Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2013, Article ID 329596, 5 pages
http://dx.doi.org/10.1155/2013/329596
Review Article

Bone Marrow Stem Cell as a Potential Treatment for Diabetes

Department of Stem Cell Disorders, Kansai Medical University, Moriguchi, Osaka 570-8506, Japan

Received 11 December 2012; Accepted 8 March 2013

Academic Editor: Gordana Kocic

Copyright © 2013 Ming Li and Susumu Ikehara. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. American Diabetes Association, “Diagnosis and classification of diabetes mellitus,” Diabetes Care, vol. 27, supplement 1, pp. S5–S10, 2004. View at Google Scholar
  2. M. A. Hussain and N. D. Theise, “Stem-cell therapy for diabetes mellitus,” The Lancet, vol. 364, no. 9429, pp. 203–209, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. T. L. Delovitch and B. Singh, “The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD,” Immunity, vol. 7, pp. 727–738, 1997. View at Google Scholar
  4. M. A. Atkinson and E. H. Leiter, “The NOD mouse model of type 1 diabetes: as good as it gets?” Nature Medicine, vol. 5, no. 6, pp. 601–604, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Marrack and D. C. Parker, “A little of what you fancy,” Nature, vol. 368, no. 6470, pp. 397–398, 1994. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Han, P. Serra, J. Yamanouchi et al., “Developmental control of CD8+ T cell-avidity maturation in autoimmune diabetes,” Journal of Clinical Investigation, vol. 115, no. 7, pp. 1879–1887, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. J. M. Gardner, A. L. Fletcher, M. S. Anderson, and S. J. Turley, “AIRE in the thymus and beyond,” Current Opinion in Immunology, vol. 21, no. 6, pp. 582–589, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Vafiadis, S. T. Bennett, J. A. Todd et al., “Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDM2 locus,” Nature Genetics, vol. 15, no. 3, pp. 289–292, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. D. V. Serreze, H. D. Chapman, D. S. Varnum et al., “B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new “speed congenic” stock of NOD.Ig mu null mice,” Journal of Experimental Medicine, vol. 184, no. 5, pp. 2049–2053, 1996. View at Google Scholar · View at Scopus
  10. M. Akashi, S. Nagafuchi, K. Anzai et al., “Direct evidence for the contribution of B cells to the progression of insulitis and the development of diabetes in non-obese diabetic mice,” International Immunology, vol. 9, no. 8, pp. 1159–1164, 1997. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Y. Hu, D. Rodriguez-Pinto, W. Du et al., “Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice,” Journal of Clinical Investigation, vol. 117, no. 12, pp. 3857–3867, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. L. J. Yang, “Liver stem cell-derived β-cell surrogates for treatment of type 1 diabetes,” Autoimmunity Reviews, vol. 5, no. 6, pp. 409–413, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. X. Xu, J. D'Hoker, G. Stangé et al., “β cells can be generated from endogenous progenitors in injured adult mouse pancreas,” Cell, vol. 132, no. 2, pp. 197–207, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. Z. Alipio, W. Liao, E. J. Roemer et al., “Reversal of hyperglycemia in diabetic mouse models using induced-pluripotent stem (iPS)-derived pancreatic β-like cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 30, pp. 13426–13431, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Segev, B. Fishman, A. Ziskind, M. Shulman, and J. Itskovitz-Eldor, “Differentiation of human embryonic stem cells into insulin-producing clusters,” Stem Cells, vol. 22, no. 3, pp. 265–274, 2004. View at Google Scholar · View at Scopus
  16. G. K. C. Brolén, N. Heins, J. Edsbagge, and H. Semb, “Signals from the embryonic mouse pancreas induce differentiation of human embryonic stem cells into insulin-producing β-cell-like cells,” Diabetes, vol. 54, no. 10, pp. 2867–2874, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. D. C. Colter, R. Class, C. M. DiGirolamo, and D. J. Prockop, “Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 7, pp. 3213–3218, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. C. P. Khoo, P. Pozzilli, and M. R. Alison, “Endothelial progenitor cells and their potential therapeutic applications,” Regenerative Medicine, vol. 3, no. 6, pp. 863–876, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Ianus, G. G. Holz, N. D. Theise, and M. A. Hussain, “In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion,” Journal of Clinical Investigation, vol. 111, no. 6, pp. 843–850, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Ikehara, H. Ohtsuki, and R. A. Good, “Prevention of type I diabetes in nonobese diabetic mice by allogeneic bone marrow transplantation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 22, pp. 7743–7747, 1985. View at Google Scholar · View at Scopus
  22. Y. Hasegawa, T. Ogihara, T. Yamada et al., “Bone marrow (BM) transplantation promotes β-cell regeneration after acute injury through BM cell mobilization,” Endocrinology, vol. 148, no. 5, pp. 2006–2015, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Yasumizu, K. Sugiura, H. Iwai et al., “Treatment of type 1 diabetes mellitus in non-obese diabetic mice by transplantation of allogeneic bone marrow and pancreatic tissue,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 18, pp. 6555–6557, 1987. View at Google Scholar · View at Scopus
  24. H. Iwai, R. Yasumizu, K. Sugiura et al., “Successful pancreatic allografts in combination with bone marrow transplantation in mice,” Immunology, vol. 62, no. 3, pp. 457–462, 1987. View at Google Scholar · View at Scopus
  25. M. Taira, M. Inaba, K. Takada et al., “Treatment of streptozotocin-induced diabetes mellitus in rats by transplantation of islet cells from two major histocompatibility complex disparate rats in combination with intra bone marrow injection of allogenic bone marrow cells,” Transplantation, vol. 79, no. 6, pp. 680–687, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Cheng, Y. C. Zhang, S. Wolfe et al., “Combinatorial treatment of bone marrow stem cells and stromal cell-derived factor 1 improves glycemia and insulin production in diabetic mice,” Molecular and Cellular Endocrinology, vol. 345, pp. 88–96, 2011. View at Google Scholar
  27. M. M. Gabr, M. M. Zakaria, A. F. Refaie et al., “Insulin-producing cells from adult human bone marrow mesenchymal stem cells control streptozotocin-induced diabetes in nude mice,” Cell Transplant. In press.
  28. R. H. Lee, M. J. Seo, R. L. Reger et al., “Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 46, pp. 17438–17443, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. V. S. Urbán, J. Kiss, J. Kovács et al., “Mesenchymal stem cells cooperate with bone marrow cells in therapy of diabetes,” Stem Cells, vol. 26, no. 1, pp. 244–253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Fiorina, M. Jurewicz, A. Augello et al., “Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes,” Journal of Immunology, vol. 183, no. 2, pp. 993–1004, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Ezquer, M. Ezquer, V. Simon, and P. Conget, “The antidiabetic effect of MSCs is not impaired by insulin prophylaxis and is not improved by a second dose of cells,” PLoS ONE, vol. 6, no. 1, Article ID e16566, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Milanesi, J. W. Lee, Z. Li et al., “beta-Cell regeneration mediated by human bone marrow mesenchymal stem cells,” PLoS ONE, vol. 7, Article ID e42177, 2012. View at Google Scholar
  33. A. Oikawa, M. Siragusa, F. Quaini et al., “Diabetes mellitus induces bone marrow microangiopathy,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, pp. 498–508, 2010. View at Google Scholar
  34. C. J. M. Loomans, E. J. P. De Koning, F. J. T. Staal et al., “Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes,” Diabetes, vol. 53, no. 1, pp. 195–199, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. O. M. Tepper, R. D. Galiano, J. M. Capla et al., “Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures,” Circulation, vol. 106, no. 22, pp. 2781–2786, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Mathews, P. T. Hanson, E. Ford, J. Fujita, K. S. Polonsky, and T. A. Graubert, “Recruitment of bone marrow-derived endothelial cells to sites of pancreatic beta-cell injury,” Diabetes, vol. 53, no. 1, pp. 91–98, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. G. P. Duffy, T. Ahsan, T. O'Brien, F. Barry, and R. M. Nerem, “Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro,” Tissue Engineering A, vol. 15, no. 9, pp. 2459–2470, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Tamama, C. K. Sen, and A. Wells, “Differentiation of bone marrow mesenchymal stem cells into the smooth muscle lineage by blocking ERK/MAPK signaling pathway,” Stem Cells and Development, vol. 17, no. 5, pp. 897–908, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. W. M. Yue, W. Liu, Y. W. Bi et al., “Mesenchymal stem cells differentiate into an endothelial phenotype, reduce neointimal formation, and enhance endothelial function in a rat vein grafting model,” Stem Cells and Development, vol. 17, no. 4, pp. 785–793, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. Z. Gong and L. E. Niklason, “Small-diameter human vessel wall engineered from bone marrow-derived mesenchymal stem cells (hMSCs),” The FASEB Journal, vol. 22, no. 6, pp. 1635–1648, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. H. C. Quevedo, K. E. Hatzistergos, B. N. Oskouei et al., “Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 14022–14027, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. K. E. Wellen and G. S. Hotamisligil, “Inflammation, stress, and diabetes,” Journal of Clinical Investigation, vol. 115, no. 5, pp. 1111–1119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. G. S. Hotamisligil, “Inflammation and metabolic disorders,” Nature, vol. 444, no. 7121, pp. 860–867, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Suganami, J. Nishida, and Y. Ogawa, “A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor α,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 10, pp. 2062–2068, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. V. A. Fonseca, “Defining and characterizing the progression of type 2 diabetes,” Diabetes Care, vol. 32, supplement 2, pp. S151–S156, 2009. View at Google Scholar · View at Scopus
  46. S. C. Hanley, E. Austin, B. Assouline-Thomas et al., “β-cell mass dynamics and islet cell plasticity in human type 2 diabetes,” Endocrinology, vol. 151, no. 4, pp. 1462–1472, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. E. H. Hathout, W. Thomas, M. El-Shahawy, F. Nahab, and J. W. Mace, “Diabetic autoimmune markers in children and adolescents with type 2 diabetes,” Pediatrics, vol. 107, no. 6, p. E102, 2001. View at Google Scholar · View at Scopus
  48. L. K. Gilliam, B. M. Brooks-Worrell, J. P. Palmer, C. J. Greenbaum, and C. Pihoker, “Autoimmunity and clinical course in children with type 1, type 2, and type 1.5 diabetes,” Journal of Autoimmunity, vol. 25, no. 3, pp. 244–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. G. J. Klingensmith, L. Pyle, S. Arslanian et al., “The presence of GAD and IA-2 antibodies in youth with a type 2 diabetes phenotype: results from the TODAY study,” Diabetes Care, vol. 33, no. 9, pp. 1970–1975, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Than, H. Ishida, M. Inaba et al., “Bone marrow transplantation as a strategy for treatment of non-insulin- dependent diabetes mellitus in KK-Ay mice,” Journal of Experimental Medicine, vol. 176, no. 4, pp. 1233–1238, 1992. View at Google Scholar · View at Scopus
  51. N. G. Abraham, M. Li, L. Vanella, S. J. Peterson, S. Ikehara, and D. Asprinio, “Bone marrow stem cell transplant into intra-bone cavity prevents type 2 diabetes: role of heme oxygenase-adiponectin,” Journal of Autoimmunity, vol. 30, no. 3, pp. 128–135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. I. Boumaza, S. Srinivasan, W. T. Witt et al., “Autologous bone marrow-derived rat mesenchymal stem cells promote PDX-1 and insulin expression in the islets, alter T cell cytokine pattern and preserve regulatory T cells in the periphery and induce sustained normoglycemia,” Journal of Autoimmunity, vol. 32, no. 1, pp. 33–42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. E. J. Estrada, F. Valacchi, E. Nicora et al., “Combined treatment of intrapancreatic autologous bone marrow stem cells and hyperbaric oxygen in type 2 diabetes mellitus,” Cell Transplantation, vol. 17, no. 12, pp. 1295–1304, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. S. C. Chua Jr., W. K. Chung, X. S. Wu-Peng et al., “Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor,” Science, vol. 271, no. 5251, pp. 994–996, 1996. View at Google Scholar · View at Scopus
  55. G. Fantuzzi and R. Faggioni, “Leptin in the regulation of immunity, inflammation, and hematopoiesis,” Journal of Leukocyte Biology, vol. 68, no. 4, pp. 437–446, 2000. View at Google Scholar · View at Scopus
  56. G. Matarese, S. Moschos, and C. S. Mantzoros, “Leptin in immunology,” Journal of Immunology, vol. 174, no. 6, pp. 3137–3142, 2005. View at Google Scholar · View at Scopus
  57. G. Fernandes, B. S. Handwerger, E. J. Yunis, and D. M. Brown, “Immune response in the mutant diabetic C57BL/Ks-db+ mouse. Discrepancies between in vitro and in vivo immunological assays,” Journal of Clinical Investigation, vol. 61, no. 2, pp. 243–250, 1978. View at Google Scholar · View at Scopus
  58. M. Kimura, S. I. Tanaka, F. Isoda, K. I. Sekigawa, T. Yamakawa, and H. Sekihara, “T lymphopenia in obese diabetic (db/db) mice is non-selective and thymus independent,” Life Sciences, vol. 62, no. 14, pp. 1243–1250, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Li, N. G. Abraham, L. Vanella et al., “Successful modulation of type 2 diabetes in db/db mice with intra-bone marrow-bone marrow transplantation plus concurrent thymic transplantation,” Journal of Autoimmunity, vol. 35, no. 4, pp. 414–423, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Li, L. Vanella, Y. Zhang et al., “Stem cell transplantation increases antioxidant effects in diabetic mice,” International Journal of Biological Sciences, vol. 8, pp. 1335–1344, 2012. View at Google Scholar
  61. L. Wang, S. Zhao, H. Mao et al., “Autologous bone marrow stem cell transplantation for the treatment of type 2 diabetes mellitus,” Chinese Medical Journal, vol. 124, pp. 3622–3628, 2011. View at Google Scholar