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Mesenchymal Stem Cells for Diabetes and Related Complications

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Essentials of Mesenchymal Stem Cell Biology and Its Clinical Translation

Abstract

Mesenchymal stem cells (MSCs) are self-renewing cells with multipotent differentiation characteristics and capability for the regulation of immune response. Accordingly, in the context of diabetes research, the ability of MSC to generate insulin-producing cells and to enhance islet engraftment and survival makes them attractive as new therapeutic agents for treatment of diabetes and related complications. In this chapter we emphasized the role of MSCs in the repair of β cell mass and function and we described the capacity of MSCs to modulate the autoimmune response during the pathogenesis of diabetes mellitus. In addition, we also presented here the mechanisms, promises and potential obstacles for MSC therapy of diabetic complications: cardiomyopathy, critical limb ischemia, nephropathy, polyneuropathy, retinopathy and diabetic wounds.

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References

  1. Eizirik DL, Mandrup-Poulsen T. A choice of death. The signal transduction of immune-mediated b-cell apoptosis. Diabetologia. 2001;44:2115–33.

    Article  PubMed  CAS  Google Scholar 

  2. DeFronzo RA. Pathogenesis of type 2 diabetes: metabolic and molecular implications for identifying diabetes genes. Diabetes Rev. 1997;5:177–269.

    Google Scholar 

  3. Hani EH, Stoffers DA, Chevre JC, Durand E, Stanojevic V, Dina C, Habener JF, Froguel P. Defective mutations in the insulin promoter factor-1 (IPF-1) gene in late-onset type 2 diabetes mellitus. J Clin Invest. 1999;104:R41–8.

    Article  PubMed  CAS  Google Scholar 

  4. Davis NE, Hamilton D, Fontaine MJ. Harnessing the immunomodulatory and tissue repair properties of mesenchymal stem cells to restore β cell function. Curr Diab Rep. 2012;12:612–22.

    Article  PubMed  CAS  Google Scholar 

  5. Rother K. Diabetes treatment-bridging the divide. N Engl J Med. 2007;356:1499–501.

    Article  PubMed  CAS  Google Scholar 

  6. Mabed M, Shahin M. Mesenchymal stem cell-based therapy for the treatment of type 1 diabetes mellitus. Curr Stem Cell Res Ther. 2012;7:179–90.

    Article  PubMed  CAS  Google Scholar 

  7. Bernardi S, Severini GM, Zauli G, Secchiero P. Cell-based therapies for diabetic complications. Exp Diabetes Res. 2012;2012:872504.

    Article  PubMed  Google Scholar 

  8. Fiorina P, Voltarelli J, Zavazava N. Immunological applications of stem cells in type 1 diabetes. Endocr Rev. 2011;32:725–54.

    Article  PubMed  CAS  Google Scholar 

  9. Pileggi A. Mesenchymal stem cells for the treatment of diabetes. Diabetes. 2012;61:1355–6.

    Article  PubMed  CAS  Google Scholar 

  10. Volarevic V, Arsenijevic N, Lukic ML, Stojkovic M. Concise review: mesenchymal stem cell treatment of the complications of diabetes mellitus. Stem Cells. 2011;29:5–10.

    Article  PubMed  CAS  Google Scholar 

  11. Porada CD, Zanjani ED, Almeida-Porad G. Adult mesenchymal stem cells: a pluripotent population with multiple applications. Curr Stem Cell Res Ther. 2006;1:365–9.

    Article  PubMed  CAS  Google Scholar 

  12. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci. 2006;119:2204–13.

    Article  PubMed  Google Scholar 

  13. Kanjevac T, Milovanovic M, Volarevic V, Lukic ML, Arsenijevic N, Markovic D, Zdravkovic N, Tesic Z, Lukic A. Cytotoxic effects of glass ionomer cements on human dental pulp stem cells correlate with fluoride release. Med Chem. 2012;8:40–5.

    Article  PubMed  CAS  Google Scholar 

  14. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25:2739–49.

    Article  PubMed  CAS  Google Scholar 

  15. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–7.

    Article  PubMed  CAS  Google Scholar 

  16. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–4.

    Article  PubMed  CAS  Google Scholar 

  17. Abdi R, Fiorina P, Adra CN, Atkinson M, Sayegh MH. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes. 2008;57:1759–67.

    Article  PubMed  CAS  Google Scholar 

  18. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110:3499–506.

    Article  PubMed  CAS  Google Scholar 

  19. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–7.

    Article  PubMed  CAS  Google Scholar 

  20. Guo QS, Zhu MY, Wang L, Fan XJ, Lu YH, Wang ZW, Zhu SJ, Wang Y, Huang Y. Combined transfection of the three transcriptional factors, PDX-1, NeuroD1, and MafA, causes differentiation of bone marrow mesenchymal stem cells into insulin-producing cells. Exp Diabetes Res. 2012;2012:672013.

    PubMed  Google Scholar 

  21. Milanesi A, Lee JW, Li Z, Da Sacco S, Villani V, Cervantes V, Perin L, Yu JS. β-Cell regeneration mediated by human bone marrow mesenchymal stem cells. PLoS One. 2012;7(8):e42177.

    Article  PubMed  CAS  Google Scholar 

  22. Tsai PJ, Wang HS, Shyr YM, Weng ZC, Tai LC, Shyu JF, Chen TH. Transplantation of insulin-producing cells from umbilical cord mesenchymal stem cells for the treatment of streptozotocin-induced diabetic rats. J Biomed Sci. 2012;19:47.

    Article  PubMed  CAS  Google Scholar 

  23. Ho JH, Tseng TC, Ma WH, Ong WK, Chen YF, Chen MH, Lin MW, Hong CY, Lee OK. Multiple intravenous transplantations of mesenchymal stem cells effectively restore long-term blood glucose homeostasis by hepatic engraftment and β-cell differentiation in streptozocin-induced diabetic mice. Cell Transplant. 2012;21:997–1009.

    Article  PubMed  Google Scholar 

  24. Wu H, Lu W, Mahato RI. Mesenchymal stem cells as a gene delivery vehicle for successful islet transplantation. Pharm Res. 2011;28:2098–109.

    Article  PubMed  CAS  Google Scholar 

  25. Sakata N, Goto M, Yoshimatsu G, Egawa S, Unno M. Utility of co-transplanting mesenchymal stem cells in islet transplantation. World J Gastroenterol. 2011;17:5150–5.

    Article  PubMed  Google Scholar 

  26. Volarevic V, Al-Qahtani A, Arsenijevic N, Pajovic S, Lukic ML. Interleukin-1 receptor antagonist (IL-1Ra) and IL-1Ra producing mesenchymal stem cells as modulators of diabetogenesis. Autoimmunity. 2010;43:255–63.

    Article  PubMed  CAS  Google Scholar 

  27. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 2008;111:1327–33.

    Article  PubMed  CAS  Google Scholar 

  28. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815–22.

    Article  PubMed  CAS  Google Scholar 

  29. Xu DM, Yu XF, Zhang D, Zhang MX, Zhou JF, Tan PH, Ding YC. Mesenchymal stem cells differentially mediate regulatory T cells and conventional effector T-cells to protect fully allogeneic islet grafts in mice. Diabetologia. 2012;55:1091–102.

    Article  PubMed  CAS  Google Scholar 

  30. Sioud M. New insights into mesenchymal stromal cell-mediated T-cell suppression through galectins. Scand J Immunol. 2011;73:79–84.

    Article  PubMed  CAS  Google Scholar 

  31. Volarevic V, Milovanovic M, Ljujic B, Pejnovic N, Arsenijevic N, Nilsson U, Leffler H, Lukic ML. Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology. 2012;55:1954–64.

    Article  PubMed  CAS  Google Scholar 

  32. Radosavljevic G, Volarevic V, Jovanovic I, Milovanovic M, Pejnovic N, Arsenijevic N, Hsu DK, Lukic ML. The roles of Galectin-3 in autoimmunity and tumor progression. Immunol Res. 2012;52:100–10.

    Article  PubMed  CAS  Google Scholar 

  33. Bassi EJ, Moraes-Vieira PM, Moreira-Sá CS, Almeida DC, Vieira LM, Cunha CS, Hiyane MI, Basso AS, Pacheco-Silva A, Câmara NO. Immune regulatory properties of allogeneic adipose-derived mesenchymal stem cells in the treatment of experimental autoimmune diabetes. Diabetes. 2012;61:2534–45.

    Article  PubMed  CAS  Google Scholar 

  34. Ezquer F, Ezquer M, Contador D, Ricca M, Simon V, Conget P. The antidiabetic effect of mesenchymal stem cells is unrelated to their transdifferentiation potential but to their capability to restore Th1/Th2 balance and to modify the pancreatic microenvironment. Stem Cells. 2012;30:1664–74.

    Article  PubMed  CAS  Google Scholar 

  35. Emamaullee JA, Rajotte RV, Liston P, Korneluk RG, Lakey JR, Shapiro AM, Elliott JF. XIAP overexpression in human islets prevents early posttransplant apoptosis and reduces the islet mass needed to treat diabetes. Diabetes. 2005;54:2541–8.

    Article  PubMed  CAS  Google Scholar 

  36. Ball SG, Shuttleworth CA, Kielty CM. Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J Cell Mol Med. 2007;11:1012–30.

    Article  PubMed  CAS  Google Scholar 

  37. Ghajar CM, Blevins KS, Hughes CC, George SC, Putnam AJ. Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng. 2006;12:2875–88.

    Article  PubMed  CAS  Google Scholar 

  38. Zacharek A, Chen J, Cui X, Li A, Li Y, Roberts C, Feng Y, Gao Q, Chopp M. Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J Cereb Blood Flow Metab. 2007;27:1684–91.

    Article  PubMed  CAS  Google Scholar 

  39. Johansson U, Rasmusson I, Niclou SP, Forslund N, Gustavsson L, Nilsson B, Korsgren O, Magnusson PU. Formation of composite endothelial cell-mesenchymal stem cell islets: a novel approach to promote islet revascularization. Diabetes. 2008;57:2393–401.

    Article  PubMed  CAS  Google Scholar 

  40. Si Y, Zhao Y, Hao H, Liu J, Guo Y, Mu Y, Shen J, Cheng Y, Fu X, Han W. Infusion of mesenchymal stem cells ameliorates hyperglycemia in type 2 diabetic rats: identification of a novel role in improving insulin sensitivity. Diabetes. 2012 Jun;61:1616–25.

    Article  PubMed  CAS  Google Scholar 

  41. Pantic J, Volarevic V, Djukic A. Experimental models of diabetes mellitus. Ser J Exp Med. 2011;12:29–35.

    Google Scholar 

  42. Jiang R, Han Z, Zhuo G, Qu X, Li X, Wang X, Shao Y, Yang S, Han ZC. Transplantation of placenta-derived mesenchymal stem cells in type 2 diabetes: a pilot study. Front Med. 2011;5:94–100.

    Article  PubMed  Google Scholar 

  43. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res. 2006;98:596–605.

    Article  PubMed  CAS  Google Scholar 

  44. Jesmin S, Sakuma I, Hattori Y, Kitabatake A. Role of angiotensin II in altered expression of molecules responsible for coronary matrix remodeling in insulin-resistant diabetic rats. Arterioscler Thromb Vasc Biol. 2003;23:2021–6.

    Article  PubMed  CAS  Google Scholar 

  45. Camp TM, Tyagi SC, Senior RM, et al. Gelatinase B (MMP-9) an apoptotic factor in diabetic transgenic mice. Diabetologia. 2003;46:1438–45.

    Article  PubMed  CAS  Google Scholar 

  46. Yoon YS, Uchida S, Masuo O, Cejna M, Park JS, Gwon HC, Kirchmair R, Bahlman F, Walter D, Curry C, Hanley A, Isner JM, Losordo DW. Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial growth factor. Circulation. 2005;111:2073–85.

    Article  PubMed  CAS  Google Scholar 

  47. Zhang N, Li J, Luo R, Jiang J, Wang JA. Bone marrow mesenchymal stem cells induce angiogenesis and attenuate the remodeling of diabetic cardiomyopathy. Exp Clin Endocrinol Diabetes. 2008;116:104–11.

    Article  PubMed  CAS  Google Scholar 

  48. Wang X, Zhao T, Huang W, Wang T, Qian J, Xu M, Kranias EG, Wang Y, Fan GC. Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors. Stem Cells. 2009;27:3021–31.

    PubMed  CAS  Google Scholar 

  49. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, Hermiller Jr JB, Reisman MA, Schaer GL, Sherman W. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol. 2009;54:2277–86.

    Article  PubMed  CAS  Google Scholar 

  50. Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, Bang OY. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells. 2010;28:1099–106.

    Article  PubMed  Google Scholar 

  51. Amin AH, Abd Elmageed ZY, Nair D, Partyka MI, Kadowitz PJ, Belmadani S, Matrougui K. Modified multipotent stromal cells with epidermal growth factor restore vasculogenesis and blood flow in ischemic hind-limb of type II diabetic mice. Lab Invest. 2010;90:985–96.

    Article  PubMed  CAS  Google Scholar 

  52. Comerota AJ, Link A, Douville J, Burchardt ER. Upper extremity ischemia treated with tissue repair cells from adult bone marrow. J Vasc Surg. 2010;52:723–9.

    Article  PubMed  Google Scholar 

  53. Fazan Jr R, Dias da Silva VJ, Ballejo G, Salgado HC. Power spectra of arterial pressure and heart rate in streptozotocin-induced diabetes in rats. J Hypertens. 1999;17:489–95.

    Article  PubMed  Google Scholar 

  54. Abdel Aziz MT, El-Asmar MF, Haidara M, Atta HM, Roshdy NK, Rashed LA, Sabry D, Youssef MA, Abdel Aziz AT, Moustafa M. Effect of bone marrow-derived mesenchymal stem cells on cardiovascular complications in diabetic rats. Med Sci Monit. 2008;14:249–55.

    Google Scholar 

  55. Volarevic V, Ljujic B, Stojkovic P, Lukic A, Arsenijevic N, Stojkovic M. Human stem cell research and regenerative medicine-present and future. Br Med Bull. 2011;99:155–68.

    Article  PubMed  Google Scholar 

  56. Lu D, Zhang L, Wang H, Zhang Y, Liu J, Xu J, Liang Z, Deng W, Jiang Y, Wu Q, Li S, Ai Z, Zhong Y, Ying Y, Liu H, Gao F, Zhang Z, Chen B. Peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) enhances engraftment and angiogenesis of mesenchymal stem cells in diabetic hindlimb ischemia. Diabetes. 2012;61:1153–9.

    Article  PubMed  CAS  Google Scholar 

  57. Lee HC, An SG, Lee HW, Park JS, Cha KS, Hong TJ, Park JH, Lee SY, Kim SP, Kim YD, Chung SW, Bae YC, Shin YB, Kim JI, Jung JS. Safety and effect of adipose tissue-derived stem cell implantation in patients with critical limb ischemia: a pilot study. Circ J. 2012;76:1750–60.

    Article  PubMed  CAS  Google Scholar 

  58. Ezquer FE, Ezquer ME, Parrau DB, Carpio D, Yañez AJ, Conget PA. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant. 2008;14:631–40.

    Article  PubMed  CAS  Google Scholar 

  59. Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, Prockop DJ. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci USA. 2006;103:17438–43.

    Article  PubMed  CAS  Google Scholar 

  60. Herrera MB, Bussolati B, Bruno S, Fonsato V, Romanazzi GM, Camussi G. Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med. 2004;14:1035–41.

    PubMed  Google Scholar 

  61. Park JH, Park J, Hwang SH, Han H, Ha H. Delayed treatment with human umbilical cord blood-derived stem cells attenuates diabetic renal injury. Transplant Proc. 2012;44:1123–6.

    Article  PubMed  CAS  Google Scholar 

  62. Fang Y, Tian X, Bai S, Fan J, Hou W, Tong H, Li D. Autologous transplantation of adipose-derived mesenchymal stem cells ameliorates streptozotocin-induced diabetic nephropathy in rats by inhibiting oxidative stress, pro-inflammatory cytokines and the p38 MAPK signaling pathway. Int J Mol Med. 2012;30:85–92.

    PubMed  CAS  Google Scholar 

  63. Vinik AI, Park TS, Stansberry KB, Pittenger GL. Diabetic neuropathies. Diabetologia. 2000;43:957–73.

    Article  PubMed  CAS  Google Scholar 

  64. Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation. 2004;109:1543–9.

    Article  PubMed  CAS  Google Scholar 

  65. Shibata T, Naruse K, Kamiya H, Kozakae M, Kondo M, Yasuda Y, Nakamura N, Ota K, Tosaki T, Matsuki T, Nakashima E, Hamada Y, Oiso Y, Nakamura J. Transplantation of bone marrow-derived mesenchymal stem cells improves diabetic polyneuropathy in rats. Diabetes. 2008;57:3099–107.

    Article  PubMed  CAS  Google Scholar 

  66. Volarevic V, Erceg S, Bhattacharya S, Stojkovic P, Horner P, Stojkovic M. Stem cell based therapy for spinal cord injury. Cell Transplant. 2012 Oct 3. doi:10.3727/096368912X657260.

  67. Yang Z, Li K, Yan X, Dong F, Zhao C. Amelioration of diabetic retinopathy by engrafted human adipose-derived mesenchymal stem cells in streptozotocin diabetic rats. Graefes Arch Clin Exp Ophthalmol. 2010;248:1415–22.

    Article  PubMed  Google Scholar 

  68. Scalinci SZ, Scorolli L, Corradetti G, Domanico D, Vingolo EM, Meduri A, Bifani M, Siravo D. Potential role of intravitreal human placental stem cell implants in inhibiting progression of diabetic retinopathy in type 2 diabetes: neuroprotective growth factors in the vitreous. Clin Ophthalmol. 2011;5:691–6.

    Article  PubMed  Google Scholar 

  69. Medina A, Scott PG, Ghahary A, Tredget EE. Pathophysiology of chronic nonhealing wounds. J Burn Care Rehabil. 2005;26:306–19.

    Article  PubMed  Google Scholar 

  70. Kwon DS, Gao X, Liu YB, Dulchavsky DS, Danyluk AL, Bansal M, Chopp M, McIntosh K, Arbab AS, Dulchavsky SA, Gautam SC. Treatment with bone marrow-derived stromal cells accelerates wound healing in diabetic rats. Int Wound J. 2008;5:453–63.

    Article  PubMed  Google Scholar 

  71. Kuo YR, Wang CT, Cheng JT, Wang FS, Chiang YC, Wang CJ. Bone marrow-derived mesenchymal stem cells enhanced diabetic wound healing through recruitment of tissue regeneration in a rat model of streptozotocin-induced diabetes. Plast Reconstr Surg. 2011;128:872–80.

    Article  PubMed  CAS  Google Scholar 

  72. Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells. 2007;25:2648–59.

    Article  PubMed  CAS  Google Scholar 

  73. Falanga V, Iwamoto S, Chartier M, Yufit T, Butmarc J, Kouttab N, Shrayer D, Carson P. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 2007;13:1299–312.

    Article  PubMed  CAS  Google Scholar 

  74. Kim SW, Zhang HZ, Guo L, Kim JM, Kim MH. Amniotic mesenchymal stem cells enhance wound healing in diabetic NOD/SCID mice through high angiogenic and engraftment capabilities. PLoS One. 2012;7:e41105.

    Article  PubMed  CAS  Google Scholar 

  75. Shen L, Zeng W, Wu YX, Hou CL, Chen W, Yang MC, Li L, Zhang YF, Zhu CH. Neurotrophin-3 accelerates wound healing in diabetic mice by promoting a paracrine response in mesenchymal stem cells. Cell Transplant. 2012 Oct 3. doi: 10.3727/096368912X657495.

  76. Vojtassák J, Danisovic L, Kubes M, Bakos D, Jarábek L, Ulicná M, Blasko M. Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot. Neuro Endocrinol Lett. 2006;27:134–7.

    PubMed  Google Scholar 

  77. Lataillade JJ, Doucet C, Bey E, Carsin H, Huet C, Clairand I, Bottollier-Depois JF, Chapel A, Ernou I, Gourven M, Boutin L, Hayden A, Carcamo C, Buglova E, Joussemet M, de Revel T, Gourmelon P. New approach to radiation burn treatment by dosimetry-guided surgery combined with autologous mesenchymal stem cell therapy. Regen Med. 2007;2:785–94.

    Article  PubMed  CAS  Google Scholar 

  78. 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;12:359–66.

    Article  PubMed  CAS  Google Scholar 

  79. Hou C, Shen L, Huang Q, Mi J, Wu Y, Yang M, Zeng W, Li L, Chen W, Zhu C. The effect of heme oxygenase-1 complexed with collagen on MSC performance in the treatment of diabetic ischemic ulcer. Biomaterials. 2013;34:112–20.

    Article  PubMed  CAS  Google Scholar 

  80. Yu M, Zhou W, Song Y, Yu F, Li D, Na S, Zou G, Zhai M, Xie C. Development of mesenchymal stem cell-implant complexes by cultured cells sheet enhances oseointegration in type 2 diabetic rat model. Bone. 2011;49:387–94.

    Article  PubMed  CAS  Google Scholar 

  81. Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, Xia L, Zhou N, Riddle M, Schroeder TM, Westendorf JJ, McIvor RS, Hogendoorn PC, Szuhai K, Oseth L, Hirsch B, Yant SR, Kay MA, Peister A, Prockop DJ, Fibbe WE, Blazar BR. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells. 2007;25:371–9.

    Article  PubMed  CAS  Google Scholar 

  82. Mottaghi S, Larijani B, Sharifi AM. Apelin 13: a novel approach to enhance efficacy of hypoxic preconditioned mesenchymal stem cells for cell therapy of diabetes. Med Hypotheses. 2012;79(6):717–8. doi:10.1016/j.mehy.2012.08.007.

    Article  PubMed  CAS  Google Scholar 

  83. Le Blanc K, Pittenger M. Mesenchymal stem cells: progress toward promise. Cytotherapy. 2005;7:36–45.

    PubMed  Google Scholar 

  84. Atsma DE, Fibbe WE, Rabelink TJ. Opportunities and challenges for mesenchymal stem cell-mediated heart repair. Curr Opin Lipidol. 2007;18:645–9.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Centre for Molecular Medicine and Stem Cell Research, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia

    Vladislav Volarevic & Miodrag Stojkovic

  2. Institute of Genetic Medicine, International Centre for Life, Newcastle University, Newcastle, UK

    Majlinda Lako

  3. Department of Genetics, Spebo Medical, Leskovac, Serbia

    Miodrag Stojkovic

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  1. Vladislav Volarevic
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  2. Majlinda Lako
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  3. Miodrag Stojkovic
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Correspondence to Miodrag Stojkovic .

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  1. Chinese Academy of Medical Sciences and Peking Union Medical College, Center of Excellence in Tissue Engineering, Institute of Basic Medical Sciences and School of Basic Medicine, 5 Dong Dan San Tiao, Beijing, 100005, China, People's Republic

    Robert Chunhua Zhao

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Volarevic, V., Lako, M., Stojkovic, M. (2013). Mesenchymal Stem Cells for Diabetes and Related Complications. In: Zhao, R. (eds) Essentials of Mesenchymal Stem Cell Biology and Its Clinical Translation. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6716-4_14

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