Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2012, Article ID 175979, 11 pages
http://dx.doi.org/10.1155/2012/175979
Review Article

Mesenchymal Stem Cells and Cardiovascular Disease: A Bench to Bedside Roadmap

Department of Hematology and Cell Therapy, Clínica Universidad de Navarra, Foundation for Applied Medical Research, University of Navarra, Avenida Pío XII 36, Pamplona, 31008 Navarra, Spain

Received 1 September 2011; Accepted 13 October 2011

Academic Editor: Wolfgang Wagner

Copyright © 2012 Manuel Mazo 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. World Health Organization, World Health Statistics 2008, 2008.
  2. M. Mazo, B. Pelacho, and F. Prósper, “Stem cell therapy for chronic myocardial infarction,” Journal of Cardiovascular Translational Research, vol. 3, no. 2, pp. 79–88, 2010. View at Publisher · View at Google Scholar
  3. N. G. Frangogiannis, “Chemokines in the ischemic myocardium: from inflammation to fibrosis,” Inflammation Research, vol. 53, no. 11, pp. 585–595, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. A. J. Friedenstein, K. V. Petrakova, A. I. Kurolesova, and G. P. Frolova, “Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues,” Transplantation, vol. 6, no. 2, pp. 230–247, 1968. View at Google Scholar · View at Scopus
  5. B. Pelacho and F. Prosper, “Stem cells and cardiac disease: where are we going?” Current Stem Cell Research & Therapy, vol. 3, no. 4, pp. 265–276, 2008. View at Google Scholar · View at Scopus
  6. C. Clavel and C. M. Verfaillie, “Bone-marrow-derived cells and heart repair,” Current Opinion in Organ Transplantation, vol. 13, no. 1, pp. 36–43, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Walenda, S. Bork, P. Horn et al., “Co-culture with mesenchymal stromal cells increases proliferation and maintenance of haematopoietic progenitor cells,” Journal of Cellular and Molecular Medicine, vol. 14, no. 1-2, pp. 337–350, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. D. L. Jones and A. J. Wagers, “No place like home: anatomy and function of the stem cell niche,” Nature Reviews Molecular Cell Biology, vol. 9, no. 1, pp. 11–21, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. W. Wagner, C. Roderburg, F. Wein et al., “Molecular and secretory profiles of human mesenchymal stromal cells and their abilities to maintain primitive hematopoietic progenitors,” Stem Cells, vol. 25, no. 10, pp. 2638–2647, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. X. Cai, Y. Lin, C. C. Friedrich et al., “Bone marrow derived pluripotent cells are pericytes which contribute to vascularization,” Stem Cell Reviews and Reports, vol. 5, no. 4, pp. 437–445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. 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
  12. M. Mazo, J. J. Gavira, B. Pelacho, and F. Prosper, “Adipose-derived stem cells for myocardial infarction,” Journal of Cardiovascular Translational Research, vol. 4, no. 2, pp. 145–153, 2011. View at Publisher · View at Google Scholar
  13. L. Casteilla, V. Planat-Benard, P. Laharrague, and B. Cousin, “Adipose-derived stromal cells: their identity and uses in clinical trials, an update,” World Journal of Stem Cells, vol. 3, pp. 25–33, 2011. View at Google Scholar
  14. S. Kern, H. Eichler, J. Stoeve, H. Kluter, and K. Bieback, “Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue,” Stem Cells, vol. 24, no. 5, pp. 1294–1301, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. J. M. Gimble, A. J. Katz, and B. A. Bunnell, “Adipose-derived stem cells for regenerative medicine,” Circulation Research, vol. 100, no. 9, pp. 1249–1260, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. S. E. Yang, C. W. Ha, M. H. Jung et al., “Mesenchymal stem/progenitor cells developed in cultures from UC blood,” Cytotherapy, vol. 6, no. 5, pp. 476–486, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Gandia, A. N.A. Armiñan, J. M. García-Verdugo et al., “Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction,” Stem Cells, vol. 26, no. 3, pp. 638–645, 2008. View at Publisher · View at Google Scholar
  18. N. Hida, N. Nishiyama, S. Miyoshi et al., “Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells,” Stem Cells, vol. 26, no. 7, pp. 1695–1704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Carlson, J. Trial, C. Soeller, and M. L. Entman, “Cardiac mesenchymal stem cells contribute to scar formation after myocardial infarction,” Cardiovascular Research, vol. 91, no. 1, pp. 99–107, 2011. View at Publisher · View at Google Scholar
  20. D. C. Ding, W. C. Shyu, and S. Z. Lin, “Mesenchymal stem cells,” Cell Transplant, vol. 20, pp. 5–14, 2011. View at Google Scholar
  21. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. E. M. Horwitz, K. Le Blanc, M. Dominici et al., “Clarification of the nomenclature for MSC: the international society for cellular therapy position statement,” Cytotherapy, vol. 7, no. 5, pp. 393–395, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Sacchetti, A. Funari, S. Michienzi et al., “Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment,” Cell, vol. 131, no. 2, pp. 324–336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. T. P. Lozito, J. M. Taboas, C. K. Kuo, and R. S. Tuan, “Mesenchymal stem cell modification of endothelial matrix regulates their vascular differentiation,” Journal of Cellular Biochemistry, vol. 107, no. 4, pp. 706–713, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. J. W. Liu, S. Dunoyer-Geindre, V. Serre-Beinier et al., “Characterization of endothelial-like cells derived from human mesenchymal stem cells,” Journal of Thrombosis and Haemostasis, vol. 5, no. 4, pp. 826–834, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Xu, X. Zhang, H. Qian et al., “Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro,” Experimental Biology and Medicine, vol. 229, no. 7, pp. 623–631, 2004. View at Google Scholar · View at Scopus
  27. X. Yan, A. Lv, Y. Xing et al., “Inhibition of p53-p21 pathway promotes the differentiation of rat bone marrow mesenchymal stem cells into cardiomyocytes,” Molecular and Cellular Biochemistry, vol. 354, no. 1-2, pp. 21–28, 2011. View at Publisher · View at Google Scholar
  28. A. Armiñán, C. Gandía, J. M. García-Verdugo et al., “Cardiac transcription factors driven lineage-specification of adult stem cells,” Journal of Cardiovascular Translational Research, vol. 3, no. 1, pp. 61–65, 2010. View at Publisher · View at Google Scholar
  29. A. van Dijk, H. W. M. Niessen, B. Zandieh Doulabi, F. C. Visser, and F. J. Van Milligen, “Differentiation of human adipose-derived stem cells towards cardiomyocytes is facilitated by laminin,” Cell and Tissue Research, vol. 334, no. 3, pp. 457–467, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. K. G. Gaustad, A. C. Boquest, B. E. Anderson, A. M. Gerdes, and P. Collas, “Differentiation of human adipose tissue stem cells using extracts of rat cardiomyocytes,” Biochemical and Biophysical Research Communications, vol. 314, no. 2, pp. 420–427, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. X. Bai, K. Pinkernell, Y. H. Song, C. Nabzdyk, J. Reiser, and E. Alt, “Genetically selected stem cells from human adipose tissue express cardiac markers,” Biochemical and Biophysical Research Communications, vol. 353, no. 3, pp. 665–671, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. H. Song, S. Gehmert, S. Sadat et al., “VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes,” Biochemical and Biophysical Research Communications, vol. 354, no. 4, pp. 999–1003, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. M. Kim, E. S. Jeon, M. R. Kim, S. K. Jho, S. W. Ryu, and J. H. Kim, “Angiotensin II-induced differentiation of adipose tissue-derived mesenchymal stem cells to smooth muscle-like cells,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 11, pp. 2482–2491, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Planat-Benard, J. S. Silvestre, B. Cousin et al., “Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives,” Circulation, vol. 109, no. 5, pp. 656–663, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. L. J. Fischer, S. McIlhenny, T. Tulenko et al., “Endothelial differentiation of adipose-derived stem cells: effects of endothelial cell growth supplement and shear force,” Journal of Surgical Research, vol. 152, no. 1, pp. 157–166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Sengenès, A. Miranville, M. Maumus, S. De Barros, R. Busse, and A. Bouloumié, “Chemotaxis and differentiation of human adipose tissue CD34 +/CD31- progenitor cells: role of stromal derived factor-1 released by adipose tissue capillary endothelial cells,” Stem Cells, vol. 25, no. 9, pp. 2269–2276, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Chang, J. L. Eun, H. J. Kang et al., “Impact of myocardial infarct proteins and oscillating pressure on the differentiation of mesenchymal stem cells: effect of acute myocardial infarction on stem cell differentiation,” Stem Cells, vol. 26, no. 7, pp. 1901–1912, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Kondo, M. Hayashi, K. Takeshita et al., “Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 8, pp. 1442–1447, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Vasa, S. Fichtlscherer, A. Aicher et al., “Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease,” Circulation research, vol. 89, no. 1, pp. E1–7, 2001. View at Google Scholar · View at Scopus
  40. R. Madonna, F. V. Renna, C. Cellini et al., “Age-dependent impairment of number and angiogenic potential of adipose tissue-derived progenitor cells,” European Journal of Clinical Investigation, vol. 41, no. 2, pp. 126–133, 2011. View at Publisher · View at Google Scholar
  41. H. Liang, H. Hou, W. Yi, G. Yang, C. Gu, W. B. Lau et al., “Increased expression of pigment epithelium-derived factor in aged mesenchymal stem cells impairs their therapeutic efficacy for attenuating myocardial infarction injury,” European Heart Journal. In press. View at Publisher · View at Google Scholar
  42. H. K. Haider and M. Ashraf, “Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation,” Journal of Molecular and Cellular Cardiology, vol. 45, no. 4, pp. 554–566, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. T. E. Robey, M. K. Saiget, H. Reinecke, and C. E. Murry, “Systems approaches to preventing transplanted cell death in cardiac repair,” Journal of Molecular and Cellular Cardiology, vol. 45, no. 4, pp. 567–581, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. P. W. M. Fedak, “Paracrine effects of cell transplantation: modifying ventricular remodeling in the failing heart,” Seminars in Thoracic and Cardiovascular Surgery, vol. 20, no. 2, pp. 87–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Chen, E. E. Tredget, P. Y. G. Wu, Y. Wu, and Y. Wu, “Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing,” PLoS ONE, vol. 3, no. 4, Article ID e1886, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Oskowitz, H. McFerrin, M. Gutschow, M. L. Carter, and R. Pochampally, “Serum-deprived human multipotent mesenchymal stromal cells (MSCs) are highly angiogenic,” Stem Cell Research, vol. 6, no. 3, pp. 215–225, 2011. View at Publisher · View at Google Scholar
  47. G. E. Kilroy, S. J. Foster, X. Wu et al., “Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors,” Journal of Cellular Physiology, vol. 212, no. 3, pp. 702–709, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. D. O. Traktuev, S. Merfeld-Clauss, J. Li et al., “A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks,” Circulation Research, vol. 102, no. 1, pp. 77–85, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. D. O. Traktuev, D. N. Prater, S. Merfeld-Clauss et al., “Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells,” Circulation Research, vol. 104, no. 12, pp. 1410–1420, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Li, S. Zhang, Y. Zhang, B. Yu, Y. Xu, and Z. Guan, “Paracrine action mediate the antifibrotic effect of transplanted mesenchymal stem cells in a rat model of global heart failure,” Molecular Biology Reports, vol. 36, no. 4, pp. 725–731, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Ohnishi, H. Sumiyoshi, S. Kitamura, and N. Nagaya, “Mesenchymal stem cells attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions,” FEBS Letters, vol. 581, no. 21, pp. 3961–3966, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Mias, O. Lairez, E. Trouche et al., “Mesenchymal stem cells promote matrix metalloproteinase secretion by cardiac fibroblasts and reduce cardiac ventricular fibrosis after myocardial infarction,” Stem Cells, vol. 27, no. 11, pp. 2734–2743, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. T. B. Rogers, S. Pati, S. Gaa et al., “Mesenchymal stem cells stimulate protective genetic reprogramming of injured cardiac ventricular myocytes,” Journal of Molecular and Cellular Cardiology, vol. 50, no. 2, pp. 346–356, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Rehman, D. Traktuev, J. Li et al., “Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells,” Circulation, vol. 109, no. 10, pp. 1292–1298, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. 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
  56. X. P. Huang, Z. Sun, Y. Miyagi et al., “Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair,” Circulation, vol. 122, no. 23, pp. 2419–2429, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. J. B. Mitchell, K. McIntosh, S. Zvonic et al., “Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers,” Stem Cells, vol. 24, no. 2, pp. 376–385, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. K. McIntosh, S. Zvonic, S. Garrett et al., “The immunogenicity of human adipose-derived cells: temporal changes in vitro,” Stem Cells, vol. 24, no. 5, pp. 1246–1253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. M. J. Crop, C. C. Baan, S. S. Korevaar et al., “Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells,” Clinical and experimental immunology, vol. 162, no. 3, pp. 474–486, 2010. View at Google Scholar
  60. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. P. A. Tat, H. Sumer, K. L. Jones, K. Upton, and P. J. Verma, “The efficient generation of induced pluripotent stem (iPS) cells from adult mouse adipose tissue-derived and neural stem cells,” Cell Transplantation, vol. 19, no. 5, pp. 525–536, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. N. Sun, N. J. Panetta, D. M. Gupta et al., “Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 37, pp. 15720–15725, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. M. K. Mamidi, R. Pal, N. A.B. Mori et al., “Co-culture of mesenchymal-like stromal cells derived from human foreskin permits long term propagation and differentiation of human embryonic stem cells,” Journal of Cellular Biochemistry, vol. 112, no. 5, pp. 1353–1363, 2011. View at Publisher · View at Google Scholar
  64. S. T. Hwang, S. W. Kang, S. J. Lee et al., “The expansion of human ES and iPS cells on porous membranes and proliferating human adipose-derived feeder cells,” Biomaterials, vol. 31, no. 31, pp. 8012–8021, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Nian, P. Lee, N. Khaper, and P. Liu, “Inflammatory cytokines and postmyocardial infarction remodeling,” Circulation Research, vol. 94, no. 12, pp. 1543–1553, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. D. L. Mann, “Mechanisms and models in heart failure: a combinatorial approach,” Circulation, vol. 100, no. 9, pp. 999–1008, 1999. View at Google Scholar · View at Scopus
  67. M. S. Penn, “Importance of the SDF-1: CXCR4 axis in myocardial repair,” Circulation Research, vol. 104, no. 10, pp. 1133–1135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. J. P. M. Cleutjens, J. C. Kandala, E. Guarda, R. V. Guntaka, and K. T. Weber, “Regulation of collagen degradation in the rat myocardium after infarction,” Journal of Molecular and Cellular Cardiology, vol. 27, no. 6, pp. 1281–1292, 1995. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Ii, M. Horii, A. Yokoyama et al., “Synergistic effect of adipose-derived stem cell therapy and bone marrow progenitor recruitment in ischemic heart,” Laboratory Investigation, vol. 91, no. 4, pp. 539–552, 2011. View at Publisher · View at Google Scholar
  70. R. Gaebel, D. Furlani, H. Sorg et al., “Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration,” PLoS ONE, vol. 6, no. 2, Article ID e15652, 2011. View at Publisher · View at Google Scholar
  71. X. Bai, Y. Yan, M. Coleman et al., “Tracking long-term survival of intramyocardially delivered human adipose tissue-derived stem cells using bioluminescence imaging,” Molecular Imaging and Biology, pp. 1–13, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Dubois, X. Liu, P. Claus et al., “Differential Effects of Progenitor Cell Populations on Left Ventricular Remodeling and Myocardial Neovascularization After Myocardial Infarction,” Journal of the American College of Cardiology, vol. 55, no. 20, pp. 2232–2243, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. J. Yang, H. Y. Qian, J. Huang et al., “Combined therapy with simvastatin and bone marrow-derived mesenchymal stem cells increases benefits in infarcted swine hearts,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 12, pp. 2076–2082, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. K. E. A. van der Bogt, S. Schrepfer, J. Yu et al., “Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart,” Transplantation, vol. 87, no. 5, pp. 642–652, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. J. A. Dixon, R. C. Gorman, R. E. Stroud et al., “Mesenchymal cell transplantation and myocardial remodeling after myocardial infarction,” Circulation, vol. 120, no. 1, pp. S220–S229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. X. Bai, Y. Yan, Y. H. Song et al., “Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction,” European Heart Journal, vol. 31, no. 4, pp. 489–501, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. K. E. van der Bogt, A. Y. Sheikh, S. Schrepfer et al., “Comparison of different adult stem cell types for treatment of myocardial ischemia,” Circulation, vol. 118, no. 14, pp. S121–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. Imanishi, A. Saito, H. Komoda et al., “Allogenic mesenchymal stem cell transplantation has a therapeutic effect in acute myocardial infarction in rats,” Journal of Molecular and Cellular Cardiology, vol. 44, no. 4, pp. 662–671, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. S. M. Hashemi, S. Ghods, F. D. Kolodgie et al., “A placebo controlled, dose-ranging, safety study of allogenic mesenchymal stem cells injected by endomyocardial delivery after an acute myocardial infarction,” European Heart Journal, vol. 29, no. 2, pp. 251–259, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. S. L. Hale, W. Dai, J. S. Dow, and R. A. Kloner, “Mesenchymal stem cell administration at coronary artery reperfusion in the rat by two delivery routes: a quantitative assessment,” Life Sciences, vol. 83, no. 13-14, pp. 511–515, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. C. A. Carr, D. J. Stuckey, L. Tatton et al., “Bone marrow-derived stromal cells home to and remain in the infarcted rat heart but fail to improve function: an in vivo cine-MRI study,” American Journal of Physiology, Heart and Circulatory Physiology, vol. 295, no. 2, pp. H533–H542, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. L. Cai, B. H. Johnstone, T. G. Cook et al., “IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function,” Stem Cells, vol. 27, no. 1, pp. 230–237, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. C. Valina, K. Pinkernell, Y. H. Song et al., “Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction,” European Heart Journal, vol. 28, no. 21, pp. 2667–2677, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. B. Li, Q. Zeng, H. Wang et al., “Adipose tissue stromal cells transplantation in rats of acute myocardial infarction,” Coronary Artery Disease, vol. 18, no. 3, pp. 221–227, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. J. I. Virag and C. E. Murry, “Myofibroblast and endothelial cell proliferation during murine myocardial infarct repair,” American Journal of Pathology, vol. 163, no. 6, pp. 2433–2440, 2003. View at Google Scholar · View at Scopus
  86. Y. Sun, M. F. Kiani, A. E. Postlethwaite, and K. T. Weber, “Infarct scar as living tissue,” Basic Research in Cardiology, vol. 97, no. 5, pp. 343–347, 2002. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Song, M. J. Cha, B. W. Song et al., “Reactive oxygen species inhibit adhesion of mesenchymal stem cells implanted into ischemic myocardium via interference of focal adhesion complex,” Stem Cells, vol. 28, no. 3, pp. 555–563, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Mazo, J. J. Gavira, G. Abizanda et al., “Transplantation of mesenchymal stem cells exerts a greater long-term effect than bone marrow mononuclear cells in a chronic myocardial infarction model in rat,” Cell Transplantation, vol. 19, no. 3, pp. 313–328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. M. F. Chen, B. C. Lee, H. C. Hsu et al., “Cell therapy generates a favourable chemokine gradient for stem cell recruitment into the infarcted heart in rabbits,” European Journal of Heart Failure, vol. 11, no. 3, pp. 238–245, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Mazo, V. Planat-Bénard, G. Abizanda et al., “Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction,” European Journal of Heart Failure, vol. 10, no. 5, pp. 454–462, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. K. Jujo, M. Ii, and D. W. Losordo, “Endothelial progenitor cells in neovascularization of infarcted myocardium,” Journal of Molecular and Cellular Cardiology, vol. 45, no. 4, pp. 530–544, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Nahrendorf, F. K. Swirski, E. Aikawa et al., “The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions,” Journal of Experimental Medicine, vol. 204, no. 12, pp. 3037–3047, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Wang, J. Deng, W. Tian et al., “Adipose-derived stem cells are an effective cell candidate for treatment of heart failure: an MR imaging study of rat hearts,” American Journal of Physiology, Heart and Circulatory Physiology, vol. 297, no. 3, pp. H1020–H1031, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. L. C. Amado, A. P. Saliaris, K. H. Schuleri et al., “Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 32, pp. 11474–11479, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. H. Li, D. Malhotra, C. C. Yeh et al., “Myocardial survival signaling in response to stem cell transplantation,” Journal of the American College of Surgeons, vol. 208, no. 4, pp. 607–613, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. J. Cho, P. Zhai, Y. Maejima, and J. Sadoshima, “Myocardial injection with GSK-3β-overexpressing bone marrow-derived mesenchymal stem cells attenuates cardiac dysfunction after myocardial infarction,” Circulation Research, vol. 108, no. 4, pp. 478–489, 2011. View at Publisher · View at Google Scholar
  97. X. Wang, T. Zhao, W. Huang et al., “Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors,” Stem Cells, vol. 27, no. 12, pp. 3021–3031, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Le Blanc, “Mesenchymal stromal cells: tissue repair and immune modulation,” Cytotherapy, vol. 8, no. 6, pp. 559–561, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. K. H. Schuleri, L. C. Amado, A. J. Boyle et al., “Early improvement in cardiac tissue perfusion due to mesenchymal stem cells,” American Journal of Physiology, Heart and Circulatory Physiology, vol. 294, no. 5, pp. H2002–H2011, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. L. C. Amado, K. H. Schuleri, A. P. Saliaris et al., “Multimodality noninvasive imaging demonstrates in vivo cardiac regeneration after mesenchymal stem cell therapy,” Journal of the American College of Cardiology, vol. 48, no. 10, pp. 2116–2124, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Rigol, N. Solanes, J. Farré et al., “Effects of adipose tissue-derived stem cell therapy after myocardial infarction: impact of the route of administration,” Journal of Cardiac Failure, vol. 16, no. 4, pp. 357–366, 2010. View at Publisher · View at Google Scholar
  102. Y. Zhou, S. Wang, Z. Yu et al., “Direct injection of autologous mesenchymal stromal cells improves myocardial function,” Biochemical and Biophysical Research Communications, vol. 390, no. 3, pp. 902–907, 2009. View at Publisher · View at Google Scholar
  103. J. Ma, J. Ge, S. Zhang et al., “Time course of myocardial stromal cell-derived factor 1 expression and beneficial effects of intravenously administered bone marrow stem cells in rats with experimental myocardial infarction,” Basic Research in Cardiology, vol. 100, no. 3, pp. 217–223, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. Z. Cheng, L. Ou, X. Zhou et al., “Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance,” Molecular Therapy, vol. 16, no. 3, pp. 571–579, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. Z. Cheng, X. Liu, L. Ou et al., “Mobilization of mesenchymal stem cells by granulocyte colony-stimulating factor in rats with acute myocardial infarction,” Cardiovascular Drugs and Therapy, vol. 22, no. 5, pp. 363–371, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Huang, Z. Zhang, J. Guo et al., “Genetic modification of mesenchymal stem cells overexpressing ccr1 increases cell viability, migration, engraftment, and capillary density in the injured myocardium,” Circulation Research, vol. 106, no. 11, pp. 1753–1762, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. X. H. Liu, C. G. Bai, Z. Y. Xu et al., “Therapeutic potential of angiogenin modified mesenchymal stem cells: angiogenin improves mesenchymal stem cells survival under hypoxia and enhances vasculogenesis in myocardial infarction,” Microvascular Research, vol. 76, no. 1, pp. 23–30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Zeng, H. Chen, C. Zhu, X. Ren, G. Lin, and F. Cao, “Effects of combined mesenchymal stem cells and heme oxygenase-1 therapy on cardiac performance,” European Journal of Cardio-Thoracic Surgery, vol. 34, no. 4, pp. 850–856, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Gnecchi, H. He, L. G. Melo et al., “Early beneficial effects of bone marrow-derived mesenchymal stem cells overexpressing akt on cardiac metabolism after myocardial infarction,” Stem Cells, vol. 27, no. 4, pp. 971–979, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Gnecchi, H. He, N. Noiseux et al., “Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement,” FASEB Journal, vol. 20, no. 6, pp. 661–669, 2006. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Gnecchi, H. He, O. D. Liang et al., “Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells,” Nature Medicine, vol. 11, no. 4, pp. 367–368, 2005. View at Publisher · View at Google Scholar · View at Scopus
  112. H. Song, M. J. Cha, B. W. Song et al., “Reactive oxygen species inhibit adhesion of mesenchymal stem cells implanted into ischemic myocardium via interference of focal adhesion complex,” Stem Cells, vol. 28, no. 3, pp. 555–563, 2010. View at Publisher · View at Google Scholar · View at Scopus
  113. J. Jin, S. I. Jeong, Y. M. Shin et al., “Transplantation of mesenchymal stem cells within a poly(lactide-co-ε- caprolactone) scaffold improves cardiac function in a rat myocardial infarction model,” European Journal of Heart Failure, vol. 11, no. 2, pp. 147–153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Y. Tan, W. Zhi, R. Q. Wei et al., “Repair of infarcted myocardium using mesenchymal stem cell seeded small intestinal submucosa in rabbits,” Biomaterials, vol. 30, no. 19, pp. 3234–3240, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. C. H. Chen, H. J. Wei, W. W. Lin et al., “Porous tissue grafts sandwiched with multilayered mesenchymal stromal cell sheets induce tissue regeneration for cardiac repair,” Cardiovascular Research, vol. 80, no. 1, pp. 88–95, 2008. View at Publisher · View at Google Scholar · View at Scopus
  116. Y. Miyahara, N. Nagaya, M. Kataoka et al., “Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction,” Nature Medicine, vol. 12, no. 4, pp. 459–465, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. A. Bel, V. Planat-Bernard, A. Saito et al., “Composite cell sheets: a further step toward safe and effective myocardial regeneration by cardiac progenitors derived from embryonic stem cells,” Circulation, vol. 122, no. 11, pp. S118–S123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. S. Chen, Z. Liu, N. Tian et al., “Intracoronary transplantation of autologous bone marrow mesenchymal stem cells for ischemic cardiomyopathy due to isolated chronic occluded left anterior descending artery,” Journal of Invasive Cardiology, vol. 18, no. 11, pp. 552–556, 2006. View at Google Scholar · View at Scopus
  119. D. G. Katritsis, P. A. Sotiropoulou, E. Karvouni et al., “Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium,” Catheterization and Cardiovascular Interventions, vol. 65, no. 3, pp. 321–329, 2005. View at Publisher · View at Google Scholar
  120. S. L. Chen, W. W. Fang, F. Ye et al., “Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction,” American Journal of Cardiology, vol. 94, no. 1, pp. 92–95, 2004. View at Publisher · View at Google Scholar · View at Scopus
  121. J. M. Hare, “Translational development of mesenchymal stem cell therapy for cardiovascular diseases,” Texas Heart Institute Journal, vol. 36, no. 2, pp. 145–147, 2009. View at Google Scholar · View at Scopus
  122. 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
  123. N. Dib, T. Henry, A. DeMaria, S. Itescu, M. M. McCarthy, and S. C. Jaggar, “The first US study to assess the feasibility and safety of endocardial delivery of allogenic mesenchymal precursor cells in patient with heart failure: three-month interim analysis,” Circulation, vol. 120, p. S810, 2009. View at Google Scholar
  124. H. J. Duckers, J. Houtgraaf, R. J. van Geuns, B. D. van Dalen, E. Regar, and W. van der Giessen, “First-in-man experience with intracoronary infusion of adipose-derived regenerative cells in the treatment of patients with ST-elevation myocardial infarction: the apollo trial,” Circulation, vol. 120, Article ID A12225, 2010. View at Google Scholar
  125. A. Schaefer, C. Zwadlo, M. Fuchs et al., “Long-term effects of intracoronary bone marrow cell transfer on diastolic function in patients after acute myocardial infarction: 5-year results from the randomized-controlled BOOST trial—an echocardiographic study,” European Journal of Echocardiography, vol. 11, no. 2, pp. 165–171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  126. J. A. Miettinen, K. Ylitalo, P. Hedberg et al., “Determinants of functional recovery after myocardial infarction of patients treated with bone marrow-derived stem cells after thrombolytic therapy,” Heart, vol. 96, no. 5, pp. 362–367, 2009. View at Publisher · View at Google Scholar
  127. C. Stamm, H. D. Kleine, Y. H. Choi et al., “Intramyocardial delivery of CD133+ bone marrow cells and coronary artery bypass grafting for chronic ischemic heart disease: safety and efficacy studies,” Journal of Thoracic and Cardiovascular Surgery, vol. 133, no. 3, pp. 717–725, 2007. View at Publisher · View at Google Scholar · View at Scopus
  128. E. Martin-Rendon, S. J. Brunskill, C. J. Hyde, S. J. Stanworth, A. Mathur, and S. M. Watt, “Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review,” European Heart Journal, vol. 29, no. 15, pp. 1807–1818, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. T. S. Li, M. Kubo, K. Ueda, M. Murakami, A. Mikamo, and K. Hamano, “Impaired angiogenic potency of bone marrow cells from patients with advanced age, anemia, and renal failure,” Journal of Thoracic and Cardiovascular Surgery, vol. 139, no. 2, pp. 459–465, 2010. View at Publisher · View at Google Scholar · View at Scopus
  130. C. K. Kissel, R. Lehmann, B. Assmus et al., “Selective functional exhaustion of hematopoietic progenitor cells in the bone marrow of patients with postinfarction heart failure,” Journal of the American College of Cardiology, vol. 49, no. 24, pp. 2341–2349, 2007. View at Publisher · View at Google Scholar · View at Scopus
  131. 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
  132. A. J. Nauta and W. E. Fibbe, “Immunomodulatory properties of mesenchymal stromal cells,” Blood, vol. 110, no. 10, pp. 3499–3506, 2007. View at Publisher · View at Google Scholar · View at Scopus
  133. J. C. Chachques, J. C. Trainini, N. Lago et al., “Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM clinical trial): one year follow-up,” Cell Transplantation, vol. 16, no. 9, pp. 927–934, 2007. View at Publisher · View at Google Scholar · View at Scopus