Abstract
The skin is one of the crucial body organs with anatomy and physiology linked to various disorders including congenital and acquired diseases. Nowadays, mesenchymal stem cell (MSCs)- based therapy has appeared as a promising therapeutic field, in which many see opportunities to cure the costliest and incurable diseases. However, one question to be asked is that if the use of MSCs in clinical trials studies and diseases treatment has improved. In this study, the clinical trials using MSCs in skin diseases were reviewed. A remarkable number of clinical trial studies are in progress in this field; however, only a few of them have led to tangible benefits for patients. The relevant papers and ongoing clinical trials that address MSC’s therapeutic goals for various skin disorders were examined. This review can be very useful for both the dermatologists and basic skin researchers interested in contributing to stem cell-based therapeutic researches in the area of skin disorders.
Keywords: Cell therapy, clinical trial, mesenchymal stem cells, skin diseases, cell-based, dermatologists.
[1]
Golchin A, Niknejad H. Cell therapy using embryonic stem cell source in clinical trial studies: advantages and limitations. J Maz Univ Med Sci 2017; 27(148): 161-75.
[2]
Ardeshirylajimi A. Applied induced pluripotent stem cells in combination with biomaterials in bone tissue engineering. J Cell Biochem 2017; 118(10): 3034-42.
[3]
Wei X, Yang X, Han Z, Qu F, Shao L, Shi Y. Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacol Sin 2013; 34(6): 747-54.
[4]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[5]
Ardeshirylajimi A, Mossahebi-Mohammadi M, Vakilian S, et al. Comparison of osteogenic differentiation potential of human adult stem cells loaded on bioceramic-coated electrospun poly (L-lactide) nanofibres. Cell Prolif 2015; 48(1): 47-58.
[6]
Parekkadan B, Milwid JM. Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng 2010; 12: 87-117.
[7]
Fouillard L, Chapel A, Bories D, et al. Infusion of allogeneic-related HLA mismatched mesenchymal stem cells for the treatment of incomplete engraftment following autologous haematopoietic stem cell transplantation. Leukemia 2007; 21(3): 568-70.
[8]
National Library of Medicine. ClinicalTrials.gov.. https://clinicaltrials.gov/ct2/home (Accessed 2018 Jan 19).
[9]
Jouybar A, Seyedjafari E, Ardeshirylajimi A, et al. Enhanced skin regeneration by herbal extract-coated poly-l-lactic acid nanofibrous scaffold. Artif Organs 2017; 41(11): E296-307.
[10]
Piran M, Vakilian S, Piran M, Mohammadi-Sangcheshmeh A, Hosseinzadeh S, Ardeshirylajimi A. In vitro fibroblast migration by sustained release of PDGF-BB loaded in chitosan nanoparticles incorporated in electrospun nanofibers for wound dressing applications. Artif Cells Nanomed Biotechnol 2018; 1-10.
[11]
Toma JG, Akhavan M, Fernandes KJL, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 2001; 3(9): 778-84.
[12]
Lai D, Wang F, Dong Z, Zhang Q. Skin-Derived Mesenchymal Stem Cells Help Restore Function to Ovaries in a Premature Ovarian Failure Mouse Model.Franks S, editor PLoS One. 2014; 9: p. (5)e98749.
[13]
Dyce PW, Zhu H, Craig J, Li J. Stem cells with multilineage potential derived from porcine skin. Biochem Biophys Res Commun 2004; 316(3): 651-8.
[14]
Toma JG, McKenzie IA, Bagli D, Miller FD. Isolation and Characterization of Multipotent Skin-Derived Precursors from Human Skin. Stem Cells 2005; 23(6): 727-37.
[15]
Hoogduijn MJ, Gorjup E, Genever PG. Comparative characterization of hair follicle dermal stem cells and bone marrow mesenchymal stem cells. Stem Cells Dev 2006; 15(1): 49-60.
[16]
Lako M, Armstrong L, Cairns PM, Harris S, Hole N, Jahoda CAB. Hair follicle dermal cells repopulate the mouse haematopoietic system. J Cell Sci 2002; 115(Pt 20): 3967-74.
[17]
Jahoda CAB, Whitehouse J, Reynolds AJ, Hole N. Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp Dermatol 2003; 12(6): 849-59.
[18]
Sellheyer K, Krahl D. Skin mesenchymal stem cells: Prospects for clinical dermatology. J Am Acad Dermatol 2010; 63(5): 859-65.
[19]
Laverdet B, Micallef L, Lebreton C, et al. Use of mesenchymal stem cells for cutaneous repair and skin substitute elaboration. Pathol Biol 2014; 62(2): 108-17.
[20]
Füllgrabe A. Epidermal stem cells in physiological tissue regeneration, wound healing and cancer Thesis, Karolinska Institutet: Huddinge, February 2016.
[21]
Morris RJ, Bortner CD, Cotsarelis G, et al. Enrichment for Living Murine Keratinocytes from the Hair Follicle Bulge with the Cell Surface Marker CD34. J Invest Dermatol 2003; 120(4): 501-11.
[22]
Liu Y, Lyle S, Yang Z, Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J Invest Dermatol 2003; 121(5): 963-8.
[23]
Jaks V, Barker N, Kasper M, et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 2008; 40(11): 1291-9.
[24]
Page ME, Lombard P, Ng F, Göttgens B, Jensen KB. The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell 2013; 13(4): 471-82.
[25]
Brownell I, Guevara E, Bai CB, Loomis CA, Joyner AL. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 2011; 8(5): 552-65.
[26]
Ritsu M, Kawakami K, Kanno E, et al. Critical role of tumor necrosis factor-α in the early process of wound healing in skin. J Dermatology Dermatologic Surg 2017; 21(1): 14-9.
[27]
Frye M, Gardner C, Li ER, Arnold I, Watt FM. Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development 2003; 130(12): 2793-808.
[28]
Ruetze M, Knauer T, Gallinat S, et al. A novel niche for skin derived precursors in non-follicular skin. J Dermatol Sci 2013; 69(2): 132-9.
[29]
Nagel S, Rohr F, Weber C, et al. Multipotent nestin-positive stem cells reside in the stroma of human eccrine and apocrine sweat glands and can be propagated robustly in vitro. Amendola R, editor.PLoS One. 2013; 8: p. (10)e78365.
[30]
Liu L, Chiu PWY, Lam PK, et al. Effect of local injection of mesenchymal stem cells on healing of sutured gastric perforation in an experimental model. Br J Surg 2015; 102(2): e158-68.
[31]
Qi Y, Jiang D, Sindrilaru A, et al. TSG-6 released from intradermally injected mesenchymal stem cells accelerates wound healing and reduces tissue fibrosis in murine full-thickness skin wounds. J Invest Dermatol 2014; 134: 526-37.
[32]
Jackson WM, Nesti LJ, Tuan RS. Concise review: Clinical translation of wound healing therapies based on mesenchymal stem cells. Stem Cells Transl Med 2012; 1(1): 44-50.
[33]
Lam P, Cheng S, Lo W, et al. Topical application of mesenchymal stem cells for the treatment of chronic wounds- a pilot study. Cytotherapy 2017; 19(5): S227.
[34]
Duscher D, Barrera J, Wong VW, et al. Stem cells in wound healing: The future of regenerative medicine? A mini-review. Gerontology 2016; 62(2): 216-25.
[35]
Golchin A, Hosseinzadeh S, Roshangar L. The role of nanomaterials in cell delivery systems. Med Mol Morphol 2017; 51(1): 1-12.
[36]
Maxson S, Lopez EA, Yoo D, Danilkovitch-Miagkova A, LeRoux MA. Concise review: Role of mesenchymal stem cells in wound repair. Stem Cells Transl Med 2012; 1(2): 142-9.
[37]
Falanga V, Iwamoto S, Chartier M, et al. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng 2007; 13(6): 1299-312.
[38]
Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007; 100(9): 1249-60.
[39]
Golchin A, Rekabgardan M, Taheri RA, Nourani MR. Promotion of cell-based therapy: special focus on the cooperation of mesenchymal stem cell therapy and gene therapy for clinical trial studies. Adv Exp Med Biol 2018. [Epub ahead of print].
[40]
Hu R, Ling W, Xu W, Han D. Fibroblast-like cells differentiated from adipose-derived mesenchymal stem cells for vocal fold wound healing.Zhou Z, editor PLoS One . 2014; 9: p. (3)e92676.
[41]
Gnecchi M, Danieli P, Malpasso G, Ciuffreda MC. Paracrine mechanisms of mesenchymal stem cells in tissue repair. Methods Mol Biol 2016; 1416: 123-46.
[42]
Nuschke A. Activity of mesenchymal stem cells in therapies for chronic skin wound healing. Organogenesis 2014; 10(1): 29-37.
[43]
Zhang Q-Z, Su W-R, Shi S-H, et al. Human gingiva-derived mesenchymal stem cells elicit polarization of M2 macrophages and enhance cutaneous wound healing. Stem Cells 2010; 28(10): 1856-68.
[44]
Glenn JD, Whartenby KA. Mesenchymal stem cells: Emerging mechanisms of immunomodulation and therapy. World J Stem Cells 2014; 6(5): 526-39.
[45]
de Mayo T, Conget P, Becerra-Bayona S, Sossa CL, Galvis V, Arango-Rodríguez ML. The role of bone marrow mesenchymal stromal cell derivatives in skin wound healing in diabetic mice.Fiorina P, editor PLoS One. 2017; 12: p. (6)e0177533.
[46]
Li M, Zhao Y, Hao H, et al. Mesenchymal stem cell-conditioned medium improves the proliferation and migration of keratinocytes in a diabetes-like microenvironment. Int J Low Extrem Wounds 2015; 14(1): 73-86.
[47]
Hong SJ, Jia S-X, Xie P, et al. Topically delivered adipose derived stem cells show an activated-fibroblast phenotype and enhance granulation tissue formation in skin wounds.Eisenberg L, editor PLoS One. 2013; 8: p. (1)e55640.
[48]
Kosaraju R, Rennert RC, Maan ZN, et al. Adipose-derived stem cell-seeded hydrogels increase endogenous progenitor cell recruitment and neovascularization in wounds Tissue Eng Part A [Internet] Mary Ann Liebert, Inc 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA 2016; 22(3-4): 295-305.
[50]
Fine J-D. J Eady RA, Bauer EA, et al. The classification of inherited epidermolysis bullosa (EB): Report of the third international consensus meeting on diagnosis and classification of EB. J Am Acad Dermatol 2008; 58(6): 931-50.
[51]
Fine J-D, Bruckner-Tuderman L. J Eady RA, et al Inherited epidermolysis bullosa: Updated recommendations on diagnosis and classification. J Am Acad Dermatol 2014; 70(6): 1103-26.
[52]
Conget P, Rodriguez F, Kramer S, Allers C, Simon V, Palisson F, et al. Replenishment of type VII collagen and re-epithelialization of chronically ulcerated skin after intradermal administration of allogeneic mesenchymal stromal cells in two patients with recessive dystrophic epidermolysis bullosa. Cytotherapy 2010; 12: 429-31.
[53]
Petrof G, Lwin SM, Martinez-Queipo M, et al. Potential of systemic allogeneic mesenchymal stromal cell therapy for children with recessive dystrophic epidermolysis bullosa. J Invest Dermatol 2015; 135: 2319-21.
[54]
El-Darouti M, Fawzy M, Amin I, et al. Treatment of dystrophic epidermolysis bullosa with bone marrow non-hematopoeitic stem cells: A randomized controlled trial. Dermatologic Therapy 2016; 29: 96-100.
[55]
Jacków J, Titeux M, Portier S, et al. Gene-corrected fibroblast therapy for recessive dystrophic epidermolysis bullosa using a self-inactivating COL7A1 retroviral vector. J Invest Dermatol 2016; 136(7): 1346-54.
[56]
Venugopal SS, Yan W, Frew JW, Cohn HI, Rhodes LM, Tran K, et al. A phase II randomized vehicle-controlled trial of intradermal allogeneic fibroblasts for recessive dystrophic epidermolysis bullosa. J Am Acad Dermatol 2013; 69(6): 898-908.e7.
[57]
Petrof G, Martinez-Queipo M, Mellerio JE, Kemp P, McGrath JA. Fibroblast cell therapy enhances initial healing in recessive dystrophic epidermolysis bullosa wounds: results of a randomized, vehicle-controlled trial. Br J Dermatol 2013; 169(5): 1025-33.
[58]
Siprashvili Z, Nguyen NT, Gorell ES, et al. Safety and wound outcomes following genetically corrected autologous epidermal grafts in patients with recessive dystrophic epidermolysis bullosa. JAMA 2016; 316(17): 1808.
[59]
Siprashvili NN, Gorell E, Khuu P, et al. Phase I clinical trial of genetically corrected autologous epidermal keratinocytes for recessive dystrophic epidermolysis bullosa. J Invest Dermatol 2014; 134.
[60]
Silverberg JI, Hanifin JM. Adult eczema prevalence and associations with asthma and other health and demographic factors: A US population-based study. J Allergy Clin Immunol 2013; 132(5): 1132-8.
[61]
Lio PA, Lee M, LeBovidge J, Timmons KG, Schneider L. Clinical management of atopic dermatitis: Practical highlights and updates from the atopic dermatitis practice parameter 2012. J Allergy Clin Immunol Pract 2014; 2(4): 361-9.
[62]
American academy of family physicians. atopic dermatitis: An overview. http://www.aafp.org/afp/2012/0701/p35.html ( Accessed August 5, 2018).
[63]
Na K, Yoo HS, Zhang YX, et al. Bone marrow-derived clonal mesenchymal stem cells inhibit ovalbumin-induced atopic dermatitis. Cell Death Dis 2014; 5: e1345.
[64]
Kim H-S, Yun J-W, Shin T-H, et al. Human Umbilical Cord Blood Mesenchymal Stem Cell-Derived PGE 2 and TGF-β1 Alleviate Atopic Dermatitis by Reducing Mast Cell Degranulation. Stem Cells 2015; 33: 1254-66.
[65]
Hall MN, Rosenkrantz WS, Hong JH, Griffin CE, Mendelsohn CM. Evaluation of the potential use of adipose-derived mesenchymal stromal cells in the treatment of canine atopic dermatitis: a pilot study. Vet Ther 2010; 11(2): E1-E14.
[66]
Bizikova P, Pucheu-Haston CM, Eisenschenk MNC, Marsella R, Nuttall T, Santoro D. Review: Role of genetics and the environment in the pathogenesis of canine atopic dermatitis. Vet Dermatol 2015; 26(2): 95-e26.
[67]
Webb TL, Webb CB. Stem cell therapy in cats with chronic enteropathy: a proof-of-concept study. J Feline Med Surg 2015; 17(10): 901-8.
[68]
Kim H-S, Lee JH, Roh K-H, Jun HJ, Kang K-S, Kim T-Y. Clinical Trial of Human Umbilical Cord Blood-Derived Stem Cells for the Treatment of Moderate-to-Severe Atopic Dermatitis: Phase I/IIa Studies. Stem Cells 2017; 35(1): 248-55.
[69]
Wehbe T, Abi Saab M, Abi Chahine N, Margossian T. Mesenchymal stem cell therapy for refractory scleroderma: A report of 2 cases. Stem Cell Investig 2016; 3: 48.
[70]
Isakson M, de Blacam C, Whelan D, McArdle A, Clover AJP. Mesenchymal stem cells and cutaneous wound healing: current evidence and future potential. Stem Cells Int 2015; 2015: 831095.
[71]
Hocking AM. Mesenchymal stem cell therapy for cutaneous wounds. Adv Wound Care (New Rochelle) 2012; 1(4): 166-71.
[72]
Badiavas EV, Falanga V. Treatment of chronic wounds with bone marrow-derived cells. Arch Dermatol 2003; 139(4): 510.
[73]
Yoshikawa T, Mitsuno H, Nonaka I, et al. Wound Therapy by Marrow Mesenchymal Cell Transplantation. Plast Reconstr Surg 2008; 121(3): 860-77.
[74]
Teraa M, Sprengers RW, van der Graaf Y, Peters CEJ, Moll FL, Verhaar MC. Autologous bone marrow-derived cell therapy in patients with critical limb ischemia. Ann Surg 2013; 258(6): 922-9.
[75]
Dubský M, Jirkovská A, Bem R, et al. Comparison of the effect of stem cell therapy and percutaneous transluminal angioplasty on diabetic foot disease in patients with critical limb ischemia. Cytotherapy 2014; 16(12): 1733-8.
[76]
Gupta PK, Chullikana A, Parakh R, et al. A double blind randomized placebo controlled phase I/II study assessing the safety and efficacy of allogeneic bone marrow derived mesenchymal stem cell in critical limb ischemia. J Transl Med 2013; 11: 143.
[77]
Bura A, Planat-Benard V, Bourin P, et al. Phase I trial: the use of autologous cultured adipose-derived stroma/stem cells to treat patients with non-revascularizable critical limb ischemia. Cytotherapy 2014; 16(2): 245-57.
[78]
Klepanec A, Mistrik M, Altaner C, et al. No Difference in Intra-Arterial and Intramuscular Delivery of Autologous Bone Marrow Cells in Patients with Advanced Critical Limb Ischemia. Cell Transplant 2012; 21(9): 1909-18.
[79]
Bartsch T, Brehm M, Falke T, Kögler G, Wernet P, Strauer B-E. Schnelle Abheilung eines therapierefraktären diabetischen Fußes nach autologer Knochen markstammzell transplantation. Medizinische Klinik 2005; 100(10): 676-80.
[80]
Vojtassák J, Danisovic L, Kubes M, et al. Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot. NeuroEndocrinol Lett 2006; 27(2): 134-7.
[81]
Dash NR, Dash SN, Routray P, Mohapatra S, Mohapatra PC. Targeting nonhealing ulcers of lower extremity in human through autologous bone marrow-derived mesenchymal stem cells. Rejuvenation Res 2009; 12(5): 359-66.
[82]
Lu D, Chen B, Liang Z, et al. Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: A double-blind, randomized, controlled trial. Diabetes Res Clin Pract 2011; 92(1): 26-36.
[83]
Li X-Y, Zheng Z-H, Li X-Y, et al. Treatment of foot disease in patients with type 2 diabetes mellitus using human umbilical cord blood mesenchymal stem cells: response and correction of immunological anomalies. Curr Pharm Des 2013; 19(27): 4893-9.
[84]
Qin H, Zhu X, Zhang B, Zhou L, Wang W. Clinical evaluation of human umbilical cord mesenchymal stem cell transplantation after angioplasty for diabetic foot. Exp Clin Endocrinol Diabetes 2016; 124(18): 497-503.
[85]
Zeng X, Tang Y, Hu K, et al. Three-week topical treatment with placenta-derived mesenchymal stem cells hydrogel in a patient with diabetic foot ulcer: A case report. Medicine (Baltimore) 2017; 96(51): e9212.
[86]
Rasulov MF, Vasilchenkov AV, Onishchenko NA, et al. First experience of the use bone marrow mesenchymal stem cells for the treatment of a patient with deep skin burns. Bull Exp Biol Med 2005; 139(1): 141-4.
[87]
Lataillade J, Doucet C, Bey E, et al. New approach to radiation burn treatment by dosimetry-guided surgery combined with autologous mesenchymal stem cell therapy. Regen Med 2007; 2(5): 785-94.
[88]
Bey E, Prat M, Duhamel P, et al. Emerging therapy for improving wound repair of severe radiation burns using local bone marrow-derived stem cell administrations. Wound Repair Regen 2010; 18(1): 50-8.
[89]
Mansilla E, Marín GH, Berges M, et al. Cadaveric bone marrow mesenchymal stem cells: First experience treating a patient with large severe burns. Burns Trauma 2015; 3: 17.
[90]
Portas M, Mansilla E, Drago H, et al. Use of Human Cadaveric Mesenchymal Stem Cells for Cell Therapy of a Chronic Radiation-Induced Skin Lesion. Radiat Prot Dosimetry 2016; 171(1): 99-106.
[91]
Abo-Elkheir W, Hamza F, Elmofty AM, et al. Role of cord blood and bone marrow mesenchymal stem cells in recent deep burn: a case-control prospective study. Am J Stem Cells 2017; 6(3): 23-35.
[92]
Zhou H, Guo M, Bian C, et al. Efficacy of bone marrow-derived mesenchymal stem cells in the treatment of sclerodermatous chronic graft-versus-host disease: clinical report. Biol Blood Marrow Transplant 2010; 16(3): 403-12.
[93]
Pérez-Simon JA, López-Villar O, Andreu EJ, et al. Mesenchymal stem cells expanded in vitro with human serum for the treatment of acute and chronic graft-versus-host disease: results of a phase I/II clinical trial. Haematologica 2011; 96(7): 1072-6.
[94]
Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008; 371(9624): 1579-86.
[95]
Chen H, Niu J-W, Ning H-M, et al. Treatment of Psoriasis with Mesenchymal Stem Cells. Am J Med 2016; 129(3): e13-4.
[96]
De Jesus MM, Santiago JS, Trinidad CV, et al. Autologous adipose-derived mesenchymal stromal cells for the treatment of psoriasis vulgaris and psoriatic arthritis: A case report. Cell Transplant 2016; 25(11): 2063-9.
[97]
Wang D, Li J, Zhang Y, et al. Umbilical cord mesenchymal stem cell transplantation in active and refractory systemic lupus erythematosus: a multicenter clinical study. Arthritis Res Ther 2014; 16(2): R79.
[98]
Liang J, Zhang H, Hua B, et al. Allogenic mesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis 2010; 69(8): 1423-9.
[99]
Blum BBN, Blum B, Benvenisty N. The tumorigenicity of human embryonic stem cells. Adv Cancer Res 2008; 100: 133-58.
[100]
Revilla A, González C, Iriondo A, et al. Current advances in the generation of human iPS cells: implications in cell-based regenerative medicine. J Tissue Eng Regen Med 2016; 10: 893-907.
[101]
Nooshabadi VT, Mardpour S, Yousefi‐Ahmadipour A, et al. The extracellular vesicles‐derived from mesenchymal stromal cells: A new therapeutic option in regenerative medicine. J Cell Biochem 2018; 119(10): 8048-73.
[102]
Sakaida I, Terai S, Yamamoto N, et al. Transplantation of bone marrow cells reduces CCl 4 -induced liver fibrosis in mice. Hepatology 2004; 40: 1304-11.
[103]
Nandi S, Tripathi SK, Gupta PSP, Mondal S. Effect of metabolic stressors on survival and growth of in vitro cultured ovine preantral follicles and enclosed oocytes. Theriogenology 2017; 104: 80-6.
[104]
Golchin A, Asadpour R, Roshangar L, Jafari-Jozani R. The effect of ammonium chloride concentration in in vitro maturation culture on ovine embryo development. J Reprod Infertil 2016; 17: 144-50.
[105]
Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 2014; 14: 195-208.
[106]
Zhang B, Wang M, Gong A, et al. HucMSC-Exosome mediated-wnt4 signaling is required for cutaneous wound healing. Stem Cells 2015; 33: 2158-68.
[107]
Bruno S, Grange C, Collino F, et al. Microvesicles Derived from Mesenchymal Stem Cells Enhance Survival in a Lethal Model of Acute Kidney Injury. PLoS ONE 2012; 7: e33115.
[108]
Kim Y-J. Yoo Smi, Park HH, et al Exosomes derived from human umbilical cord blood mesenchymal stem cells stimulates rejuvenation of human skin. Biochem Biophys Res Commun 2017; 493: 1102-8.
[109]
Shi Q, Qian Z, Liu D, et al. GMSC-Derived Exosomes Combined with a Chitosan/Silk Hydrogel Sponge Accelerates Wound Healing in a Diabetic Rat Skin Defect Model. Front Physiol 2017; 8: 904.
[110]
Fang S, Xu C, Zhang Y, et al. Umbilical Cord-Derived Mesenchymal Stem Cell-Derived Exosomal MicroRNAs Suppress Myofibroblast Differentiation by Inhibiting the Transforming Growth Factor-β/SMAD2 Pathway During Wound Healing. Stem Cells Transl Med 2016; 5: 1425-39.
[111]
Blazquez R, Sanchez-Margallo FM, de la Rosa O, et al. Immunomodulatory Potential of Human Adipose Mesenchymal Stem Cells Derived Exosomes on in vitro Stimulated T Cells. Front Immunol 2014; 5: 556.
[112]
Golchin A, Hosseinzadeh S, Ardeshirylajimi A. The exosomes released from different cell types and their effects in wound healing. J Cell Biochem 2018; 119(7): 5043-52.
[113]
Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJP, Tahan SR. Increased expression of stem cell markers in malignant melanoma. Modern Pathology 2007; 20: 102-7.
[114]
Carrion F, Nova E, Ruiz C, et al. Autologous mesenchymal stem cell treatment increased T regulatory cells with no effect on disease activity in two systemic lupus erythematosus patients. Lupus 2010; 19(3): 317-22.
Article Metrics
78
14