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Experimental Diabetes Research
Volume 2012, Article ID 872504, 10 pages
http://dx.doi.org/10.1155/2012/872504
Review Article

Cell-Based Therapies for Diabetic Complications

1Department of Morphology and Embriology and LTTA Centre, University of Ferrara, 44100 Ferrara, Italy
2Baker IDI, Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
3Institute for Maternal and Child Health, IRCCS Burlo Garofolo, Trieste, 34137, Italy

Received 24 February 2011; Accepted 21 March 2011

Academic Editor: Gian Paolo Fadini

Copyright © 2012 Stella Bernardi et al. 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. N. A. Calcutt, M. E. Cooper, T. S. Kern, and A. M. Schmidt, “Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials,” Nature Reviews Drug Discovery, vol. 8, no. 5, pp. 417–429, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. P. Jarajapu and M. B. Grant, “The promise of cell-based therapies for diabetic complications: challenges and solutions,” Circulation Research, vol. 106, no. 5, pp. 854–869, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Asahara, T. Murohara, A. Sullivan et al., “Isolation of putative progenitor endothelial cells for angiogenesis,” Science, vol. 275, no. 5302, pp. 964–967, 1997. View at Publisher · View at Google Scholar · View at Scopus
  4. V. Volarevic, N. Arsenijevic, M. L. Lukic, and M. Stojkovic, “Mesenchymal stem cell treatment of complications of diabetes mellitus,” Stem Cells, vol. 29, no. 1, pp. 5–10, 2011. View at Google Scholar
  5. S. Aggarwal and M. F. Pittenger, “Human mesenchymal stem cells modulate allogeneic immune cell responses,” Blood, vol. 105, no. 4, pp. 1815–1822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. 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
  7. A. M. Madec, R. Mallone, G. Afonso et al., “Mesenchymal stem cells protect NOD mice from diabetes by inducing regulatory T cells,” Diabetologia, vol. 52, no. 7, pp. 1391–1399, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Zauli, B. Toffoli, M. G. Di Iasio, C. Celeghini, B. Fabris, and P. Secchiero, “Treatment with recombinant tumor necrosis factor-related apoptosis-inducing ligand alleviates the severity of streptozotocin-induced diabetes,” Diabetes, vol. 59, no. 5, pp. 1261–1265, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. Q. P. Xie, H. Huang, B. Xu et al., “Human bone marrow mesenchymal stem cells differentiate into insulin-producing cells upon microenvironmental manipulation in vitro,” Differentiation, vol. 77, no. 5, pp. 483–491, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. Q. Y. Dong, L. Chen, G. Q. Gao et al., “Allogeneic diabetic mesenchymal stem cells transplantation in streptozotocin-induced diabetic rat,” Clinical and Investigative Medicine, vol. 31, no. 6, pp. E328–E337, 2008. View at Google Scholar · View at Scopus
  11. T. Ito, S. Itakura, I. Todorov et al., “Mesenchymal stem cell and islet co-transplantation promotes graft revascularization and function,” Transplantation, vol. 89, no. 12, pp. 1438–1445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. G. C. Schatteman, O. Awad et al., “Hemangioblasts, angioblasts, and adult endothelial cell progenitors,” Anatomical Record—Part A Discoveries in Molecular, Cellular, and Evolutionary Biology, vol. 276, no. 1, pp. 13–21, 2004. View at Google Scholar · View at Scopus
  13. G. P. Fadini, S. Sartore, M. Schiavon et al., “Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia-reperfusion injury in rats,” Diabetologia, vol. 49, no. 12, pp. 3075–3084, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. 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
  15. 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
  16. T. Kusuyama, T. Omura, D. Nishiya et al., “Effects of treatment for diabetes mellitus on circulating vascular progenitor cells,” Journal of Pharmacological Sciences, vol. 102, no. 1, pp. 96–102, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. G. P. Fadini, L. Pucci, R. Vanacore et al., “Glucose tolerance is negatively associated with circulating progenitor cell levels,” Diabetologia, vol. 50, no. 10, pp. 2156–2163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. C. G. Egan, R. Lavery, F. Caporali et al., “Generalised reduction of putative endothelial progenitors and CXCR4-positive peripheral blood cells in type 2 diabetes,” Diabetologia, vol. 51, no. 7, pp. 1296–1305, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. V. Busik, M. Tikhonenko, A. Bhatwadekar et al., “Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock,” Journal of Experimental Medicine, vol. 206, no. 13, pp. 2897–2906, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Thum, D. Fraccarollo, M. Schultheiss et al., “Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes,” Diabetes, vol. 56, no. 3, pp. 666–674, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Heissig, K. Hattori, S. Dias et al., “Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of Kit-ligand,” Cell, vol. 109, no. 5, pp. 625–637, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. M. S. Segal, R. Shah, A. Afzal et al., “Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes,” Diabetes, vol. 55, no. 1, pp. 102–109, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. W. S. Browner, L. Y. Lui, and S. R. Cummings, “Associations of serum osteoprotegerin levels with diabetes, stroke, bone density, fractures, and mortality in elderly women,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 2, pp. 631–637, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Candido, B. Toffoli, F. Corallini et al., “Human full-length osteoprotegerin induces the proliferation of rodent vascular smooth muscle cells both in vitro and in vivo,” Journal of Vascular Research, vol. 47, no. 3, pp. 252–261, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Toffoli, S. Bernardi, R. Candido et al., “Osteoprotegerin induces morphological and functional alterations in mouse pancreatic islets,” Molecular and Cellular Endocrinology, vol. 331, no. 1, pp. 136–142, 2011. View at Publisher · View at Google Scholar
  26. P. Secchiero, E. Melloni, F. Corallini et al., “Tumor necrosis factor-related apoptosis-inducing ligand promotes migration of human bone marrow multipotent stromal cells,” Stem Cells, vol. 26, no. 11, pp. 2955–2963, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Corallini, P. Secchiero, A. P. Beltrami et al., “TNF-α modulates the migratory response of mesenchymal stem cells to TRAIL,” Cellular and Molecular Life Sciences, vol. 67, no. 8, pp. 1307–1314, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Kuki, T. Imanishi, K. Kobayashi, Y. Matsuo, M. Obana, and T. Akasaka, “Hyperglycemia accelerated endothelial progenitor cell senescence via the activation of p38 mitogen-activated protein kinase,” Circulation Journal, vol. 70, no. 8, pp. 1076–1081, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Rosso, A. Balsamo, R. Gambino et al., “p53 mediates the accelerated onset of senescence of endothelial progenitor cells in diabetes,” Journal of Biological Chemistry, vol. 281, no. 7, pp. 4339–4347, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. M. L. Balestrieri, M. Rienzo, F. Felice et al., “High glucose downregulates endothelial progenitor cell number via SIRT1,” Biochimica et Biophysica Acta, vol. 1784, no. 6, pp. 936–945, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Vasa, K. Breitschopf, A. M. Zeiher, and S. Dimmeler, “Nitric oxide activates telomerase and delays endothelial cell senescence,” Circulation Research, vol. 87, no. 7, pp. 540–542, 2000. View at Google Scholar · View at Scopus
  32. V. Di Stefano, C. Cencioni, G. Zaccagnini, A. Magenta, M. C. Capogrossi, and F. Martelli, “P66 ShcA modulates oxidative stress and survival of endothelial progenitor cells in response to high glucose,” Cardiovascular Research, vol. 82, no. 3, pp. 421–429, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. G. P. Fadini, E. Boscaro, S. De Kreutzenberg et al., “Time course and mechanisms of circulating progenitor cell reduction in the natural history of type 2 diabetes,” Diabetes Care, vol. 33, no. 5, pp. 1097–1102, 2010. View at Publisher · View at Google Scholar
  34. T. Ishizuka, T. Hinata, and Y. Watanabe, “Superoxide induced by a high-glucose concentration attenuates production of angiogenic growth factors in hypoxic mouse mesenchymal stem cells,” Journal of Endocrinology, vol. 208, no. 2, pp. 147–159, 2011. View at Publisher · View at Google Scholar
  35. Q. Chen, L. Dong, L. Wang, L. Kang, and B. Xu, “Advanced glycation end products impair function of late endothelial progenitor cells through effects on protein kinase Akt and cyclooxygenase-2,” Biochemical and Biophysical Research Communications, vol. 381, no. 2, pp. 192–197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Sun, C. Liang, Y. Ren et al., “Advanced glycation end products depress function of endothelial progenitor cells via p38 and ERK 1/2 mitogen-activated protein kinase pathways,” Basic Research in Cardiology, vol. 104, no. 1, pp. 42–49, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. R. J. Scheubel, S. Kahrstedt, H. Weber et al., “Depression of progenitor cell function by advanced glycation endproducts (AGEs): potential relevance for impaired angiogenesis in advanced age and diabetes,” Experimental Gerontology, vol. 41, no. 5, pp. 540–548, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Stolzing, D. Sellers, O. Llewelyn, and A. Scutt, “Diabetes induced changes in rat mesenchymal stem cells,” Cells Tissues Organs, vol. 191, no. 6, pp. 453–465, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Kume, S. Kato, S. I. Yamagishi et al., “Advanced glycation end-products attenuate human mesenchymal stem cells and prevent cognate differentiation into adipose tissue, cartilage, and bone,” Journal of Bone and Mineral Research, vol. 20, no. 9, pp. 1647–1658, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. J. A. Beckman, M. A. Creager, and P. Libby, “Diabetes and atherosclerosis epidemiology, pathophysiology, and management,” Journal of the American Medical Association, vol. 287, no. 19, pp. 2570–2581, 2002. View at Google Scholar · View at Scopus
  41. P. Secchiero, R. Candido, F. Corallini et al., “Systemic tumor necrosis factor-related apoptosis-inducing ligand delivery shows antiatherosclerotic activity in apolipoprotein E-null diabetic mice,” Circulation, vol. 114, no. 14, pp. 1522–1530, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Schmidt-Lucke, L. Rössig, S. Fichtlscherer et al., “Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair,” Circulation, vol. 111, no. 22, pp. 2981–2987, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Werner, S. Kosiol, T. Schiegl et al., “Circulating endothelial progenitor cells and cardiovascular outcomes,” The New England Journal of Medicine, vol. 353, no. 10, pp. 999–1007, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. G. P. Fadini, S. Maruyama, T. Ozaki et al., “Circulating progenitor cell count for cardiovascular risk stratification: a pooled analysis,” PLoS ONE, vol. 5, no. 7, Article ID e11488, 2010. View at Publisher · View at Google Scholar
  45. G. P. Fadini, S. Sartore, M. Albiero et al., “Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 9, pp. 2140–2146, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. G. P. Fadini, M. Miorin, M. Facco et al., “Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus,” Journal of the American College of Cardiology, vol. 45, no. 9, pp. 1449–1457, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. L. Ma, X. L. Mai, J. H. Sun et al., “Inhibited atherosclerotic plaque formation by local administration of magnetically labeled endothelial progenitor cells (EPCs) in a rabbit model,” Atherosclerosis, vol. 205, no. 1, pp. 80–86, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. S. Silvestre, A. Gojova, V. Brun et al., “Transplantation of bone marrow-derived mononuclear cells in ischemic apolipoprotein e-Knockout mice accelerates atherosclerosis without altering plaque composition,” Circulation, vol. 108, no. 23, pp. 2839–2842, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. P. E. Westerweel, C. T. J. van Velthoven, T. Q. Nguyen et al., “Modulation of TGF-β/BMP-6 expression and increased levels of circulating smooth muscle progenitor cells in a type I diabetes mouse model,” Cardiovascular Diabetology, vol. 9, p. 55, 2010. View at Publisher · View at Google Scholar
  50. H. J. Kang, H. S. Kim, S. Y. Zhang et al., “Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial,” The Lancet, vol. 363, no. 9411, pp. 751–756, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Menasché, “Stem cell therapy for heart failure: are arrhythmias a real safety concern?” Circulation, vol. 119, no. 20, pp. 2735–2740, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Dimmeler, J. Burchfield, and A. M. Zeiher, “Cell-based therapy of myocardial infarction,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 2, pp. 208–216, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. J. M. Hare, J. H. Traverse, T. D. Henry et al., “A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction,” Journal of the American College of Cardiology, vol. 54, no. 24, pp. 2277–2286, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Takahashi, C. Kalka, H. Masuda et al., “Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization,” Nature Medicine, vol. 5, no. 4, pp. 434–438, 1999. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Murohara, H. Ikeda, J. Duan et al., “Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization,” Journal of Clinical Investigation, vol. 105, no. 11, pp. 1527–1536, 2000. View at Google Scholar · View at Scopus
  56. C. Kalka, H. Masuda, T. Takahashi et al., “Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 7, pp. 3422–3427, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. G. P. Fadini, C. Agostini, and A. Avogaro, “Autologous stem cell therapy for peripheral arterial disease. Meta-analysis and systematic review of the literature,” Atherosclerosis, vol. 209, no. 1, pp. 10–17, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. G. C. Schatteman, H. D. Hanlon, C. Jiao, S. G. Dodds, and B. A. Christy, “Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice,” Journal of Clinical Investigation, vol. 106, no. 4, pp. 571–578, 2000. View at Google Scholar · View at Scopus
  59. K. Hirata, T. S. Li, M. Nishida et al., “Autologous bone marrow cell implantation as therapeutic angiogenesis for ischemic hindlimb in diabetic rat model,” American Journal of Physiology, vol. 284, no. 1, pp. H66–H70, 2003. View at Google Scholar · View at Scopus
  60. A. H. Amin, Z. Y. Abd Elmageed, D. Nair et al., “Modified multipotent stromal cells with epidermal growth factor restore vasculogenesis and blood flow in ischemic hind-limb of type II diabetic mice,” Laboratory Investigation, vol. 90, no. 7, pp. 985–996, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. U. M. Gehling, S. Ergün, U. Schumacher et al., “In vitro differentiation of endothelial cells from AC133-positive progenitor cells,” Blood, vol. 95, no. 10, pp. 3106–3112, 2000. View at Google Scholar · View at Scopus
  62. A. J. Comerota, A. Link, J. Douville, and E. R. Burchardt, “Upper extremity ischemia treated with tissue repair cells from adult bone marrow,” Journal of Vascular Surgery, vol. 52, no. 3, pp. 723–729, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. J. S. Lee, J. M. Hong, G. J. Moon, P. H. Lee, Y. H. Ahn, and O. Y. Bang, “A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke,” Stem Cells, vol. 28, no. 6, pp. 1099–1106, 2010. View at Publisher · View at Google Scholar
  64. B. Toffoli, S. Bernardi, R. Candido, S. Zacchigna, B. Fabris, and P. Secchiero, “TRAIL shows potential cardioprotective activity,” Investigational New Drugs. In press.
  65. M. Rota, N. LeCapitaine, T. Hosoda et al., “Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66shc gene,” Circulation Research, vol. 99, no. 1, pp. 42–52, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. S. Yoon, S. Uchida, O. Masuo et al., “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, vol. 111, no. 16, pp. 2073–2085, 2005. View at Publisher · View at Google Scholar
  67. N. Zhang, J. Li, R. Luo, J. Jiang, and J. A. Wang, “Bone marrow mesenchymal stem cells induce angiogenesis and attenuate the remodeling of diabetic cardiomyopathy,” Experimental and Clinical Endocrinology and Diabetes, vol. 116, no. 2, pp. 104–111, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Shabbir, D. Zisa, G. Suzuki, and T. Lee, “Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: a noninvasive therapeutic regimen,” American Journal of Physiology, vol. 296, no. 6, pp. H1888–H1897, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. M. E. Cooper, “Pathogenesis, prevention, and treatment of diabetic nephropathy,” Lancet, vol. 352, no. 9123, pp. 213–219, 1998. View at Publisher · View at Google Scholar · View at Scopus
  70. Y. Abe-Yoshio, K. Abe, M. Miyazaki et al., “Involvement of bone marrow-derived endothelial progenitor cells in glomerular capillary repair in habu snake venom-induced glomerulonephritis,” Virchows Archiv, vol. 453, no. 1, pp. 97–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. E. Ronconi, C. Sagrinati, M. L. Angelotti et al., “Regeneration of glomerular podocytes by human renal progenitors,” Journal of the American Society of Nephrology, vol. 20, no. 2, pp. 322–332, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. F. E. Ezquer, M. E. Ezquer, D. B. Parrau, D. Carpio, A. J. Yañez, and P. A. Conget, “Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice,” Biology of Blood and Marrow Transplantation, vol. 14, no. 6, pp. 631–640, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. F. Ezquer, M. Ezquer, V. Simon et al., “Endovenous administration of bone marrow-derived multipotent mesenchymal stromal cells prevents renal failure in diabetic mice,” Biology of Blood and Marrow Transplantation, vol. 15, no. 11, pp. 1354–1365, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. 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
  75. K. Naruse, Y. Hamada, E. Nakashima et al., “Therapeutic neovascularization using cord blood-derived endothelial progenitor cells for diabetic neuropathy,” Diabetes, vol. 54, no. 6, pp. 1823–1828, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. J. O. Jeong, M. O. Kim, H. Kim et al., “Dual angiogenic and neurotrophic effects of bone marrow-derived endothelial progenitor cells on diabetic neuropathy,” Circulation, vol. 119, no. 5, pp. 699–708, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. T. Shibata, K. Naruse, H. Kamiya et al., “Transplantation of bone marrow-derived mesenchymal stem cells improves diabetic polyneuropathy in rats,” Diabetes, vol. 57, no. 11, pp. 3099–3107, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Brunner, G. H. Schernthaner, M. Satler et al., “Correlation of different circulating endothelial progenitor cells to stages of diabetic retinopathy: first in vivo data,” Investigative Ophthalmology and Visual Science, vol. 50, no. 1, pp. 392–398, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. I. G. Lee, S. L. Chae, and J. C. Kim, “Involvement of circulating endothelial progenitor cells and vasculogenic factors in the pathogenesis of diabetic retinopathy,” Eye, vol. 20, no. 5, pp. 546–552, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. M. B. Grant, W. S. May, S. Caballero et al., “Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization,” Nature Medicine, vol. 8, no. 6, pp. 607–612, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. M. R. Ritter, E. Banin, S. K. Moreno, E. Aguilar, M. I. Dorrell, and M. Friedlander, “Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy,” Journal of Clinical Investigation, vol. 116, no. 12, pp. 3266–3276, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. Z. Yang, K. Li, X. Yan, F. Dong, and C. Zhao, “Amelioration of diabetic retinopathy by engrafted human adipose-derived mesenchymal stem cells in streptozotocin diabetic rats,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 248, no. 10, pp. 1415–1422, 2010. View at Publisher · View at Google Scholar
  83. M. Albiero, L. Menegazzo, E. Boscaro, C. Agostini, A. Avogaro, and G. P. Fadini, “Defective recruitment, survival and proliferation of bone marrow-derived progenitor cells at sites of delayed diabetic wound healing in mice,” Diabetologia, vol. 54, no. 4, pp. 945–953, 2011. View at Google Scholar
  84. Y. Wu, R. C. H. Zhao, and E. E. Tredget, “Concise review: bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration,” Stem Cells, vol. 28, no. 5, pp. 905–915, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. M. Gill, S. Dias, K. Hattori et al., “Vascular trauma induces rapid but transient mobilization of VEGFR2+ AC133+ endothelial precursor cells,” Circulation Research, vol. 88, no. 2, pp. 167–174, 2001. View at Google Scholar · View at Scopus
  86. W. Suh, K. L. Kim, J. M. Kim et al., “Transplantation of endothelial progenitor cells accelerates dermal wound healing with increased recruitment of monocytes/macrophages and neovascularization,” Stem Cells, vol. 23, no. 10, pp. 1571–1578, 2005. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Rehman, J. Li, C. M. Orschell, and K. L. March, “Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors,” Circulation, vol. 107, no. 8, pp. 1164–1169, 2003. View at Publisher · View at Google Scholar · View at Scopus
  88. Y. Wu, L. Chen, P. G. Scott, and E. E. Tredget, “Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis,” Stem Cells, vol. 25, no. 10, pp. 2648–2659, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. D. S. Kwon, X. Gao, Y. B. Liu et al., “Treatment with bone marrow-derived stromal cells accelerates wound healing in diabetic rats,” International Wound Journal, vol. 5, no. 3, pp. 453–463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. J. Vojtaššák, L. Danišovič, M. Kubeš et al., “Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot,” Neuroendocrinology Letters, vol. 27, supplement 2, pp. 134–137, 2006. View at Google Scholar
  91. E. Sivan-Loukianova, O. A. Awad, V. Stepanovic, J. Bickenbach, and G. C. Schatteman, “CD34+ blood cells accelerate vascularization and healing of diabetic mouse skin wounds,” Journal of Vascular Research, vol. 40, no. 4, pp. 368–377, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. L. S. Barcelos, C. Duplaa, N. Kränkel et al., “Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling,” Circulation Research, vol. 104, no. 9, pp. 1095–1102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. E. J. Marrotte, D. D. Chen, J. S. Hakim, and A. F. Chen, “Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice,” Journal of Clinical Investigation, vol. 120, no. 12, pp. 4207–4219, 2010. View at Publisher · View at Google Scholar
  94. S. Murasawa, J. Llevadot, M. Silver, J. M. Isner, D. W. Losordo, and T. Asahara, “Constitutive human telomerase reverse transcriptase expression enhances regenerative properties of endothelial progenitor cells,” Circulation, vol. 106, no. 9, pp. 1133–1139, 2002. View at Publisher · View at Google Scholar · View at Scopus
  95. J. H. Choi, J. Hurt, C. H. Yoon et al., “Augmentation of therapeutic augiogenesis using genetically modified human endothelial progenitor cells with altered glycogen synthase kinase-3β activity,” Journal of Biological Chemistry, vol. 279, no. 47, pp. 49430–49438, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. H. Li, S. Zuo, Z. He et al., “Paracrine factors released by GATA-4 overexpressed mesenchymal stem cells increase angiogenesis and cell survival,” American Journal of Physiology, vol. 299, no. 6, pp. H1772–H1781, 2010. View at Publisher · View at Google Scholar
  97. D. Zhang, G. C. Fan, X. Zhou et al., “Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium,” Journal of Molecular and Cellular Cardiology, vol. 44, no. 2, pp. 281–292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. A. A. Mangi, N. Noiseux, D. Kong et al., “Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts,” Nature Medicine, vol. 9, no. 9, pp. 1195–1201, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. K. I. Sasaki, C. Heeschen, A. Aicher et al., “Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 39, pp. 14537–14541, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. T. Thum, F. Fleissner, I. Klink et al., “Growth hormone treatment improves markers of systemic nitric oxide bioavailability via insulin-like growth factor-I,” Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 11, pp. 4172–4179, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. G. Ceolotto, A. Gallo, I. Papparella et al., “Rosiglitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPK-dependent mechanism,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 12, pp. 2627–2633, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. S. A. Sorrentino, F. H. Bahlmann, C. Besler et al., “Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-γ agonist rosiglitazone,” Circulation, vol. 116, no. 2, pp. 163–173, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. F. H. Seeger, J. Haendeler, D. H. Walter et al., “p38 mitogen-activated protein kinase downregulates endothelial progenitor cells,” Circulation, vol. 111, no. 9, pp. 1184–1191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Khan, S. Akhtar, S. Mohsin, N. Khan, and S. Riazuddin, “Growth factor preconditioning increases the function of diabetes-impaired mesenchymal stem cells,” Stem Cells and Development, vol. 20, no. 1, pp. 67–75, 2011. View at Publisher · View at Google Scholar
  105. C. Jiao, S. Fricker, and G. C. Schatteman, “The chemokine (C-X-C motif) receptor 4 inhibitor AMD3100 accelerates blood flow restoration in diabetic mice,” Diabetologia, vol. 49, no. 11, pp. 2786–2789, 2006. View at Publisher · View at Google Scholar · View at Scopus