Table of Contents Author Guidelines Submit a Manuscript
International Journal of Cell Biology
Volume 2009, Article ID 906507, 11 pages
http://dx.doi.org/10.1155/2009/906507
Review Article

Cellular Therapy for Repair of Cardiac Damage after Acute Myocardial Infarction

1Adult Stem Cell Laboratory, Mater Medical Research Institute, South Brisbane, QLD 4101, Australia
2School of Medicine, University of Queensland, St Lucia, QLD 4072, Australia

Received 11 December 2008; Accepted 3 February 2009

Academic Editor: Gary S. Stein

Copyright © 2009 Matthew M. Cook 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. “Cardiovascular diseases,” World Health Organisation (WHO), Geneva, Switzerland, 2007.
  2. N. G. Frangogiannis, “The mechanistic basis of infarct healing,” Antioxidants & Redox Signaling, vol. 8, no. 11-12, pp. 1907–1939, 2006. View at Publisher · View at Google Scholar · View at PubMed
  3. A. Abdel-Latif, R. Bolli, I. M. Tleyjeh et al., “Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis,” Archives of Internal Medicine, vol. 167, no. 10, pp. 989–997, 2007. View at Publisher · View at Google Scholar · View at PubMed
  4. S. Dimmeler, J. Burchfield, A. M. Zeiher et al., “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 PubMed
  5. A. P. Beltrami, L. Barlucchi, D. Torella et al., “Adult cardiac stem cells are multipotent and support myocardial regeneration,” Cell, vol. 114, no. 6, pp. 763–776, 2003. View at Publisher · View at Google Scholar
  6. J. C. Kovacic, D. W. M. Muller, R. Harvey, and R. M. Graham, “Update on the use of stem cells for cardiac disease,” Internal Medicine Journal, vol. 35, no. 6, pp. 348–356, 2005. View at Publisher · View at Google Scholar · View at PubMed
  7. Y. Jiang, B. N. Jahagirdar, R. L. Reinhardt et al., “Pluripotency of mesenchymal stem cells derived from adult marrow,” Nature, vol. 418, no. 6893, pp. 41–49, 2002. View at Publisher · View at Google Scholar · View at PubMed
  8. O. K. Lee, T. K. Kuo, W.-M. Chen, K.-D. Lee, S.-L. Hsieh, and T.-H. Chen, “Isolation of multipotent mesenchymal stem cells from umbilical cord blood,” Blood, vol. 103, no. 5, pp. 1669–1675, 2004. View at Publisher · View at Google Scholar · View at PubMed
  9. A. J. Friedenstein, R. K. Chailakhyan, and U. V. Gerasimov, “Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers,” Cell and Tissue Kinetics, vol. 20, no. 3, pp. 263–272, 1987. View at Google Scholar
  10. 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 Publisher · View at Google Scholar
  11. M. Owen and A. J. Friedenstein, “Stromal stem cells: marrow-derived osteogenic precursors,” in Ccllular and Molecular Biology of Vertebrate Hard Tissues, vol. 136 of Ciba Foundation Symposium, pp. 42–60, 1988. View at Publisher · View at Google Scholar
  12. L. Cheng, P. Qasba, P. Vanguri, and M. A. Thiede, “Human mesenchymal stem cells support megakaryocyte and pro-platelet formation from CD34+ hematopoietic progenitor cells,” Journal of Cellular Physiology, vol. 184, no. 1, pp. 58–69, 2000. View at Publisher · View at Google Scholar
  13. R. J. Deans and A. B. Moseley, “Mesenchymal stem cells: biology and potential clinical uses,” Experimental Hematology, vol. 28, no. 8, pp. 875–884, 2000. View at Publisher · View at Google Scholar
  14. W. A. Noort, A. B. Kruisselbrink, P. S. in't Anker et al., “Mesenchymal stem cells promote engraftment of human umbilical cord blood-derived CD34+ cells in NOD/SCID mice,” Experimental Hematology, vol. 30, no. 8, pp. 870–878, 2002. View at Publisher · View at Google Scholar
  15. Y. Muguruma, T. Yahata, H. Miyatake et al., “Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment,” Blood, vol. 107, no. 5, pp. 1878–1887, 2006. View at Publisher · View at Google Scholar · View at PubMed
  16. S. Barlow, G. Brooke, K. Chatterjee et al., “Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells,” Stem Cells and Development, vol. 17, no. 6, pp. 1095–1107, 2008. View at Publisher · View at Google Scholar · View at PubMed
  17. G. Brooke, T. Rossetti, N. Ilic et al., “Points to consider in designing MSC-based clinical trials,” Transfusion Medicine and Hemotherapy, vol. 35, no. 4, pp. 279–285, 2008. View at Publisher · View at Google Scholar
  18. G. Brooke, T. Rossetti, R. Pelekanos et al., “Manufacturing of human placenta-derived mesenchymal stem cells for clinical trials,” British Journal of Haematology, vol. 144, no. 4, pp. 571–579, 2009. View at Publisher · View at Google Scholar · View at PubMed
  19. G. Brooke, H. Tong, J.-P. Levesque, and K. Atkinson, “Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta,” Stem Cells and Development, vol. 17, no. 5, pp. 929–940, 2008. View at Publisher · View at Google Scholar · View at PubMed
  20. C. Campagnoli, I. A. G. Roberts, S. Kumar, P. R. Bennett, I. Bellantuono, and N. M. Fisk, “Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow,” Blood, vol. 98, no. 8, pp. 2396–2402, 2001. View at Publisher · View at Google Scholar
  21. K. Yoshimura, T. Shigeura, D. Matsumoto et al., “Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates,” Journal of Cellular Physiology, vol. 208, no. 1, pp. 64–76, 2006. View at Publisher · View at Google Scholar · View at PubMed
  22. M. Crisan, S. Yap, L. Casteilla et al., “A perivascular origin for mesenchymal stem cells in multiple human organs,” Cell Stem Cell, vol. 3, no. 3, pp. 301–313, 2008. View at Publisher · View at Google Scholar · View at PubMed
  23. L. da Silva Meirelles, A. I. Caplan, and N. B. Nardi, “In search of the in vivo identity of mesenchymal stem cells,” Stem Cells, vol. 26, no. 9, pp. 2287–2299, 2008. View at Publisher · View at Google Scholar · View at PubMed
  24. P. A. Conget and J. J. Minguell, “Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells,” Journal of Cellular Physiology, vol. 181, no. 1, pp. 67–73, 1999. View at Publisher · View at Google Scholar
  25. 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 PubMed
  26. E. Javazon, J. Tebbets, K. Beggs et al., “Isolation, expansion, and characterization of murine, adult bone marrow derived, mesenchymal stem cells,” Blood, vol. 102, pp. 180B–181B, 2003. View at Google Scholar
  27. A. Peister, J. A. Mellad, B. L. Larson, B. M. Hall, L. F. Gibson, and D. J. Prockop, “Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential,” Blood, vol. 103, no. 5, pp. 1662–1668, 2004. View at Publisher · View at Google Scholar · View at PubMed
  28. 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
  29. P. Bianco, P. G. Robey, and P. J. Simmons, “Mesenchymal stem cells: revisiting history, concepts, and assays,” Cell Stem Cell, vol. 2, no. 4, pp. 313–319, 2008. View at Publisher · View at Google Scholar · View at PubMed
  30. 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 PubMed
  31. D. J. Prockop, “Marrow stromal cells as stem cells for nonhematopoietic tissues,” Science, vol. 276, no. 5309, pp. 71–74, 1997. View at Publisher · View at Google Scholar
  32. B. J. Jones, G. Brooke, K. Atkinson, and S. J. McTaggart, “Immunosuppression by placental indoleamine 2,3-dioxygenase: a role for mesenchymal stem cells,” Placenta, vol. 28, no. 11-12, pp. 1174–1181, 2007. View at Publisher · View at Google Scholar · View at PubMed
  33. O. Ringdén, M. Uzunel, I. Rasmusson et al., “Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease,” Transplantation, vol. 81, no. 10, pp. 1390–1397, 2006. View at Publisher · View at Google Scholar · View at PubMed
  34. K. Le Blanc, “Immunomodulatory effects of fetal and adult mesenchymal stem cells,” Cytotherapy, vol. 5, no. 6, pp. 485–489, 2003. View at Publisher · View at Google Scholar · View at PubMed
  35. G. Brooke, M. Cook, C. Blair et al., “Therapeutic applications of mesenchymal stromal cells,” Seminars in Cell and Developmental Biology, vol. 18, no. 6, pp. 846–858, 2007. View at Publisher · View at Google Scholar · View at PubMed
  36. S. Beyth, Z. Borovsky, D. Mevorach et al., “Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness,” Blood, vol. 105, no. 5, pp. 2214–2219, 2005. View at Publisher · View at Google Scholar · View at PubMed
  37. I. Rasmusson, O. Ringdén, B. Sundberg, and K. Le Blanc, “Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells,” Transplantation, vol. 76, no. 8, pp. 1208–1213, 2003. View at Publisher · View at Google Scholar · View at PubMed
  38. K. Le Blanc, F. Frassoni, L. Ball et al., “Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study,” The Lancet, vol. 371, no. 9624, pp. 1579–1586, 2008. View at Publisher · View at Google Scholar · View at PubMed
  39. K. Le Blanc, I. Rasmusson, B. Sundberg et al., “Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells,” The Lancet, vol. 363, no. 9419, pp. 1439–1441, 2004. View at Publisher · View at Google Scholar · View at PubMed
  40. 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 PubMed
  41. C. Toma, M. F. Pittenger, K. S. Cahill, B. J. Byrne, and P. D. Kessler, “Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart,” Circulation, vol. 105, no. 1, pp. 93–98, 2002. View at Publisher · View at Google Scholar
  42. L.-R. Zhao, W.-M. Duan, M. Reyes, C. D. Keene, C. M. Verfaillie, and W. C. Low, “Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats,” Experimental Neurology, vol. 174, no. 1, pp. 11–20, 2002. View at Publisher · View at Google Scholar · View at PubMed
  43. R. F. Pereira, M. D. O'Hara, A. V. Laptev et al., “Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 3, pp. 1142–1147, 1998. View at Publisher · View at Google Scholar
  44. E. M. Horwitz, P. L. Gordon, W. K. K. Koo et al., “Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 13, pp. 8932–8937, 2002. View at Publisher · View at Google Scholar · View at PubMed
  45. K. Le Blanc, C. Götherström, O. Ringdén et al., “Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta,” Transplantation, vol. 79, no. 11, pp. 1607–1614, 2005. View at Publisher · View at Google Scholar
  46. J. M. Murphy, D. J. Fink, E. B. Hunziker, and F. P. Barry, “Stem cell therapy in a caprine model of osteoarthritis,” Arthritis and Rheumatism, vol. 48, no. 12, pp. 3464–3474, 2003. View at Publisher · View at Google Scholar · View at PubMed
  47. B. Fang, M. Shi, L. Liao, S. Yang, Y. Liu, and R. C. Zhao, “Systemic infusion of FLK1+ mesenchymal stem cells ameliorate carbon tetrachloride-induced liver fibrosis in mice,” Transplantation, vol. 78, no. 1, pp. 83–88, 2004. View at Publisher · View at Google Scholar
  48. M. Kudo, Y. Wang, M. A. Wani, M. Xu, A. Ayub, and M. Ashraf, “Implantation of bone marrow stem cells reduces the infarction and fibrosis in ischemic mouse heart,” Journal of Molecular and Cellular Cardiology, vol. 35, no. 9, pp. 1113–1119, 2003. View at Publisher · View at Google Scholar
  49. R. G. Andrews, E. M. Bryant, S. H. Bartelmez et al., “CD34+ marrow cells, devoid of T and B lymphocytes, reconstitute stable lymphopoiesis and myelopoiesis in lethally irradiated allogeneic baboons,” Blood, vol. 80, no. 7, pp. 1693–1701, 1992. View at Google Scholar
  50. J. L. McKenzie, O. I. Gan, M. Doedens, J. C. Y. Wang, and J. E. Dick, “Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment,” Nature Immunology, vol. 7, no. 11, pp. 1225–1233, 2006. View at Publisher · View at Google Scholar · View at PubMed
  51. F. R. Appelbaum, “The current status of hematopoietic cell transplantation,” Annual Review of Medicine, vol. 54, pp. 491–512, 2003. View at Publisher · View at Google Scholar · View at PubMed
  52. M. Mielcarek and R. Storb, “Non-myeloablative hematopoietic cell transplantation as immunotherapy for hematologic malignancies,” Cancer Treatment Reviews, vol. 29, no. 4, pp. 283–290, 2003. View at Publisher · View at Google Scholar
  53. Y. Okuno, H. Iwasaki, C. S. Huettner et al., “Differential regulation of the human and murine CD34 genes in hematopoietic stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 9, pp. 6246–6251, 2002. View at Publisher · View at Google Scholar · View at PubMed
  54. M. Osawa, K.-I. Hanada, H. Hamada, and H. Nakauchi, “Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell,” Science, vol. 273, no. 5272, pp. 242–245, 1996. View at Publisher · View at Google Scholar
  55. A. W. Wognum, A. C. Eaves, and T. E. Thomas, “Identification and isolation of hematopoietic stem cells,” Archives of Medical Research, vol. 34, no. 6, pp. 461–475, 2003. View at Publisher · View at Google Scholar
  56. A. J. Wagers, R. C. Allsopp, and I. L. Weissman, “Changes in integrin expression are associated with altered homing properties of Lin/loThy1.1loSca-1+c-Kit+ hematopoietic stem cells following mobilization by cyclophosphamide/granulocyte colony-stimulating factor,” Experimental Hematology, vol. 30, no. 2, pp. 176–185, 2002. View at Publisher · View at Google Scholar
  57. M. J. Kiel, O. H. Yilmaz, T. Iwashita, O. H. Yilmaz, C. Terhorst, and S. J. Morrison, “SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells,” Cell, vol. 121, no. 7, pp. 1109–1121, 2005. View at Publisher · View at Google Scholar · View at PubMed
  58. I. Kim, S. He, O. H. Yilmaz, M. J. Kiel, and S. J. Morrison, “Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors,” Blood, vol. 108, no. 2, pp. 737–744, 2006. View at Publisher · View at Google Scholar · View at PubMed
  59. A. Wilson, G. M. Oser, M. Jaworski et al., “Dormant and self-renewing hematopoietic stem cells and their niches,” Annals of the New York Academy of Sciences, vol. 1106, pp. 64–75, 2007. View at Publisher · View at Google Scholar · View at PubMed
  60. I. L. Weissman and J. A. Shizuru, “The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases,” Blood, vol. 112, no. 9, pp. 3543–3553, 2008. View at Publisher · View at Google Scholar · View at PubMed
  61. I. B. Mazo, J.-C. Gutierrez-Ramos, P. S. Frenette, R. O. Hynes, D. D. Wagner, and U. H. von Andrian, “Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1,” Journal of Experimental Medicine, vol. 188, no. 3, pp. 465–474, 1998. View at Publisher · View at Google Scholar
  62. T. Papayannopoulou, “Bone marrow homing: the players, the playfield, and their evolving roles,” Current Opinion in Hematology, vol. 10, no. 3, pp. 214–219, 2003. View at Publisher · View at Google Scholar
  63. I. G. Winkler and J.-P. Lévesque, “Mechanisms of hematopoietic stem cell mobilization: when innate immunity assails the cells that make blood and bone,” Experimental Hematology, vol. 34, no. 8, pp. 996–1009, 2006. View at Publisher · View at Google Scholar · View at PubMed
  64. D. Orlic, J. Kajstura, S. Chimenti et al., “Bone marrow cells regenerate infarcted myocardium,” Nature, vol. 410, no. 6829, pp. 701–705, 2001. View at Publisher · View at Google Scholar · View at PubMed
  65. M. Rota, J. Kajstura, T. Hosoda et al., “Bone marrow cells adopt the cardiomyogenic fate in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 45, pp. 17783–17788, 2007. View at Publisher · View at Google Scholar · View at PubMed
  66. M. Abedi, B. M. Foster, K. D. Wood et al., “Haematopoietic stem cells participate in muscle regeneration,” British Journal of Haematology, vol. 138, no. 6, pp. 792–801, 2007. View at Publisher · View at Google Scholar · View at PubMed
  67. L. B. Balsam, A. J. Wagers, J. L. Christensen, T. Kofidis, I. L. Weissman, and R. C. Robbins, “Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium,” Nature, vol. 428, no. 6983, pp. 668–673, 2004. View at Publisher · View at Google Scholar · View at PubMed
  68. C. E. Murry, M. H. Soonpaa, H. Reinecke et al., “Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts,” Nature, vol. 428, no. 6983, pp. 664–668, 2004. View at Publisher · View at Google Scholar · View at PubMed
  69. D. J. Prockop and S. D. Olson, “Clinical trials with adult stem/progenitor cells for tissue repair: let's not overlook some essential precautions,” Blood, vol. 109, no. 8, pp. 3147–3151, 2007. View at Publisher · View at Google Scholar · View at PubMed
  70. J. L. Spees, S. D. Olson, M. J. Whitney, and D. J. Prockop, “Mitochondrial transfer between cells can rescue aerobic respiration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 5, pp. 1283–1288, 2006. View at Publisher · View at Google Scholar · View at PubMed
  71. 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
  72. A. Jiang, M. Zhang, and Z. Liu, “Angioblasts in adult and its role in ocular disorders due to neovascularization,” Yan Ke Xue Bao, vol. 21, no. 3, pp. 158–162, 2005. View at Google Scholar
  73. N. Werner and G. Nickenig, “Influence of cardiovascular risk factors on endothelial progenitor cells: limitations for therapy?,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 2, pp. 257–266, 2006. View at Publisher · View at Google Scholar · View at PubMed
  74. G. P. Fadini, S. V. de Kreutzenberg, A. Coracina et al., “Circulating CD34+ cells, metabolic syndrome, and cardiovascular risk,” European Heart Journal, vol. 27, no. 18, pp. 2247–2255, 2006. View at Publisher · View at Google Scholar · View at PubMed
  75. J. Hur, C.-H. Yoon, H.-S. Kim et al., “Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 2, pp. 288–293, 2004. View at Publisher · View at Google Scholar · View at PubMed
  76. D. A. Ingram, L. E. Mead, H. Tanaka et al., “Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood,” Blood, vol. 104, no. 9, pp. 2752–2760, 2004. View at Publisher · View at Google Scholar · View at PubMed
  77. M. C. Yoder, L. E. Mead, D. Prater et al., “Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals,” Blood, vol. 109, no. 5, pp. 1801–1809, 2007. View at Publisher · View at Google Scholar · View at PubMed
  78. G. Kania, D. Corbeil, J. Fuchs et al., “Somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors,” Stem Cells, vol. 23, no. 6, pp. 791–804, 2005. View at Publisher · View at Google Scholar · View at PubMed
  79. S. V. Shmelkov, S. Meeus, N. Moussazadeh et al., “Cytokine preconditioning promotes codifferentiation of human fetal liver CD133+ stem cells into angiomyogenic tissue,” Circulation, vol. 111, no. 9, pp. 1175–1183, 2005. View at Publisher · View at Google Scholar · View at PubMed
  80. 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
  81. A. A. Kocher, M. D. Schuster, M. J. Szabolcs et al., “Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function,” Nature Medicine, vol. 7, no. 4, pp. 430–436, 2001. View at Publisher · View at Google Scholar · View at PubMed
  82. D. A. Ingram, N. M. Caplice, and M. C. Yoder, “Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells,” Blood, vol. 106, no. 5, pp. 1525–1531, 2005. View at Publisher · View at Google Scholar · View at PubMed
  83. R. Gulati, D. Jevremovic, T. E. Peterson et al., “Diverse origin and function of cells with endothelial phenotype obtained from adult human blood,” Circulation Research, vol. 93, no. 11, pp. 1023–1025, 2003. View at Publisher · View at Google Scholar · View at PubMed
  84. 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 PubMed
  85. C.-H. Yoon, J. Hur, K.-W. Park et al., “Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases,” Circulation, vol. 112, no. 11, pp. 1618–1627, 2005. View at Publisher · View at Google Scholar · View at PubMed
  86. M. Ishikawa and T. Asahara, “Endothelial progenitor cell culture for vascular regeneration,” Stem Cells and Development, vol. 13, no. 4, pp. 344–349, 2004. View at Publisher · View at Google Scholar
  87. A. Kawamoto, H.-C. Gwon, H. Iwaguro et al., “Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia,” Circulation, vol. 103, no. 5, pp. 634–637, 2001. View at Google Scholar
  88. S. Rafii and D. Lyden, “Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration,” Nature Medicine, vol. 9, no. 6, pp. 702–712, 2003. View at Publisher · View at Google Scholar · View at PubMed
  89. 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 · View at PubMed
  90. P. J. Polverini, R. S. Cotran, M. A. Gimbrone, Jr., and E. R. Unanue, “Activated macrophages induce vascular proliferation,” Nature, vol. 269, no. 5631, pp. 804–806, 1977. View at Publisher · View at Google Scholar
  91. Å. Dahlqvist, E. Y. Umemoto, J. J. Brokaw, M. Dupuis, and D. M. McDonald, “Tissue macrophages associated with angiogenesis in chronic airway inflammation in rats,” American Journal of Respiratory Cell and Molecular Biology, vol. 20, no. 2, pp. 237–247, 1999. View at Google Scholar
  92. L. A. DiPietro and P. J. Polverini, “Angiogenic macrophages produce the angiogenic inhibitor thrombospondin 1,” The American Journal of Pathology, vol. 143, no. 3, pp. 678–684, 1993. View at Google Scholar
  93. E. Elsheikh, M. Uzunel, Z. He, J. Holgersson, G. Nowak, and S. Sumitran-Holgersson, “Only a specific subset of human peripheral-blood monocytes has endothelial-like functional capacity,” Blood, vol. 106, no. 7, pp. 2347–2355, 2005. View at Publisher · View at Google Scholar · View at PubMed
  94. A. K. Tsirogianni, N. M. Moutsopoulos, and H. M. Moutsopoulos, “Wound healing: immunological aspects,” Injury, vol. 37, no. 1, supplement 1, pp. S5–S12, 2006. View at Publisher · View at Google Scholar · View at PubMed
  95. N. G. Frangogiannis, C. W. Smith, and M. L. Entman, “The inflammatory response in myocardial infarction,” Cardiovascular Research, vol. 53, no. 1, pp. 31–47, 2002. View at Publisher · View at Google Scholar
  96. M. De Palma, M. A. Venneri, R. Galli et al., “Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors,” Cancer Cell, vol. 8, no. 3, pp. 211–226, 2005. View at Publisher · View at Google Scholar · View at PubMed
  97. K. G. Peters, C. D. Kontos, P. C. Lin et al., “Functional significance of Tie2 signaling in the adult vasculature,” Recent Progress in Hormone Research, vol. 59, pp. 51–71, 2004. View at Publisher · View at Google Scholar
  98. M. A. Venneri, M. De Palma, M. Ponzoni et al., “Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer,” Blood, vol. 109, no. 12, pp. 5276–5285, 2007. View at Publisher · View at Google Scholar · View at PubMed
  99. C. Murdoch, S. Tazzyman, S. Webster, and C. E. Lewis, “Expression of Tie-2 by human monocytes and their responses to angiopoietin-2,” The Journal of Immunology, vol. 178, no. 11, pp. 7405–7411, 2007. View at Google Scholar
  100. M. Anghelina, P. Krishnan, L. Moldovan, and N. I. Moldovan, “Monocytes and macrophages form branched cell columns in matrigel: implications for a role in neovascularization,” Stem Cells and Development, vol. 13, no. 6, pp. 665–676, 2004. View at Publisher · View at Google Scholar · View at PubMed
  101. M. Anghelina, P. Krishnan, L. Moldovan, and N. I. Moldovan, “Monocytes/macrophages cooperate with progenitor cells during neovascularization and tissue repair: conversion of cell columns into fibrovascular bundles,” The American Journal of Pathology, vol. 168, no. 2, pp. 529–541, 2006. View at Publisher · View at Google Scholar
  102. N. I. Moldovan, P. J. Goldschmidt-Clermont, J. Parker-Thornburg, S. D. Shapiro, and P. E. Kolattukudy, “Contribution of monocytes/macrophages to compensatory neovascularization: the drilling of metalloelastase-positive tunnels in ischemic myocardium,” Circulation Research, vol. 87, no. 5, pp. 378–384, 2000. View at Google Scholar
  103. K. Urbanek, M. Rota, S. Cascapera et al., “Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival,” Circulation Research, vol. 97, no. 7, pp. 663–673, 2005. View at Publisher · View at Google Scholar · View at PubMed
  104. M. A. Laflamme, S. Zbinden, S. E. Epstein, and C. E. Murry, “Cell-based therapy for myocardial ischemia and infarction: pathophysiological mechanisms,” Annual Review of Pathology, vol. 2, pp. 307–339, 2007. View at Publisher · View at Google Scholar · View at PubMed
  105. C. Badorff, R. P. Brandes, R. Popp et al., “Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes,” Circulation, vol. 107, no. 7, pp. 1024–1032, 2003. View at Publisher · View at Google Scholar
  106. A. Deten, H. C. Volz, S. Clamors et al., “Hematopoietic stem cells do not repair the infarcted mouse heart,” Cardiovascular Research, vol. 65, no. 1, pp. 52–63, 2005. View at Publisher · View at Google Scholar · View at PubMed
  107. M. Alvarez-Dolado, R. Pardal, J. M. Garcia-Verdugo et al., “Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes,” Nature, vol. 425, no. 6961, pp. 968–973, 2003. View at Publisher · View at Google Scholar · View at PubMed
  108. J. Endo, M. Sano, J. Fujita et al., “Bone marrow-derived cells are involved in the pathogenesis of cardiac hypertrophy in response to pressure overload,” Circulation, vol. 116, no. 10, pp. 1176–1184, 2007. View at Publisher · View at Google Scholar · View at PubMed
  109. J. M. Nygren, S. Jovinge, M. Breitbach et al., “Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation,” Nature Medicine, vol. 10, no. 5, pp. 494–501, 2004. View at Publisher · View at Google Scholar · View at PubMed
  110. W. Dai, S. L. Hale, and R. A. Kloner, “Role of a paracrine action of mesenchymal stem cells in the improvement of left ventricular function after coronary artery occlusion in rats,” Regenerative Medicine, vol. 2, no. 1, pp. 63–68, 2007. View at Publisher · View at Google Scholar · View at PubMed
  111. 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 PubMed
  112. M. Takahashi, T.-S. Li, R. Suzuki et al., “Cytokines produced by bone marrow cells can contribute to functional improvement of the infarcted heart by protecting cardiomyocytes from ischemic injury,” American Journal of Physiology, vol. 291, no. 2, pp. H886–H893, 2006. View at Publisher · View at Google Scholar · View at PubMed
  113. L. Timmers, S. K. Lim, F. Arslan et al., “Reduction of myocardial infarct size by human mesenchymal stem cell conditioned medium,” Stem Cell Research, vol. 1, no. 2, pp. 129–137, 2007. View at Publisher · View at Google Scholar · View at PubMed
  114. T. Kinnaird, E. Stabile, M. S. Burnett et al., “Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms,” Circulation, vol. 109, no. 12, pp. 1543–1549, 2004. View at Publisher · View at Google Scholar · View at PubMed
  115. M. Heil and W. Schaper, “Influence of mechanical, cellular, and molecular factors on collateral artery growth (Arteriogenesis),” Circulation Research, vol. 95, no. 5, pp. 449–458, 2004. View at Publisher · View at Google Scholar · View at PubMed
  116. B. J. Capoccia, R. M. Shepherd, and D. C. Link, “G-CSF and AMD3100 mobilize monocytes into the blood that stimulate angiogenesis in vivo through a paracrine mechanism,” Blood, vol. 108, no. 7, pp. 2438–2445, 2006. View at Publisher · View at Google Scholar · View at PubMed
  117. A. Kawamoto, T. Tkebuchava, J.-I. Yamaguchi et al., “Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia,” Circulation, vol. 107, no. 3, pp. 461–468, 2003. View at Publisher · View at Google Scholar
  118. R. M. Shepherd, B. J. Capoccia, S. M. Devine et al., “Angiogenic cells can be rapidly mobilized and efficiently harvested from the blood following treatment with AMD3100,” Blood, vol. 108, no. 12, pp. 3662–3667, 2006. View at Publisher · View at Google Scholar · View at PubMed
  119. T. Kobayashi, K. Hamano, T.-S. Li et al., “Enhancement of angiogenesis by the implantation of self bone marrow cells in a rat ischemic heart model,” Journal of Surgical Research, vol. 89, no. 2, pp. 189–195, 2000. View at Publisher · View at Google Scholar · View at PubMed
  120. G. V. Silva, S. Litovsky, J. A. R. Assad et al., “Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model,” Circulation, vol. 111, no. 2, pp. 150–156, 2005. View at Publisher · View at Google Scholar · View at PubMed
  121. T. Ziegelhoeffer, B. Fernandez, S. Kostin et al., “Bone marrow-derived cells do not incorporate into the adult growing vasculature,” Circulation Research, vol. 94, no. 2, pp. 230–238, 2004. View at Publisher · View at Google Scholar · View at PubMed
  122. L. Wang, W. Ma, R. Markovich, J.-W. Chen, and P. H. Wang, “Regulation of cardiomyocyte apoptotic signaling by insulin-like growth factor I,” Circulation Research, vol. 83, no. 5, pp. 516–522, 1998. View at Google Scholar
  123. K. Kitta, R. M. Day, T. Ikeda, and Y. J. Suzuki, “Hepatocyte growth factor protects cardiac myocytes against oxidative stress-induced apoptosis,” Free Radical Biology and Medicine, vol. 31, no. 7, pp. 902–910, 2001. View at Publisher · View at Google Scholar
  124. E. Iwai-Kanai, K. Hasegawa, M. Fujita et al., “Basic fibroblast growth factor protects cardiac myocytes from iNOS-mediated apoptosis,” Journal of Cellular Physiology, vol. 190, no. 1, pp. 54–62, 2002. View at Google Scholar