices, scaffolds, and bioreactors.5, 8 Despite this impressive profile on the benchside, RM has so far underperformed in terms of clinical applications (i.e., poor therapy translation).8 Simply put, a disappointing number of discoveries are making it through clinical trials and onto the market.11 Although some experts say that the field is reaching a critical mass in terms of potential therapies and that we will soon see results, others, like Dr. Harper Jr. from the Mayo Clinic in Minnesota, say that the transformative power of RM is well recognized, but the complexity of translating isnt.7, 8, 12

This brings us to the subject matter of the present paper: RM and translation. The goals of this historical review are twofold. The first is to understand how RM, over the past 50years or so, has changed the way discoveries/new technologies are transferred to the clinic. How has the translational strategy changed in response to these new therapies? The second is to identify challenges that have led to RMs modest performance on the bedside. Some articles have already documented these but have focused on the clinical and postclinical factors, and whereas they will be briefly discussed here, the focus will be on preclinical factors.13 To accomplish these objectives, we will begin by summarizing the historical development of RM (which has been extensively documented by other works2, 3, 14, 15), followed by a detailed look at the definition of translational medicine (TM). With this background information established, we then look at the various preclinical and clinical impacts of RM on TM, as well as some of its effects on the private sector. Limiting factors of the field are then described, again focusing on those that are preclinical. This endeavor was initiated via a librarianassisted literature search for original research and historical documentation of the field of RM and other related subjects. The documents were then screened for relevance and the analyzed information was categorized into the themes discussed below. Conclusions were then drawn based on the interplay among these themes.

As mentioned, the idea of regeneration first started in myths and legends. This is logical because, as Drs. Himanshu Kaul and Yiannis Ventikos put it, myths shape ideas, and ideas then shape technologies.8 In addition to the tale of Prometheus, there are many others. For example, there is the Hindu myth of Raktabeej whose blood drops could each form a clone of himself, or the Indian story of the birth of the Kaurava brothers where pieces of flesh were grown in pots and treated with herbs to grow fullsized humans.8 The idea of regeneration has persisted throughout history and started to become a possibility in the early 1900s when scientists like Alexis Carrel (who invented the technique of cell culture) were finally able to keep cells and tissues alive outside of the body. This allowed them to study the mechanisms of cell renewal, regulation, and repair.8 In addition, studying regeneration goes handinhand with developmental biology. Seminal work in experimental embryology began in the 1820s with the detailed description of the differentiation of embryonic germ layers.16 An increased understanding of basic embryological mechanisms led to Hans Spemanns Nobel Prize for his theory of embryonic induction; a field that was further elaborated by his students and others, advancing it toward the possibility of cloning and demonstrating how development and regeneration are intimately linked.16 Before this era, the study of regeneration was done through the study of animals, with scientists studying the phenomena in serpents, snails, and crustaceans, for example.17, 18 However, the modern study of regeneration is said to have started with Abraham Trembleys study of the hydra, which showed that it was possible for an entire organism to regenerate from its cut appendage.19 The 18th century on through to the 19th century is also when scientists became intrigued by the amphibian newts and axolotls for their astonishing regenerative capabilities, which are still used today as the gold standard models for studying regeneration along with certain fish, such as the zebrafish.20

Now, although the term RM as we know it today would only be coined in 1999 by William Haseltine, the field itself started in the late 1970s in the form of TE (pioneered by Drs. Joseph Vacanti and Robert Langer) in the city of Boston.2, 14, 21 To address the need for novel therapies, biomedical engineers, material scientists, and biologists at Harvard and MIT started working on regenerating parts of the largest and simplest organ of the human body: the skin. In 1979, the first cellbased TE product appeared and was named Epicel.15 Developed by Dr. Howard Green et al., this technology consisted of isolating keratinocytes from a skin biopsy and having them proliferate outside of the body to make cell sheets that were then used as an autologous treatment for burn patients.15 Another famous product (this time allogeneic), developed in 1981, was Apligraf, a composite skin invention capable of rebuilding both the dermis and epidermis of skin wounds.15 With these two therapies and many more being created, TE in the 1980s was booming. At the time, researchers were also developing therapies for cartilage regeneration.

Once the 1990s came around, TE strategies were combined with stem cells (which had just been discovered) to create RM.3, 8 At that time, RM was a hot topic. After the first products for skin were commercialized, scientists became more enthused and started trying other tissues.15 Startup companies were popping up left and right, private funding was abnormally high, and public hype was gaining lots of traction. However, governments were not so quick to fund this research and took their time before making decisions, whereas private investors saw this field as very promising and thought it was their ticket to the top.14 Given that 90% of the funding of RM came from the private sector, this greatly influenced the direction of the research and its timeframe.14 People were simply trying to copy tissue formation rather than understanding it, so as to make the development process quicker.3 As a result, many of the technologies that initially looked promising failed in clinical trials or on the market.

These disappointing results coupled with the dot.com crash meant that by the end of 2002, the capital value of the industry was reduced by 90%, the workforce by 80%, and out of the 20 US Food and Drug Administration (FDA) products with clinical trials, only 4 were approved and none had any success.22 This phenomenon has been extensively studied and, according to Lysaght and Hazlehurst, five factors contributed to the industry crash22:

The products were not much better than the existing treatment options and so making the switch was not worth it for clinicians.

Even if the science was good, lowcost manufacturing procedures did not exist.

The approval process for these novel therapies was unrealistically challenging and the regulatory cost was too high.

Companies lacked the skill to market their new products.

The reimbursement strategies were unclear.

Despite these events, the industry had 89 firms survive the crash and stem cell research was not affected. In fact, from 2000 to 2004, the number of companies increased but the number of jobs decreased, which means investors were supporting research in basic and applied science with smaller firms that were lower risk, and by 2004, the field was dominated by startup companies.22 Before the crash, RM was primarily happening in the United States, but in 2004, other countries like the United Kingdom and Japan started catching up.22 The industry slowly started growing again. In 2006, the first engineered tissue (bladder) was implanted, and by 2008, commercial successes were being achieved.3, 10 As an example, hematopoietic stem cell transplants were approved and are now a curative treatment for blood disorders and other immunodeficiencies.7 Now, the RM field had ironically regenerated itself.3 It has gained increased governmental attention (federal funding has increased) and has been recognized as being at the forefront of health care.7, 22 There is once again intense media coverage that is raising public expectations.23 The number and variety of clinical trials is also increasing everywhere.23 According to allied market research, RM is predicted to be worth US $67.5 billion by 2020.10

Unfortunately, regardless of these seemingly cheerful notes, the fact remains that cell therapies remain experimental, except for the aforementioned hematopoietic stem cell treatments.13 The market for RM is still small and will remain so until RM proves that its therapies are better and cheaper than the existing ones.15 Yet, the pressure for clinical translation is increasing through the needs of the population, investors that are eager to make a return on their investments, and scientists who believe that these technologies are the future.23 Moreover, there has been a growing appreciation of the magnitude and complexity of the obstacles the field is facing, but it remains to be seen how they will be solved; although initial steps have already been taken, which will be discussed further below.

Now that we have established the background for RM, there needs to be a proper understanding of TM before conclusions on how the two are related can be drawn, which is the purpose of the following section.

The European Society for Translational Medicine (EUSTM) has defined TM as an interdisciplinary branch of the biomedical field supported by three main pillars: benchside, bedside, and community. The goals of TM are to combine disciplines, resources, expertise, and techniques within these pillars to promote enhancements in prevention, diagnosis, and therapies.24 TMs goals can be split into two categories: T1 and T2. T1 is to apply research from bench to bedside and back, whereas T2 is to help move successful new therapies from a research context to an everyday clinical context.25 In other words, TM is a medical practice explicitly devoted to helping basic research attain clinical application. Conceptual medical research, preclinical studies, clinical trials, and implementation of research findings are all included within TM.26

Between basic science and the clinic is an area that is popularly referred to as the valley of death.25 This gap is fraught with not only scientific obstacles (like an unknown molecular mechanism), but social and economic ones as well. This is where many novel ideas die and, consequently, companies are weary of going through this valley for fear of wasted financial resources.25 For these reasons, many of the approved drugs we get now are derivatives of others that have been previously approved.25 This is the area that TM seeks to impact, to be the bridge between idea and cure, and to act as a catalyst to increase the efficiency between laboratory and clinic.25, 26 The term bench to bedside and back is commonly used. The cost of development for a therapy is very high (estimated at US $800 million to $2.6 billion for a drug) because of increasing regulatory demands and the complexity of clinical trials, among others. TM aims to streamline the early development stages to reduce the time and cost of development.24

What will be important to note for the discussion below is that TM focuses more on the pathophysiological mechanisms of a disease and/or treatment and favors a more trialanderror method rather than an evidencebased method. Dr. Miriam Solomon argues in his book chapter entitled What is Translational Medicine? that most medical innovations proceed unpredictably with interdisciplinary teams and with shifts from laboratory to patient and back again, and that freedom of trialanderror is what will lead to more therapeutic translation.25 Furthermore, for years, TM did not have any technical suggestions for improving translation, only two broad categories that were claimed to be essential for translatability: improving research infrastructure and broadening the goals of inquiry. This discrepancy has since been identified and efforts have been made to address it. For example, the EUSTM provided a textbook called Translational Medicine: Tools and Techniques as an initiative to provide concise knowledge to the fields stakeholders.24

Presently, TM has attracted considerable attention with substantial funding and numerous institutions and journals committed to its cause.25, 27 But before this, its arrival had to be incited. TM emerged in the late 1990s to offer hope in response to the shortcomings of evidencebased medicine and basic science research, such as the unsatisfactory results from the Human Genome Project, for instance.25 There were growing concerns that the explosion of biomedical research was not being translated in a meaningful manner proportionate with the expenditures and growing needs of the patients.27 The research had ignored what it took to properly disseminate new ideas.25 The difficulties of translation from bench to bedside have always been known, but what is different with TM is the amount of emphasis that is now put on translation and the recognition on how difficult and multifaceted it is to translate technologies.25 Over the past 20years, the role, power, and research volume of the field has increased, and TM is now a top priority for the scientific community.26 TM is also often used as common justification for research funding and conveys the message to politicians and taxpayers that research activities ultimately serve the public, which is also why it appeals to todays generation of students who want to work on big, realworld problems and make a meaningful difference.28, 29

As already mentioned, RM therapies are proving difficult to translate to the clinic.11 Although the basic research discoveries are never ceasing (books such as NewPerspectives in Regeneration by Drs. HeberKatz and Stocum30, and articles such as "Tissue Engineering and Regenerative Medicine: Past, Present, and Future" by Dr. Antnio Salgado et al.,31 provide comprehensive summaries of these advancements), therapy approval is practically nonexistent.30, 31, 32 This may be due, in part, to a tendency for people to blame the lack of translation of their technologies on extrinsic factors, thus removing responsibility.11 Additionally, the failures are not being studied. For example, stem cell research looks good in small animals but often fails in larger ones and then does not progress beyond phase II or III clinical trials because no benefits are found, and historically we have not been exploring why.11, 32 Consequently, the next therapies that are developed are improved by guesses rather than through a better understanding of the disease in mind (Figure).11

The negative feedback cycle currently present in most discovery and development processes of regenerative medicine. This cycle obstructs progression of the field.

RM has the potential to impact not only the quality of healthcare but also the economy, because the costs that could be avoided with curative therapies are immense.33 For this reason, analyzing the impact of RM on the translational strategy over time can help identify aspects that should be encouraged or discouraged to drastically improve translation. Reflecting on this history cannot only help us to avoid past mistakes but can also aid in redirecting the field to a onceproductive path.34 In the following section, the preclinical impact of RM on TM will be discussed, focusing on the shift from evidencebased medicine to trialanderror, the role of the basic scientist, and the emergence of the multidisciplinary approach. Clinical impact is also covered, concentrating on regulatory modifications. Last, changes in the private sector are considered as the shift in business models is detailed.

Because the RM field is essentially comprised of new ideas on cell renewal and tissue healing, it is logical that most of its impact would be on the preclinical side, as this is where ideas are tested, finetuned, and developed. Coincidentally, it is also where the translational strategy begins. Considering certain aspects early in the developmental process, such as realistic applications and ease of use, can help facilitate translation. RMs influence on TM can thus be separated into the three themes below.

Before the late 20th century, the majority of medical research was done using evidencebased medicine. This is a systematic approach to solving a clinical problem that integrates the best available research evidence together with clinical signs, patient values, and individual clinical experience all to support scientific decision making and research progression.35 As such, evidencebased medicine favors clinical trials and does not allow for much tinkering and only that which possesses highquality clinical evidence is to be pursued. This has its limitations, as it devalues mechanistic reasoning, and both in vitro and animal studies. Therefore, evidencebased medicine may have played a role in RMs downfall in the early 2000s. TE in the 1990s was using evidencebased medicine and was simply trying to copy tissue formation rather than trying to understand it.3 That most of the funding was coming from the private sector probably did not help either. Investors saw TE as an opportunity for quick returns on their investments, so therapies were rushed to clinical trials, which led to inconsistent results.14, 25, 32

As well, evidencebased medicine obscured the need for different methods of discovery. After RMs decline and the idea of TM came about, a trialanderror method was adopted. This technique favors a team effort, mechanistic reasoning, and seeks to change the social structure of research.25 Although clinical trials are still deemed important, the trialanderror method identifies that an idea needs to first be explored and should not necessarily require the confirmation of a hypothesis.11, 25 This new method is based more so on facts and has stimulated a more informed dialogue among stakeholders (whereas the confirmation or refusal of a hypothesis cannot always be made relevant to people outside the field). This, in turn, can help the regulatory agencies reduce the burden on their review boards in the evaluation and acceptance of novel strategies.11 Therefore, the failures of RM had helped to highlight the boundaries of evidencebased medicine and, combined with the rising intensity put on TM in the 1990s, assisted in defining the trialanderror based method.

Another thing that is changed with the historical development of RM has been the role of the basic scientist. Please see Figure for a summary of the differences between the traditional and modern scientist discussed in this review. Traditionally, basic scientists have worked with a discovery mindset, but without a noticeable regard for potential therapeutic applications. It has been noted that RM has made us realize how important it is to take the practical and industrializing aspects (like cost, for example) into account even at the basic research level.7, 14 The needs of the end users need to be considered during the developmental phase if RM is to establish a proper foothold within the market.15 In view of this, over the past 2decades, medical philosophy has changed in that it encourages basic scientists to communicate more with clinicians and vice versa. Experts like Barry Coller, MD, Vice President for Medical Affairs and PhysicianinChief at the Rockefeller University Medical Center, have identified various skills that a basic scientist must possess if translational research is to be improved.26, 28 Additionally, other researchers have commented that more and more basic scientists are motivated to have an impact on global health and this passion can be a source of inspiration that can help fuel interdisciplinary cooperation.28 Efforts have also been made to familiarize basic scientists with regulatory requirements. For example, the FDA publishes guide documents with recommendations on how to address these requirements.36 Despite this, much remains to be done, as there is still a lack of TM professionals and the current research environment hampers cooperation between experts (e.g., specialization is still encouraged, and achievement awards are individualized).26, 28

A comparison between the traditional and modern scientist. Although traditional scientists are more hypothesisdriven and rigid in terms of research methodology, if the concepts shown above are used, it can generate the modern scientist who is better suited for the translation of regenerative therapies. RM, regenerative medicine.

An additional point that can be argued is that because RM got basic scientists more involved in the translational process, this has consequently made them more realistic.37 As already mentioned, early RM therapies were comprised of complex cell therapies that were not fully understood. From 2004 onward, the field diversified to include research into simpler acellular products.38 Other avenues, such as induced pluripotent stem cells, endogenous repair, nanotechnology, and regenerative pharmacology, are also being explored.37, 39, 40, 41 Increasingly, experts are trying to spread this message; for instance, in the field of cardiology, Dr. Mark Sussman, a world renowned cardiac researcher, and his colleague Dr. Kathleen Broughton at the San Diego State University Heart Institute and the Integrated Regenerative Research Institute, recently stated that After over a decade of myocardial regenerative research studies, the initial optimism and enthusiasm that fueled rapid and widespread adoption of cellular therapies for heart failure has given way to more pragmatic, realistic, and achievable goals.9

The last preclinical impact of RM to be discussed is the arrival of the multidisciplinary approach. This now widespread notion identifies that to improve translation and accelerate technology development, it is better to have a team composed of experts from multiple disciplines, because the various backgrounds and schools of thought can be combined with each contributing to a project in a different way.25, 39 What has surely incited its evolution is that RM inherently requires contributions from biologists, chemists, engineers, and medical professionals. This need has led to the formation of institutions that house all the required expertise under the same roof (such centers have increased in number since 2003), which promotes more teamwork between laboratories and clinics.28 Dr. Jennifer Hobin et al.28 states that bringing dissimilar research expertise together in close proximity is the key to creating an environment that facilitates collaboration. In addition, it could be said that these collaborative environments help minimize the flaws of medical specialization, which occurred in the second half of the 19th century; where the ideological basis that the human body can be categorized combined with the rapid arrival of new medical technologies led to the specialization of medical practice, which, in turn, led to the segregation of medical professionals from each other and the patient.42 Coincidentally, if one recalls the definition of TM, it, along with the trialanderror based method, suggests that improved research infrastructures and team efforts can facilitate the translation of therapies.

We now look at the influence that RM has had on the clinical side of therapy development. Before the subject is discussed, it is important to note that the reason clinical research has been affected is because of the uniqueness of RM therapies. Their novelty does not fit within the current regulatory process or use in clinical trials, and although the latter has yet to adapt, the regulatory sector has attempted over the years to facilitate the journey from bench to bedside.7, 43, 44

Initially, when RM was in its infancy, its therapies were regulated by the criteria originally developed for drugs; and as we have seen, this was identified as a factor that led to its downfall. Now, in 2019, several regulatory changes have been implemented to rectify this. What has helped has been the input from other countries. As mentioned above, RM started in the United States, but after the crash, other countries like the United Kingdom and Japan caught up, and their less stringent regulatory procedures have allowed them to better adapt the framework for these new therapies.22 In 2007, the European Union passed the Advanced Therapy Products Regulation law, which defined regenerative therapies, categorized them, and provided them with separate regulatory criteria for advanced approval.13, 43 In 2014, public pressure and researcher demands led Japan to enact three new laws: the Regenerative Medicine Promotion Act, the Pharmaceuticals, Medical Devices, and Other Therapeutic Products Act, and the Act on the Safety of Regenerative Medicine. These unprecedented national policies now help therapies gain accelerated and conditional approval to better conduct clinical trials and to better meet the demands of the patients.7, 13, 44, 45 During this time, the United States has not stood idle. In 2012, the US Congress passed the FDA Safety and Innovation Act (FDASIA), which expanded its existing Accelerated Approval Pathway to include breakthrough therapies, a category created for new emerging technologies, including regenerative strategies.13, 46 Drs. Celia Witten, Richard McFarland, and Stephanie Simek provide a wellwritten overview on the efforts of the FDA to accommodate RM.36 By and large, it is safe to say that RM has spurred a drastic change in traditional regulatory pathways to not only better manage these novel therapies but also put more weight on efficient translation.

It is also important to discuss changes in the private sector because manufacturing and marketing is and will remain one of the greatest obstacles facing RM, and, once again, the novelty of the field is responsible. Although the bulk of the problems remain, there has nonetheless been a change in business strategies that is worth appreciating.

Throughout its history, RM research has been carried out by academic research institutions or small and mediumsized enterprises.23, 47 With this in mind, the business model used in the health industry varies depending on the type of company. The royalty model is the one primarily used by biotech companies.8, 14 Here, businesses will develop a therapy up to the clinical stage and then hand it off to a company with more resources (usually a pharmaceutical one) who can carry out the larger scale studies. With this model, biotech companies make money simply through royalties and this carries both pros and cons (Figure).

A comparison of both the royalty and integrated business models used by private companies in the biomedical industry. The pros and cons are listed with the assumption that they are for a startup company in regenerative medicine.

Because the market for regenerative therapies currently is not big enough for the royalty model, startups have had to shift to an integrated model where the discovery, development, approval, and manufacturing of a new therapy are all done internally (which is unusual for small startups).8 Using this strategy, the companies can reap all the rewards but obviously also assume all the risk.

The market for regenerative therapies has so far been small enough that smaller firms do not have to manufacture large quantities of their products (like they do in the pharmaceutical industry) and they can start making money in a quicker fashion.8 Whether the business model will change again as the market grows or if the original startups will grow in proportion remains to be seen.14 What is to be highlighted here is that those who seek to commercialize regenerative therapies have had to shift to an integrated business model (that was not previously the norm for smaller ventures), which has affected translation by letting them have more influence in determining how their therapy is being developed, marketed, and manufactured.

Having detailed RMs relationship with the translation strategy and the aspects that changed in conjunction with the fields development, the remainder of the review will summarize the challenges that are contributing to RMs modest performance in the clinic.

With increased funding and a growing number of committed institutions, many countries have become increasingly invested in RMs success. For example, the US Department of Health and Human Services recognizes RM as being at the forefront of healthcare.7 As well, the UK government has identified RM as a field in which they can become global leaders and that will generate significant economic returns.44 The literature indicates that RM is reaching a critical mass and is on the verge of a significant clinical transition. The optimism is as high as it has ever been and the rush to succeed with clinical trials is equally felt.23 However, the bottom line is that the clinical and market performance is still very poor. Being that a gold standard for treatment in RM remains elusive, clinicians are often illinformed about current applications, and studies on safety and efficacy are lacking.23, 44, 48, 49 The National Institute of Health estimates that 8090% of potential therapies run into problems during the preclinical phase.28 Naturally, scientists have offered various explanations for these results, such as deficiencies in translational science and poor research practices in the clinical sciences.50 Shockingly, in a 2004 analysis, 101 articles by basic scientists were found that clearly promised a product with major clinical application, and yet 20years later, only 5 were licensed and only 1 had a major impact.50 Therefore, it is easily deducible that many challenges still lie ahead. The perceived riskbenefit ratio remains high and, as a consequence, clinical trials have been proceeding with caution.13, 23, 33 Numerous reviews have been published on these challenges but with an emphasis on those relating to the clinical phase.11, 13, 22, 51 Although these will be summarized below, the present study highlights the identification and analysis of the preclinical challenges. Please see Figure for a summary of the preclinical and clinical obstacles discussed herein.

Summary of the preclinical and postclinical challenges discussed. Even though preclinical obstacles to the translation of regenerative medicine therapies are more elusive, they are just as significant as their counterparts.

To begin, a possible explanation for the preclinical obstacles being underrepresented in the literature is because of the pliability of the phase itself. Although the clinical phase is composed of numerous subphases and strict protocols, the preclinical research is much less structured with less oversight. Whereas rigorous scientific method is applied to the experiments themselves, which usually consist of in vitro followed by in vivo experiments, the basic scientist has more flexibility regarding experimental organization, structure, and backtracking; thus, making explicit challenges possibly harder to recognize.

Some researchers have nevertheless attempted to do so. For example, Dr. Jennifer Hobin et al. have identified three major risks associated with RM technologies as being tumorigenicity, immunogenicity, and risks involved with the implantation procedure.13 The first two relate to arguably the largest preclinical challenge, which have been identified as needing a better understanding of the mechanism of action.12 Although the difficulties of identifying a mechanism are appreciated in the scientific community, it is imperative that improvements in this area are made as it will affect application and manufacturing decisions. Hence, greater emphasis on identifying the mechanism of action(s) will need to be adopted by basic scientists who are looking to develop a technology.

Another significant preclinical challenge is the lack of translation streamlining for basic scientists. Although basic scientists have become more involved in the translational process and more pragmatic over the years, there is, in general, still a lack of incentive and available resources to help a scientist translate their research. Academic faculty members are given tenure and promotion based on funding success (grants) and intellectual contributions (publications).28 Thus, researchers who have received money to conduct research and publish their work on a promising new therapy might stop short of translation as there may be no additional recognizable accomplishment or motivation for such an endeavor. For example, Jennifer Hobin et al. described the case of Dr. Daria MochlyRosen at Stanford Universitys Translational Research Program, who sought help for an interesting idea for a heart rate regulation therapy.13 She was turned down by numerous companies that found the clinical challenges too daunting and her colleagues offered no support but rather discouraged her from pursuing the idea saying that it would not be worthwhile for her career.

Last, a very important preclinical challenge that has gained recognition over the past few years is the lack of appropriate preclinical testing models. It is often reported that novel therapies that do well in the laboratory but then fail in larger animal studies or clinical trials. This is partly due to a lack of mechanistic insight, but also because of a shortage of appropriate in vitro, in vivo, and ex vivo models.9, 36 With properly validated preclinical models, we would be better able to gauge the performance of novel therapies and predict their future clinical success, but instead we are misidentifying the potential of therapies. Notably, the lack of appropriate models also contributes to the difficulty in obtaining reliable data on the underlying mechanism(s) of action of RM therapies, as differences may exist between the preclinical and clinical settings.

As far as clinical challenges go, they are numerous. Stem cell trials in particular have received criticism from a perceived lack of rigor and controlled trials.23 Related to this, a potent point that has arisen over the past few years is the absence of longterm followup studies for clinical trials, which is clearly necessary to establish the safety and efficacy of these interventions.13, 33 Unfortunately, they are costly and they are timeconsuming. Efforts are nonetheless being made to overcome these obstacles. For example, in 2015, the Mayo Clinic released an RM buildout perspective offering a blueprint for the discovery, translation and application of regenerative medicine therapies for accelerated adoption into standard of care.7 Institutions, such as Canadas Center for Commercialization of Regenerative Medicine, have been launched to help researchers mitigate the risks of cell therapy development by offering technical as well as business services.12, 51 Experts are also stepping up; for example, Drs. Arnold Caplan and Michael West proposed a new regulatory pathway that incorporates large postmarket studies into clinical trials.33

In terms of manufacturing, it is difficult to engage industry because the necessary technology to produce RM therapies at an industrial level does not exist yet. Scaleout and automated production methods for the manufacturing of regenerative therapies are needed.7, 10, 12, 23, 52, 53 This challenge stems from the complexity and natural intrinsic variation of the biological components, which makes longterm stability difficult to achieve and increases manufacturing costs.13, 44 Now, if RM therapies could establish their superiority over conventional treatments, then this would potentially alleviate costs and increase the likelihood of being reimbursed, but it remains to be seen.13 A hot topic at the moment is the choice between autologous or allogeneicbased products, which would entail either a centralized or decentralized manufacturing model, respectively (although hybrid models have been proposed).7, 23, 54 Autologous products, being patientspecific, have the advantage of having smaller startup costs, simpler regulations, and point of care processing.47 As for allogeneic products, they are more suitable for an off the shelf product, for a scaleout model and quality controls can be applied in bulk.47, 54 Dr. Yves Bayon et al.51 provided a thorough description of this topic while simultaneously indicating areas that have been identified for improvement.

As mentioned above, regulatory challenges are what have been most addressed thus far through scientific and public pressure. Moving forward, the goal identified by expert thinktank sessions is to harmonize RMspecific regulations across agencies and countries.7, 36 Reimbursement is the last of the regulatory challenges to be considered. In order for RM treatments to become broadly available, reimbursement is a necessity and both public and private healthcare need to determine how the regulations will be modified for disruptive therapies coming down the pipeline.13, 23, 44

RM has had an undeniable influence on the process of bench to bedside research. Preclinically, it has helped identify the limitations of evidencebased medicine and contributed to the paradigm shift to the trialanderror method. Likewise, the field has changed its mindset and the basic scientist is adopting new responsibilities becoming more motivated, pragmatic, and involved in TM, rivaling researchers in the applied sciences. The multidisciplinary approach has also been promoted by RM over the years and institutions dedicated to fostering collaborative research in RM have increased in numbers. Clinically, regulatory pathways that were developed for drugs and biomedical devices, and which have been in place for decades, have been adapted to aid RMs disruptive technologies, leading to new guidelines that favor translation. In the private sector, the novel nature of RM therapies has led to startup companies using an alternative business model that provides them toptobottom authority over the development of their products and it is yet to be seen if the business strategy in place will be sufficient as the industry grows.

If the translation of RM therapies is to be improved, many of the challenges to be overcome lie in the early stages of therapy development, such as identifying the mechanism(s) of action, validating preclinical experimental models, and incentivizing translational research for basic scientists. In later stages, regulatory changes have been made, but much still needs to be addressed. This includes the adoption of clinical trials that are more rigorous and include longterm followup studies, the development of appropriate manufacturing technology, the synchronization of regulatory agencies, and a clear plan for reimbursement strategies. Once again, these challenges have been discussed in greater detail in previous works.2, 3, 7, 12, 13, 15, 22, 23, 26, 31, 38, 44, 48, 51, 52 While it seems that the field may be at a tipping point with many challenges remaining, the fact that translation has been influenced in a positive way gives promise to the future progression of RM therapies.

This work was supported by a Collaborative Research Grant from the Canadian Institutes of Health Research (CIHR) and the Natural Sciences and Engineering Research Council (NSERC; CPG158280 to E.J.S.), and the Hetenyi Memorial Studentship from the University of Ottawa (to E.J.).

All authors declared no competing interest for this work.

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Immune cell injection significantly boosts healing of bone, muscle & skin

Friday, September 13th, 2024

Injecting regulatory T cells or Tregs, which control the bodys immune responses, directly into damaged bone, muscle and skin significantly boosts healing, according to new research. The door is now open to developing a universal cell-based method of enhancing healing after an injury.

A few months ago, we reported on research by the University of Cambridge in the UK that overturned traditional thinking about regulatory T cells or Tregs, finding that these active controllers of the bodys immune response have the potential to be used as an army of healers for almost everything.

Now, researchers from the Immunology Frontier Research Center (IFReC) at Osaka University, Japan, and Monash University in Melbourne, Australia, have investigated that potential as part of a new study and found that its true.

We began exploring administering Tregs for regenerative medicine purposes because they can directly impact other immune cell types called monocytes and macrophages, said Mikal Martino, an associate professor at Monash who also held a cross-appointment position at Osaka University, and the studys corresponding author. Additionally, Tregs can secrete signaling molecules that support tissue healing. Despite their strong potential, few studies have explored using Tregs for such applications.

Monocytes are white blood cells responsible for fighting certain infections and helping other white blood cells remove dead or damaged cells. Macrophages, another type of white blood cell of the immune system, engulf and digest (phagocytose) pathogens like microbes, cancer cells, cellular debris and foreign substances.

Essential to healing and tissue restoration post-injury is the bodys ability to transition from a pro-inflammatory to an anti-inflammatory state. Theres plenty of scientific evidence about what can occur when the inflammatory response is not switched off and becomes chronic. Understandably, regenerative medicine therapies seek to capitalize on the main immune system players in this pro- and anti-inflammatory process. Thats where Tregs come in.

Nayer et al.

In the present study, the researchers locally administered a fibrin hydrogel containing Tregs into the injured tissue of mice to see to what extent they promoted tissue healing in bone, muscle and skin. Specifically, they chose three models of acute injury: severe skull defects, loss of skeletal muscle resulting in impaired function, and full-thickness skin wounds. Fibrin is a protein thats naturally involved in wound healing; its the end product of the bodys blood clotting pathway and can also act as a medium for regenerative cells like Tregs.

Compared to those administered fibrin hydrogel without Tregs, mice given Tregs showed enhanced bone volume and coverage over injured cranial areas, higher amounts of muscle tissue and large muscle fiber size, and faster skin wound closure, said Shizuo Akira, a professor from IFReC and a senior author on the study.

Examining the mechanics of the Treg-promoted healing, the researchers observed that the cells adopted an injury-specific phenotype a phenotype is an observable trait after being introduced to the damaged area. The Tregs showed increased levels of expression in genes related to immune system modulation and tissue healing. Further experiments showed that the Tregs caused monocytes and macrophages in damaged tissue to switch to an anti-inflammatory state, specifically by secreting signaling molecules like interleukin-10 (IL-10).

Interestingly, we observed that when the gene encoding IL-10 is knocked out of the Tregs, their pro-healing effects are lost, Martino said. This finding indicates the key role of IL-10 in how these Tregs support tissue repair and regeneration.

The studys findings demonstrate the strong potential for using Tregs as a cell-based regenerative medicine therapy after tissue injury. Although this study examined the effect of Tregs administered immediately post-injury, future studies will determine the time frame in which Tregs need to be administered to damaged tissue to effectively aid healing.

The study was published in the journal Nature Communications.

Source: IFReC

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Regenerative Medicine Foundation

Friday, September 13th, 2024

Regenerative cellular therapies represent the next generation of groundbreaking treatments that are showing great promise in cardiology, neurology, oncology, orthopedics, ophthalmology, and other areas. Several well-designed clinical trials are being conducted under FDA investigational new drug (IND) protocols. At the same time, a handful of clinics have caused patient harm or made questionable claims, taking advantage of vulnerable patients and casting a negative light on this emerging science and industry.

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Regenerative Medicine Foundation

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BridgeBio Receives FDAs Regenerative Medicine Advanced Therapy (RMAT …

Friday, September 13th, 2024

- Receipt of RMAT Designation is based on preliminary clinical evidence from the CANaspire Phase 1/2 clinical trial, which showed functional improvements in all dosed patients indicating that BBP-812 has potential to address the unmet needs of individuals with Canavan disease

- BridgeBio will leverage the benefits of RMAT designation, including early and more frequent interactions with the FDA, to establish an Accelerated Approval pathway for BBP-812

- If approved, BridgeBios gene therapy for Canavan disease could be the first therapeutic option for children born with this devastating and fatal neurodevelopmental disorder

PALO ALTO, Calif., Sept. 10, 2024 (GLOBE NEWSWIRE) -- BridgeBio Pharma, Inc. (Nasdaq: BBIO) (BridgeBio), a commercial-stage biopharmaceutical company focused on genetic diseases, today announced that the United States Food and Drug Administration (FDA) has granted Regenerative Medicine Advanced Therapy (RMAT) designation to BBP-812, an investigational intravenous (IV) adeno-associated virus serotype 9 (AAV9) gene therapy for the treatment of Canavan disease. RMAT designation was granted following the FDAs review of clinical data from the CANaspire Phase 1/2 clinical trial investigating BBP-812 as a potential therapy to address the unmet medical needs of individuals with Canavan disease.

RMAT is an expedited FDA program available to sponsors of regenerative medicine therapies intended to treat, modify, reverse, or cure serious conditions. Benefits of the RMAT designation include all the advantages of the Fast Track and Breakthrough Therapy Designation programs, including faster and more frequent interactions with the FDA to achieve early alignment on critical aspects of the program. FDA granted RMAT designation based on its review of 12 months of safety and efficacy data from the first eight patients with Canavan disease dosed with BBP-812 in the CANaspire Phase 1/2 clinical trial.

We are honored to be granted RMAT designation for BBP-812 and are eager to work closely with the FDA and the Canavan community with the goal of bringing our therapy to families living with Canavan disease as fast as possible, said Eric David, M.D., J.D., CEO at BridgeBio Gene Therapy. We are beyond grateful to the children and their families who are participating in CANaspire, as well as to the study investigators. RMAT will allow us to work more closely with FDA to ensure we are responding to the urgency that families feel.

To date, results from CANaspire show that all patients dosedwith at least one follow-up assessment havedemonstrated improvements in functional outcomes in key areas important to caregivers such as head control, sitting upright, reaching for and grasping objects, and visual tracking. All patients dosed with BBP-812 with at least one follow-up assessment have shownreductions in N-acetylaspartate (NAA), both in urine and in the central nervous system, to levels associated with mild disease. BBP-812 has been well-tolerated, with a safety profile generally consistent with that of other AAV9 gene therapy programs.

Canavan disease is an extremely rare and rapidly progressive neurodegenerative disease that prevents most children from meeting basic developmental milestones, such as crawling, walking, speaking, and even holding their heads up. It is a terminal diagnosis with no approved treatment to date. The news of the RMAT designation, coupled with the preliminary results seen in the clinical trial, provides hope to children worldwide living with Canavan disease and their families, said Kathleen Flynn,CEO of National Tay-Sachs & Allied Diseases Association, an advocacy organization dedicated to driving research, forging collaboration, and supporting families within the Tay-Sachs, Canavan, GM1, and Sandhoff disease communities.

In addition to RMAT designation, BBP-812 has been granted Orphan Drug, Rare Pediatric Disease (RPDD), and Fast Track Designations from the FDA, as well as Orphan Drug Designation from the European Medicines Agency. With RPDD, if approved, BridgeBio may qualify for a Priority Review Voucher.

About CANaspireCANaspire is a Phase 1/2 open-label study designed to evaluate the safety, tolerability, and pharmacodynamic activity of BridgeBios AAV9 gene therapy candidate, BBP-812, in pediatric patients with Canavan disease. Each eligible patient will receive a single IV infusion of BBP-812. The primary outcomes of the study are safety, as well as change from baseline of urine and central nervous system NAA levels. Motor function and development will also be assessed.

For more information about the CANaspire trial, visit TreatCanavan.com or ClinicalTrials.gov (NCT04998396).

About Canavan DiseaseAffecting approximately 1,000 children in the U.S. and European Union, Canavan disease is an ultra-rare, disabling and fatal disease with no approved therapy. Most children are not able to meet developmental milestones, are unable to crawl, walk, sit or talk, and die at a young age. The disease is caused by an inherited mutation of the ASPA gene that codes for aspartoacylase, a protein that breaks down a compound called NAA. Deficiency of aspartoacylase activity results in accumulation of NAA, and ultimately results in toxicity to myelin in ways that are not currently well understood. Myelin insulates neuronal axons, and without it, neurons are unable to send and receive messages as they should. The current standard of care for Canavan disease is limited to supportive therapy.

About BridgeBio Pharma, Inc.BridgeBio Pharma, Inc. (BridgeBio) is a commercial-stage biopharmaceutical company founded to discover, create, test and deliver transformative medicines to treat patients who suffer from genetic diseases. BridgeBios pipeline of development programs ranges from early science to advanced clinical trials. BridgeBio was founded in 2015 and its team of experienced drug discoverers, developers and innovators are committed to applying advances in genetic medicine to help patients as quickly as possible. For more information visitbridgebio.comand follow us onLinkedIn,Twitter and Facebook.

BridgeBio Pharma, Inc. Forward-Looking StatementsThis press release contains forward-looking statements. Statements BridgeBio makes in this press release may include statements that are not historical facts and are considered forward-looking within the meaning of Section 27A of the Securities Act of 1933, as amended (the Securities Act), and Section 21E of the Securities Exchange Act of 1934, as amended (the Exchange Act), which are usually identified by the use of words such as anticipates, believes, continues, estimates, expects, hopes, intends, may, plans, projects, remains, seeks, should, will, and variations of such words or similar expressions. BridgeBio intends these forward-looking statements to be covered by the safe harbor provisions for forward-looking statements contained in Section 27A of the Securities Act and Section 21E of the Exchange Act. These forward-looking statements, including statements relating to the timing and success of BridgeBios Phase 1/2 clinical trial of BBP-812 for the treatment of Canavan disease, expectations, plans and prospects regarding BridgeBios regulatory approval process for BBP-812, the ability of BBP-812 to be the first therapeutic treatment option for children born with Canavan disease, reflect BridgeBios current views about its plans, intentions, expectations, strategies and prospects, which are based on the information currently available to BridgeBio and on assumptions BridgeBio has made. Although BridgeBio believes that its plans, intentions, expectations, strategies and prospects as reflected in or suggested by those forward-looking statements are reasonable, BridgeBio can give no assurance that the plans, intentions, expectations or strategies will be attained or achieved. Furthermore, actual results may differ materially from those described in the forward-looking statements and will be affected by a number of risks, uncertainties and assumptions, including, but not limited to, BridgeBios ability to continue and complete its Phase 1/2 clinical trial of BBP-812 for the treatment of Canavan disease, BridgeBios ability to advance BBP-812 in clinical development according to its plans, the ability of BBP-812 to treat Canavan disease, the ability of BBP-812 to retain Fast Track Designation, Rare Pediatric Drug Designation, Regenerative Medicine Advanced Therapy Designation and Orphan Drug Designation from the U.S. Food and Drug Administration and Orphan Drug Designation from the European Medicines Agency, and potential adverse impacts due to global health emergencies, including delays in regulatory review, manufacturing and supply chain interruptions, adverse effects on healthcare systems and disruption of the global economy, the impacts of current macroeconomic and geopolitical events, including changing conditions from hostilities in Ukraine and in Israel and the Gaza Strip, increasing rates of inflation and rising interest rates, on our business operations and expectations as well as those risks set forth in the Risk Factors section of BridgeBios most recent Annual Report on Form 10-K, and BridgeBios other filings with the U.S. Securities and Exchange Commission. Moreover, BridgeBio operates in a very competitive and rapidly changing environment in which new risks emerge from time to time. These forward-looking statements are based upon the current expectations and beliefs of BridgeBios management as of the date of this press release and are subject to certain risks and uncertainties that could cause actual results to differ materially from those described in the forward-looking statements. Except as required by applicable law, we assume no obligation to update publicly any forward-looking statements, whether as a result of new information, future events or otherwise.

BridgeBio Contact:Vikram Balicontact@bridgebio.com(650)-789-8220

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