The application of human Wharton's jelly mesenchymal stem cells in wound healing: A narrative review

Reza Rezaee, Javad Verdi, Mahsa Sadeghi, Mehran Soleymanha, Mojtaba Mirzaei, Mohammad Reza Mobayen, Arad Kianoush

Abstract


Management and treatment of chronic wounds remain a significant problem in clinical practice. Stem cell therapies are an important and promising approach for regenerative medicine because of their self-renewal and differentiation potential. Mesenchymal stem cells (MSCs), a major cellular source for regeneration, are present in almost all tissues. The use of embryonic stem cells is morally controversial because of the need to nurture and destroy embryonic cells. Therefore, adult umbilical cord tissues are of particular importance as an alternative source of perinatal tissues. Wharton Jelly is a gelatinous connective tissue in the umbilical cord containing MSCs that can differentiate into osteogenic, adipose, chondrogenic, and other lineages. These cells do not express the MHC-II molecule and show immunomodulatory properties that make them viable for allogeneic and xenogenic transplants in cell therapy. Therefore, the umbilical cord, especially the part named Wharton's jelly, is an important and promising source of mesenchymal stem cells.


Keywords


Stem cells; Wharton's Jelly; Cell therapy; Wound healing; Regenerative medicine

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References


Kim DJ, Mustoe T, Clark RA. Cutaneous wound healing in aging small mammals: a systematic review. Wound Repair Regen. 2015; 23(3):318-39.

Agarwal PK, Singh A, Gaurav K, Goel S, Khanna HD, Goel RK. Evaluation of wound healing activity of extracts of plantain banana (Musa sapientum var. paradisiaca) in rats. Indian J Exp Biol. 2009; 47(1):32-40.

Murthy S, Gautam MK, Goel S, Purohit V, Sharma H, Goel RK. Evaluation of in vivo wound healing activity of Bacopa monniera on different wound model in rats. Biomed Res Int. 2013; 2013:972028.

Diegelmann RF, Evans MC. Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci. 2004; 9:283-9.

Jayaraman P, Nathan P, Vasanthan P, Musa S, Govindasamy V. Stem cells conditioned medium: a new approach to skin wound healing management. Cell Biol Int. 2013; 37(10):1122-8.

Ghieh F, Jurjus R, Ibrahim A, Geagea AG, Daouk H, El Baba B, et al. The Use of Stem Cells in Burn Wound Healing: A Review. Biomed Res Int. 2015; 2015:684084.

Hassan WU, Greiser U, Wang W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen. 2014; 22(3):313-25.

Raaijmakers MH. Overview of stem cells. 2019. Availible from: https://www.uptodate.com/contents/overview-of-stem-cells

Sabapathy V, Sundaram B, V MS, Mankuzhy P, Kumar S. Human Wharton's Jelly Mesenchymal Stem Cells plasticity augments scar-free skin wound healing with hair growth. PLoS One. 2014; 9(4):e93726.

Abbaszadeh H, Ghorbani F, Derakhshani M, Movassaghpour AA, Yousefi M, Talebi M, et al. Regenerative potential of Wharton's jelly-derived mesenchymal stem cells: A new horizon of stem cell therapy. J Cell Physiol. 2020; 235(12):9230-40.

Cui HS, Joo SY, Cho YS, Park JH, Kim JB, Seo CH. Effect of Combining Low Temperature Plasma, Negative Pressure Wound Therapy, and Bone Marrow Mesenchymal Stem Cells on an Acute Skin Wound Healing Mouse Model. Int J Mol Sci. 2020; 21(10):3675.

Peng Y, Xuan M, Zou J, Liu H, Zhuo Z, Wan Y, et al. Freeze-dried rat bone marrow mesenchymal stem cell paracrine factors: a simplified novel material for skin wound therapy. Tissue Eng Part A. 2015; 21(5-6):1036-46.

Abo-Elkheir W, Hamza F, Elmofty AM, Emam A, Abdl-Moktader M, Elsherefy S, 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.

Himal I, Goyal U, Ta M. Evaluating Wharton's Jelly-Derived Mesenchymal Stem Cell's Survival, Migration, and Expression of Wound Repair Markers under Conditions of Ischemia-Like Stress. Stem Cells Int. 2017; 2017:5259849.

Shi Y, Su J, Roberts AI, Shou P, Rabson AB, Ren G. How mesenchymal stem cells interact with tissue immune responses. Trends Immunol. 2012; 33(3):136-43.

Tamama K, Kerpedjieva SS. Acceleration of Wound Healing by Multiple Growth Factors and Cytokines Secreted from Multipotential Stromal Cells/Mesenchymal Stem Cells. Adv Wound Care (New Rochelle). 2012; 1(4):177-82.

Doi H, Kitajima Y, Luo L, Yan C, Tateishi S, Ono Y, et al. Potency of umbilical cord blood- and Wharton's jelly-derived mesenchymal stem cells for scarless wound healing. Sci Rep. 2016; 6:18844.

Kamolz LP, Keck M, Kasper C. Wharton's jelly mesenchymal stem cells promote wound healing and tissue regeneration. Stem Cell Res Ther. 2014; 5(3):62.

Can A, Karahuseyinoglu S. Concise review: human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells. 2007; 25(11):2886-95.

Varaa N, Azandeh S, Khodabandeh Z, Gharravi AM. Wharton's Jelly Mesenchymal Stem Cell: Various Protocols for Isolation and Differentiation of Hepatocyte-Like Cells; Narrative Review. Iran J Med Sci. 2019; 44(6):437-48.

Sobolewski K, Małkowski A, Bańkowski E, Jaworski S. Wharton's jelly as a reservoir of peptide growth factors. Placenta. 2005; 26(10):747-52.

Kuroda Y, Kitada M, Wakao S, Dezawa M. Mesenchymal stem cells and umbilical cord as sources for schwann cell differentiation: their potential in peripheral nerve repair. Open Tissue Eng Regen Med J. 2011; 4(1):54-63.

Du T, Zou X, Cheng J, Wu S, Zhong L, Ju G, et al. Human Wharton's jelly-derived mesenchymal stromal cells reduce renal fibrosis through induction of native and foreign hepatocyte growth factor synthesis in injured tubular epithelial cells. Stem Cell Res Ther. 2013; 4(3):59.

Moodley Y, Atienza D, Manuelpillai U, Samuel CS, Tchongue J, Ilancheran S, et al. Human umbilical cord mesenchymal stem cells reduce fibrosis of bleomycin-induced lung injury. Am J Pathol. 2009; 175(1):303-13.

Lo Iacono M, Anzalone R, Corrao S, Giuffrè M, Di Stefano A, Giannuzzi P, et al. Perinatal and wharton's jelly-derived mesenchymal stem cells in cartilage regenerative medicine and tissue engineering strategies. Open Tissue Eng Regen Med J. 2011; 4(1):72-81.

Tamura M, Kawabata A, Ohta N, Uppalapati L, G Becker K, Troyer D. Wharton's jelly stem cells as agents for cancer therapy. Open Tissue Eng Regen Med J. 2011; 4(1):39-47.

Zhang Y, Hao H, Liu J, Fu X, Han W. Repair and regeneration of skin injury by transplanting microparticles mixed with Wharton's jelly and MSCs from the human umbilical cord. Int J Low Extrem Wounds. 2012; 11(4):264-70.

Tam K, Cheyyatraviendran S, Venugopal J, Biswas A, Choolani M, Ramakrishna S, et al. A nanoscaffold impregnated with human wharton's jelly stem cells or its secretions improves healing of wounds. J Cell Biochem. 2014; 115(4):794-803.

Stefańska K, Ożegowska K, Hutchings G, Popis M, Moncrieff L, Dompe C, et al. Human Wharton's Jelly-Cellular Specificity, Stemness Potency, Animal Models, and Current Application in Human Clinical Trials. J Clin Med. 2020; 9(4):1102.

Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS One. 2010; 5(2):e9016.

Deuse T, Stubbendorff M, Tang-Quan K, Phillips N, Kay MA, Eiermann T, et al. Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant. 2011; 20(5):655-67.

Arno AI, Amini-Nik S, Blit PH, Al-Shehab M, Belo C, Herer E, et al. Human Wharton's jelly mesenchymal stem cells promote skin wound healing through paracrine signaling. Stem Cell Res Ther. 2014; 5(1):28.

Graham-Brown R, Burns T. Dermatology: lecture notes: John Wiley & Sons; 2011.

Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med. 1999; 341(10):738-46.

Kujath P, Michelsen A. Wounds - from physiology to wound dressing. Dtsch Arztebl Int. 2008; 105(13):239-48.

Mobayen M, Rimaz S, Malekshahi A. Evaluation of clinical and laboratory causes of burns in pre-school children. J Curr Biomed Rep. 2021; 2(1):27-31.

Spear M. Acute or chronic? What's the difference? Plast Surg Nurs. 2013; 33(2):98-100.

Garcia Guillen A, Millán Rivero J, Martínez C, Moraleda J, García-Bernal D. Wharton´s Jelly Mesenchymal Stem Cell Therapy for Skin Wound Healing. J Stem Cell Res Dev. 2020; 6:037.

Coutinho P, Qiu C, Frank S, Tamber K, Becker D. Dynamic changes in connexin expression correlate with key events in the wound healing process. Cell Biol Int. 2003; 27(7):525-41.

Haggstrom M. Medical gallery of mikael haggstrom 2014. Wiki J Med. 2014; 1(2):1-53.

Lopes B, Sousa P, Alvites R, Branquinho M, Sousa A, Mendonça C, et al. The Application of Mesenchymal Stem Cells on Wound Repair and Regeneration. Appl Sci. 2021; 11(7):3000.

Rezvani Ghomi E, Khalili S, Nouri Khorasani S, Esmaeely Neisiany R, Ramakrishna S. Wound dressings: Current advances and future directions. J Appl Polym Sci. 2019; 136(27):47738.

Ojeh N, Pastar I, Tomic-Canic M, Stojadinovic O. Stem Cells in Skin Regeneration, Wound Healing, and Their Clinical Applications. Int J Mol Sci. 2015; 16(10):25476-501.

Xiong S, Zhang X, Lu P, Wu Y, Wang Q. A Gelatin-sulfonated Silk Composite Scaffold based on 3D Printing Technology Enhances Skin Regeneration by Stimulating Epidermal Growth and Dermal Neovascularization. Sci Rep. 2017; 7(1):4288.

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.

Ohanube G, Obeta UM, Ikeagwulonu CR. Case reports in the use of vitamin C based regimen in prophylaxis and management of COVID-19 among Nigerians. J Curr Biomed Rep. 2020; 1(2):77-80.

Grada A, Falanga V. Novel Stem Cell Therapies for Applications to Wound Healing and Tissue Repair. Surg Technol Int. 2016; 29:29-37.

Dorai AA. Wound care with traditional, complementary and alternative medicine. Indian J Plast Surg. 2012; 45(2):418-24.

Zhang C, Wang T, Zhang L, Chen P, Tang S, Chen A, et al. Combination of lyophilized adipose-derived stem cell concentrated conditioned medium and polysaccharide hydrogel in the inhibition of hypertrophic scarring. Stem Cell Res Ther. 2021; 12(1):23.

Li M, Zhong L, He W, Ding Z, Hou Q, Zhao Y, et al. Concentrated Conditioned Medium-Loaded Silk Nanofiber Hydrogels with Sustained Release of Bioactive Factors To Improve Skin Regeneration. ACS Appl Bio Mater. 2019; 2(10):4397-407.

Das S, Baker AB. Biomaterials and Nanotherapeutics for Enhancing Skin Wound Healing. Front Bioeng Biotechnol. 2016; 4:82.

Chouhan D, Dey N, Bhardwaj N, Mandal BB. Emerging and innovative approaches for wound healing and skin regeneration: Current status and advances. Biomaterials. 2019; 216:119267.

Cable J, Fuchs E, Weissman I, Jasper H, Glass D, Rando TA, et al. Adult stem cells and regenerative medicine-a symposium report. Ann N Y Acad Sci. 2020; 1462(1):27-36.

Devireddy LR, Boxer L, Myers MJ, Skasko M, Screven R. Questions and Challenges in the Development of Mesenchymal Stromal/Stem Cell-Based Therapies in Veterinary Medicine. Tissue Eng Part B Rev. 2017; 23(5):462-70.

Kanji S, Das H. Advances of Stem Cell Therapeutics in Cutaneous Wound Healing and Regeneration. Mediators Inflamm. 2017; 2017:5217967.

Nakamura Y, Ishikawa H, Kawai K, Tabata Y, Suzuki S. Enhanced wound healing by topical administration of mesenchymal stem cells transfected with stromal cell-derived factor-1. Biomaterials. 2013; 34(37):9393-400.

Hu M, Ludlow D, Alexander JS, McLarty J, Lian T. Improved wound healing of postischemic cutaneous flaps with the use of bone marrow-derived stem cells. Laryngoscope. 2014; 124(3):642-8.

Xiao Y, Peng J, Liu Q, Chen L, Shi K, Han R, et al. Ultrasmall CuS@BSA nanoparticles with mild photothermal conversion synergistically induce MSCs-differentiated fibroblast and improve skin regeneration. Theranostics. 2020; 10(4):1500-13.

Isakson M, de Blacam C, Whelan D, McArdle A, Clover AJ. Mesenchymal Stem Cells and Cutaneous Wound Healing: Current Evidence and Future Potential. Stem Cells Int. 2015; 2015:831095.

Castellanos G, Bernabé-García Á, Moraleda JM, Nicolás FJ. Amniotic membrane application for the healing of chronic wounds and ulcers. Placenta. 2017; 59:146-53.

Valiente MR, Nicolás FJ, García-Hernández AM, Fuente Mora C, Blanquer M, Alcaraz PJ, et al. Cryopreserved amniotic membrane in the treatment of diabetic foot ulcers: a case series. J Wound Care. 2018; 27(12):806-15.

Lu D, Chen B, Liang Z, Deng W, Jiang Y, Li S, 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.

Rabinovich SS, Seledtsov VI, Banul NV, Poveshchenko OV, Senyukov VV, Astrakov SV, et al. Cell therapy of brain stroke. Bull Exp Biol Med. 2005; 139(1):126-8.

Resnick IB, Metodiev K, Lazarova P. Hematopoietic cell transplantation for autoimmune diseases: a review of history, current state, and future issues. Immunotherapy-Myths, Reality, Ideas, Future. 2017.

Lindvall O, Kokaia Z. Stem cells for the treatment of neurological disorders. Nature. 2006; 441(7097):1094-6.

Mackay-Sim A, Féron F, Cochrane J, Bassingthwaighte L, Bayliss C, Davies W, et al. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain. 2008; 131(Pt 9):2376-86.

Yang FC, Riordan SM, Winter M, Gan L, Smith PG, Vivian JL, et al. Fate of Neural Progenitor Cells Transplanted Into Jaundiced and Nonjaundiced Rat Brains. Cell Transplant. 2017; 26(4):605-11.

Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol. 2008; 26(4):443-52.

Trivedi HL, Vanikar AV, Thakker U, Firoze A, Dave SD, Patel CN, et al. Human adipose tissue-derived mesenchymal stem cells combined with hematopoietic stem cell transplantation synthesize insulin. Transplant Proc. 2008; 40(4):1135-9.

Mishra R, Dhawan P, Srivastava AS, Singh AB. Inflammatory bowel disease: Therapeutic limitations and prospective of the stem cell therapy. World J Stem Cells. 2020; 12(10):1050-66.

Gratwohl A, Heim D. Current role of stem cell transplantation in chronic myeloid leukaemia. Best Pract Res Clin Haematol. 2009; 22(3):431-43.

Hackanson B, Waller CF. Long-term follow-up of patients with chronic myeloid leukemia having received autologous stem cell transplantation. Ann Hematol. 2011; 90(4):395-9.

Menasché P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, et al. The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation. 2008; 117(9):1189-200.

Hagège AA, Marolleau JP, Vilquin JT, Alhéritière A, Peyrard S, Duboc D, et al. Skeletal myoblast transplantation in ischemic heart failure: long-term follow-up of the first phase I cohort of patients. Circulation. 2006; 114(1 Suppl):I108-13.

Kuo TK, Hung SP, Chuang CH, Chen CT, Shih YR, Fang SC, et al. Stem cell therapy for liver disease: parameters governing the success of using bone marrow mesenchymal stem cells. Gastroenterology. 2008; 134(7):2111-21, 21.e1-3.

Pai M, Zacharoulis D, Milicevic MN, Helmy S, Jiao LR, Levicar N, et al. Autologous infusion of expanded mobilized adult bone marrow-derived CD34+ cells into patients with alcoholic liver cirrhosis. Am J Gastroenterol. 2008; 103(8):1952-8.

Rostamzadeh A, Anjomshoa M, Kurd S, Chai J-K, Jahangiri F, Nilforoushzadeh MA, et al. The role of Wharton’s jelly mesenchymal stem cells in skin reconstruction. J Skin Stem Cell. 2015; 2(2):e60143.

Sundelacruz S, Kaplan DL. Stem cell- and scaffold-based tissue engineering approaches to osteochondral regenerative medicine. Semin Cell Dev Biol. 2009; 20(6):646-55.

Simon C, Pellicer A. Stem cells in human reproduction: basic science and therapeutic potential: CRC Press; 2009.

Bongso A, Fong C-Y. Human Embryonic Stem Cells: Their Nature, Properties, and Uses. In: Baharvand H, editor. Trends in Stem Cell Biology and Technology. Totowa, NJ: Humana Press; 2009. p. 1-17.

Alison MR, Poulsom R, Forbes S, Wright NA. An introduction to stem cells. J Pathol. 2002; 197(4):419-23.

Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol. 2005; 21:605-31.

Smith A. The battlefield of pluripotency. Cell. 2005; 123(5):757-60.

Fu RH, Wang YC, Liu SP, Huang CM, Kang YH, Tsai CH, et al. Differentiation of stem cells: strategies for modifying surface biomaterials. Cell Transplant. 2011; 20(1):37-47.

Nandedkar T, Narkar M. Stem cell research: its relevance to reproductive biology. Indian J Exp Biol. 2003; 41(7):724-39.

Beck B, Blanpain C. Mechanisms regulating epidermal stem cells. Embo j. 2012; 31(9):2067-75.

Overturf K, al-Dhalimy M, Ou CN, Finegold M, Grompe M. Serial transplantation reveals the stem-cell-like regenerative potential of adult mouse hepatocytes. Am J Pathol. 1997; 151(5):1273-80.

de Rooij DG, Grootegoed JA. Spermatogonial stem cells. Curr Opin Cell Biol. 1998; 10(6):694-701.

Bentzinger CF, Wang YX, von Maltzahn J, Rudnicki MA. The emerging biology of muscle stem cells: implications for cell-based therapies. Bioessays. 2013; 35(3):231-41.

Kolios G, Moodley Y. Introduction to stem cells and regenerative medicine. Respiration. 2013; 85(1):3-10.

Majo F, Rochat A, Nicolas M, Jaoudé GA, Barrandon Y. Oligopotent stem cells are distributed throughout the mammalian ocular surface. Nature. 2008; 456(7219):250-4.

Marone M, De Ritis D, Bonanno G, Mozzetti S, Rutella S, Scambia G, et al. Cell cycle regulation in human hematopoietic stem cells: from isolation to activation. Leuk Lymphoma. 2002; 43(3):493-501.

Krampera M, Franchini M, Pizzolo G, Aprili G. Mesenchymal stem cells: from biology to clinical use. Blood Transfus. 2007; 5(3):120-9.

Jaenisch R, Young R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell. 2008; 132(4):567-82.

Ratajczak MZ, Zuba-Surma E, Kucia M, Poniewierska A, Suszynska M, Ratajczak J. Pluripotent and multipotent stem cells in adult tissues. Adv Med Sci. 2012; 57(1):1-17.

Augello A, Kurth TB, De Bari C. Mesenchymal stem cells: a perspective from in vitro cultures to in vivo migration and niches. Eur Cell Mater. 2010; 20:121-33.

Bruder SP, Jaiswal N, Haynesworth SE. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem. 1997; 64(2):278-94.

Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997; 276(5309):71-4.

Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970; 3(4):393-403.

Barzilay R, Melamed E, Offen D. Introducing transcription factors to multipotent mesenchymal stem cells: making transdifferentiation possible. Stem Cells. 2009; 27(10):2509-15.

Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981; 292(5819):154-6.

Rossant J. Stem cells from the Mammalian blastocyst. Stem Cells. 2001; 19(6):477-82.

Gauthaman K, Fong CY, Suganya CA, Subramanian A, Biswas A, Choolani M, et al. Extra-embryonic human Wharton's jelly stem cells do not induce tumorigenesis, unlike human embryonic stem cells. Reprod Biomed Online. 2012; 24(2):235-46.

Takagi R, Ishimaru J, Sugawara A, Toyoshima KE, Ishida K, Ogawa M, et al. Bioengineering a 3D integumentary organ system from iPS cells using an in vivo transplantation model. Sci Adv. 2016; 2(4):e1500887.

Cerqueira MT, Marques AP, Reis RL. Using stem cells in skin regeneration: possibilities and reality. Stem Cells Dev. 2012; 21(8):1201-14.

Rezaie F, Momeni-Moghaddam M, Naderi-Meshkin H. Regeneration and Repair of Skin Wounds: Various Strategies for Treatment. Int J Low Extrem Wounds. 2019; 18(3):247-61.

Ochiai H, Kishi K, Kubota Y, Oka A, Hirata E, Yabuki H, et al. Transplanted mesenchymal stem cells are effective for skin regeneration in acute cutaneous wounds of pigs. Regen Ther. 2017; 7:8-16.

Li JY, Ren KK, Zhang WJ, Xiao L, Wu HY, Liu QY, et al. Human amniotic mesenchymal stem cells and their paracrine factors promote wound healing by inhibiting heat stress-induced skin cell apoptosis and enhancing their proliferation through activating PI3K/AKT signaling pathway. Stem Cell Res Ther. 2019; 10(1):247.

Cerqueira MT, Pirraco RP, Marques AP. Stem Cells in Skin Wound Healing: Are We There Yet? Adv Wound Care (New Rochelle). 2016; 5(4):164-75.

He P, Zhao J, Zhang J, Li B, Gou Z, Gou M, et al. Bioprinting of skin constructs for wound healing. Burns Trauma. 2018; 6:5.

Hu MS, Borrelli MR, Lorenz HP, Longaker MT, Wan DC. Mesenchymal Stromal Cells and Cutaneous Wound Healing: A Comprehensive Review of the Background, Role, and Therapeutic Potential. 2018; 2018:6901983.

Hassouna A, Elgwad M, Fahmy H. Stromal stem cells: nature, biology and potential therapeutic applications. Stromal Cells-Structure, Function, and Therapeutic Implications. 2019.

Huang YZ, Xie HQ, Silini A, Parolini O, Zhang Y, Deng L, et al. Mesenchymal Stem/Progenitor Cells Derived from Articular Cartilage, Synovial Membrane and Synovial Fluid for Cartilage Regeneration: Current Status and Future Perspectives. Stem Cell Rev Rep. 2017; 13(5):575-86.

Tang C, Wang M, Wang P, Wang L, Wu Q, Guo W. Neural Stem Cells Behave as a Functional Niche for the Maturation of Newborn Neurons through the Secretion of PTN. Neuron. 2019; 101(1):32-44.e6.

Sibov TT, Severino P, Marti LC, Pavon LF, Oliveira DM, Tobo PR, et al. Mesenchymal stem cells from umbilical cord blood: parameters for isolation, characterization and adipogenic differentiation. Cytotechnology. 2012; 64(5):511-21.

Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8(4):315-7.

Kim JE, Lee JH, Kim SH, Jung Y. Skin Regeneration with Self-Assembled Peptide Hydrogels Conjugated with Substance P in a Diabetic Rat Model. Tissue Eng Part A. 2018; 24(1-2):21-33.

Gugjoo MB, Fazili MR, Gayas MA, Ahmad RA, Dhama K. Animal mesenchymal stem cell research in cartilage regenerative medicine - a review. Vet Q. 2019; 39(1):95-120.

Kucharzewski M, Rojczyk E, Wilemska-Kucharzewska K, Wilk R, Hudecki J, Los MJ. Novel trends in application of stem cells in skin wound healing. Eur J Pharmacol. 2019; 843:307-15.

Karimi H, Mobayen M, Alijanpour A. Management of Hypertrophic Burn Scar: A Comparison between the Efficacy of Exercise-Physiotherapy and Pressure Garment-Silicone on Hypertrophic Scar. Asian J Sports Med. 2013; 4(1):70-5.

Ramasamy R, Fazekasova H, Lam EW, Soeiro I, Lombardi G, Dazzi F. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation. 2007; 83(1):71-6.

Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002; 99(10):3838-43.

Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, Yu XD, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005; 105(10):4120-6.

Zhou C, Yang B, Tian Y, Jiao H, Zheng W, Wang J, et al. Immunomodulatory effect of human umbilical cord Wharton's jelly-derived mesenchymal stem cells on lymphocytes. Cell Immunol. 2011; 272(1):33-8.

Waterman RS, Tomchuck SL, Henkle SL, Betancourt AM. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. PLoS One. 2010; 5(4):e10088.

Opitz CA, Litzenburger UM, Lutz C, Lanz TV, Tritschler I, Köppel A, et al. Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells. 2009; 27(4):909-19.

Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol. 2002; 23(3):144-50.

Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007; 110(10):3499-506.

Ge W, Jiang J, Arp J, Liu W, Garcia B, Wang H. Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression. Transplantation. 2010; 90(12):1312-20.

Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells. 2006; 24(2):386-98.

English K. Mechanisms of mesenchymal stromal cell immunomodulation. Immunol Cell Biol. 2013; 91(1):19-26.

Walter MN, Wright KT, Fuller HR, MacNeil S, Johnson WE. Mesenchymal stem cell-conditioned medium accelerates skin wound healing: an in vitro study of fibroblast and keratinocyte scratch assays. Exp Cell Res. 2010; 316(7):1271-81.

Chen L, Xu Y, Zhao J, Zhang Z, Yang R, Xie J, et al. Conditioned medium from hypoxic bone marrow-derived mesenchymal stem cells enhances wound healing in mice. PLoS One. 2014; 9(4):e96161.

Kim JY, Song SH, Kim KL, Ko JJ, Im JE, Yie SW, et al. Human cord blood-derived endothelial progenitor cells and their conditioned media exhibit therapeutic equivalence for diabetic wound healing. Cell Transplant. 2010; 19(12):1635-44.

Santos JM, Camões SP, Filipe E, Cipriano M, Barcia RN, Filipe M, et al. Three-dimensional spheroid cell culture of umbilical cord tissue-derived mesenchymal stromal cells leads to enhanced paracrine induction of wound healing. Stem Cell Res Ther. 2015; 6(1):90.

Li CY, Wu XY, Tong JB, Yang XX, Zhao JL, Zheng QF, et al. Comparative analysis of human mesenchymal stem cells from bone marrow and adipose tissue under xeno-free conditions for cell therapy. Stem Cell Res Ther. 2015; 6(1):55.

Heo JS, Choi Y, Kim HS, Kim HO. Comparison of molecular profiles of human mesenchymal stem cells derived from bone marrow, umbilical cord blood, placenta and adipose tissue. Int J Mol Med. 2016; 37(1):115-25.

Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006; 24(5):1294-301.

Golle L, Gerth HU, Beul K, Heitplatz B, Barth P, Fobker M, et al. Bone marrow-derived cells and their conditioned medium induce microvascular repair in uremic rats by stimulation of endogenous repair mechanisms. Sci Rep. 2017; 7(1):9444.

Cantinieaux D, Quertainmont R, Blacher S, Rossi L, Wanet T, Noël A, et al. Conditioned medium from bone marrow-derived mesenchymal stem cells improves recovery after spinal cord injury in rats: an original strategy to avoid cell transplantation. PLoS One. 2013; 8(8):e69515.

Kassem M, Abdallah BM. Human bone-marrow-derived mesenchymal stem cells: biological characteristics and potential role in therapy of degenerative diseases. Cell Tissue Res. 2008; 331(1):157-63.

Shi C. Recent progress toward understanding the physiological function of bone marrow mesenchymal stem cells. Immunology. 2012; 136(2):133-8.

Ratajczak J, Kucia M, Mierzejewska K, Marlicz W, Pietrzkowski Z, Wojakowski W, et al. Paracrine proangiopoietic effects of human umbilical cord blood-derived purified CD133+ cells--implications for stem cell therapies in regenerative medicine. Stem Cells Dev. 2013; 22(3):422-30.

Assmus B, Leistner DM, Schächinger V, Erbs S, Elsässer A, Haberbosch W, et al. Long-term clinical outcome after intracoronary application of bone marrow-derived mononuclear cells for acute myocardial infarction: migratory capacity of administered cells determines event-free survival. Eur Heart J. 2014; 35(19):1275-83.

Schächinger V, Erbs S, Elsässer A, Haberbosch W, Hambrecht R, Hölschermann H, et al. Improved clinical outcome after intracoronary administration of bone-marrow-derived progenitor cells in acute myocardial infarction: final 1-year results of the REPAIR-AMI trial. Eur Heart J. 2006; 27(23):2775-83.

Yuen DA, Connelly KA, Advani A, Liao C, Kuliszewski MA, Trogadis J, et al. Culture-modified bone marrow cells attenuate cardiac and renal injury in a chronic kidney disease rat model via a novel antifibrotic mechanism. PLoS One. 2010; 5(3):e9543.

van Koppen A, Joles JA, van Balkom BW, Lim SK, de Kleijn D, Giles RH, et al. Human embryonic mesenchymal stem cell-derived conditioned medium rescues kidney function in rats with established chronic kidney disease. PLoS One. 2012; 7(6):e38746.

Bermudez MA, Sendon-Lago J, Seoane S, Eiro N, Gonzalez F, Saa J, et al. Anti-inflammatory effect of conditioned medium from human uterine cervical stem cells in uveitis. Exp Eye Res. 2016; 149:84-92.

Frese L, Dijkman PE, Hoerstrup SP. Adipose Tissue-Derived Stem Cells in Regenerative Medicine. Transfus Med Hemother. 2016; 43(4):268-74.

Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002; 13(12):4279-95.

Bertolini F, Lohsiriwat V, Petit JY, Kolonin MG. Adipose tissue cells, lipotransfer and cancer: a challenge for scientists, oncologists and surgeons. Biochim Biophys Acta. 2012; 1826(1):209-14.

Ceccarelli S, Pontecorvi P, Anastasiadou E, Napoli C, Marchese C. Immunomodulatory Effect of Adipose-Derived Stem Cells: The Cutting Edge of Clinical Application. Front Cell Dev Biol. 2020; 8:236.

Tian J, Zhu Q, Zhang Y, Bian Q, Hong Y, Shen Z, et al. Olfactory Ecto-Mesenchymal Stem Cell-Derived Exosomes Ameliorate Experimental Colitis via Modulating Th1/Th17 and Treg Cell Responses. Front Immunol. 2020; 11:598322.

Nivet E, Vignes M, Girard SD, Pierrisnard C, Baril N, Devèze A, et al. Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. J Clin Invest. 2011; 121(7):2808-20.

Delorme B, Nivet E, Gaillard J, Häupl T, Ringe J, Devèze A, et al. The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev. 2010; 19(6):853-66.

Rui K, Zhang Z, Tian J, Lin X, Wang X, Ma J, et al. Olfactory ecto-mesenchymal stem cells possess immunoregulatory function and suppress autoimmune arthritis. Cell Mol Immunol. 2016; 13(3):401-8.

Ourednik J, Ourednik V, Lynch WP, Schachner M, Snyder EY. Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat Biotechnol. 2002; 20(11):1103-10.

Okano H. Stem cell biology of the central nervous system. J Neurosci Res. 2002; 69(6):698-707.

Tang Y, Yu P, Cheng L. Current progress in the derivation and therapeutic application of neural stem cells. 2017; 8(10):e3108.

Rong Y, Liu W, Wang J, Fan J, Luo Y, Li L, et al. Neural stem cell-derived small extracellular vesicles attenuate apoptosis and neuroinflammation after traumatic spinal cord injury by activating autophagy. Cell Death Dis. 2019; 10(5):340.

Marino L, Castaldi MA, Rosamilio R, Ragni E, Vitolo R, Fulgione C, et al. Mesenchymal Stem Cells from the Wharton's Jelly of the Human Umbilical Cord: Biological Properties and Therapeutic Potential. Int J Stem Cells. 2019; 12(2):218-26.

McElreavey KD, Irvine AI, Ennis KT, McLean WH. Isolation, culture and characterisation of fibroblast-like cells derived from the Wharton's jelly portion of human umbilical cord. Biochem Soc Trans. 1991; 19(1):29s.

Lindahl A. 5.514 - Chondrocyte Transplantation and Selection. In: Ducheyne P, editor. Comprehensive Biomaterials. Oxford: Elsevier; 2011. p. 189-98.

EM S. Cell therapy for the treatment of metabolic liver disease: an update on the umbilical cord derived stem cells candidates. Open Tissue Eng Regen Med J. 2011; 4(1):48-53.

Zhang J, La X, Fan L, Li P, Yu Y, Huang Y, et al. Immunosuppressive effects of mesenchymal stem cell transplantation in rat burn models. Int J Clin Exp Pathol. 2015; 8(5):5129-36.

Zhang B, Wang M, Gong A, Zhang X, Wu X, Zhu Y, et al. HucMSC-Exosome Mediated-Wnt4 Signaling Is Required for Cutaneous Wound Healing. Stem Cells. 2015; 33(7):2158-68.

Shi H, Xu X, Zhang B, Xu J, Pan Z, Gong A, et al. 3,3'-Diindolylmethane stimulates exosomal Wnt11 autocrine signaling in human umbilical cord mesenchymal stem cells to enhance wound healing. Theranostics. 2017; 7(6):1674-88.

Pourfath MR, Behzad-Behbahani A, Hashemi SS, Derakhsahnfar A, Taheri MN, Salehi S. Monitoring wound healing of burn in rat model using human Wharton's jelly mesenchymal stem cells containing cGFP integrated by lentiviral vectors. Iran J Basic Med Sci. 2018; 21(1):70-6.

Gholipour-Kanani A, Bahrami SH, Joghataie MT, Samadikuchaksaraei A, Ahmadi-Taftie H, Rabbani S, et al. Tissue engineered poly(caprolactone)-chitosan-poly(vinyl alcohol) nanofibrous scaffolds for burn and cutting wound healing. IET Nanobiotechnol. 2014; 8(2):123-31.

Gholipour-Kanani A, Bahrami SH, Samadi-Kochaksaraie A, Ahmadi-Tafti H, Rabbani S, Kororian A, et al. Effect of tissue-engineered chitosan-poly(vinyl alcohol) nanofibrous scaffolds on healing of burn wounds of rat skin. IET Nanobiotechnol. 2012; 6(4):129-35.

Liu L, Yu Y, Hou Y, Chai J, Duan H, Chu W, et al. Human umbilical cord mesenchymal stem cells transplantation promotes cutaneous wound healing of severe burned rats. PLoS One. 2014; 9(2):e88348.

Liu L, Song H, Duan H, Chai J, Yang J, Li X, et al. TSG-6 secreted by human umbilical cord-MSCs attenuates severe burn-induced excessive inflammation via inhibiting activations of P38 and JNK signaling. Sci Rep. 2016; 6:30121.

Rangatchew F, Vester-Glowinski P, Rasmussen BS, Haastrup E, Munthe-Fog L, Talman ML, et al. Mesenchymal stem cell therapy of acute thermal burns: A systematic review of the effect on inflammation and wound healing. Burns. 2021; 47(2):270-94.

Takeo M, Lee W, Ito M. Wound healing and skin regeneration. Cold Spring Harb Perspect Med. 2015; 5(1):a023267.

Campos JM, Sousa AC, Caseiro AR, Pedrosa SS, Pinto PO, Branquinho MV, et al. Dental pulp stem cells and Bonelike(®) for bone regeneration in ovine model. Regen Biomater. 2019; 6(1):49-59.

Hashemi SS, Mohammadi AA, Kabiri H, Hashempoor MR, Mahmoodi M, Amini M, et al. The healing effect of Wharton's jelly stem cells seeded on biological scaffold in chronic skin ulcers: A randomized clinical trial. J Cosmet Dermatol. 2019; 18(6):1961-7.

Martin-Piedra MA, Alfonso-Rodriguez CA, Zapater A, Durand-Herrera D, Chato-Astrain J, Campos F, et al. Effective use of mesenchymal stem cells in human skin substitutes generated by tissue engineering. Eur Cell Mater. 2019; 37:233-49.

Millán-Rivero JE, Martínez CM, Romecín PA, Aznar-Cervantes SD, Carpes-Ruiz M, Cenis JL, et al. Silk fibroin scaffolds seeded with Wharton's jelly mesenchymal stem cells enhance re-epithelialization and reduce formation of scar tissue after cutaneous wound healing. Stem Cell Res Ther. 2019; 10(1):126.

Somal A, Bhat IA, B I, Singh AP, Panda BSK, Desingu PA, et al. Impact of Cryopreservation on Caprine Fetal Adnexa Derived Stem Cells and Its Evaluation for Growth Kinetics, Phenotypic Characterization, and Wound Healing Potential in Xenogenic Rat Model. J Cell Physiol. 2017; 232(8):2186-200.

Shohara R, Yamamoto A, Takikawa S, Iwase A, Hibi H, Kikkawa F, et al. Mesenchymal stromal cells of human umbilical cord Wharton's jelly accelerate wound healing by paracrine mechanisms. Cytotherapy. 2012; 14(10):1171-81.

Sun J, Zhang Y, Song X, Zhu J, Zhu Q. The Healing Effects of Conditioned Medium Derived from Mesenchymal Stem Cells on Radiation-Induced Skin Wounds in Rats. Cell Transplant. 2019; 28(1):105-15.

Fong CY, Tam K, Cheyyatraivendran S, Gan SU, Gauthaman K, Armugam A, et al. Human Wharton's jelly stem cells and its conditioned medium enhance healing of excisional and diabetic wounds. J Cell Biochem. 2014; 115(2):290-302.

Zhao G, Liu F, Liu Z, Zuo K, Wang B, Zhang Y, et al. MSC-derived exosomes attenuate cell death through suppressing AIF nucleus translocation and enhance cutaneous wound healing. Stem Cell Res Ther. 2020; 11(1):174.

Sandel MJ. Embryo ethics--the moral logic of stem-cell research. N Engl J Med. 2004; 351(3):207-9.

Einsiedel E, Premji S, Geransar R, Orton NC, Thavaratnam T, Bennett LK. Diversity in public views toward stem cell sources and policies. Stem Cell Rev Rep. 2009; 5(2):102-7.

Clover AJ, O'Neill BL, Kumar AH. Analysis of attitudes toward the source of progenitor cells in tissue-engineered products for use in burns compared with other disease states. Wound Repair Regen. 2012; 20(3):311-6.

Leal EC, Carvalho E, Tellechea A, Kafanas A, Tecilazich F, Kearney C, et al. Substance P promotes wound healing in diabetes by modulating inflammation and macrophage phenotype. Am J Pathol. 2015; 185(6):1638-48.

Duscher D, Barrera J, Wong VW, Maan ZN, Whittam AJ, Januszyk M, et al. Stem Cells in Wound Healing: The Future of Regenerative Medicine? A Mini-Review. Gerontology. 2016; 62(2):216-25.

Strong AL, Neumeister MW, Levi B. Stem Cells and Tissue Engineering: Regeneration of the Skin and Its Contents. Clin Plast Surg. 2017; 44(3):635-50.




DOI: https://doi.org/10.52547/JCBioR.3.1.109

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