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Preconditioning and Stem Cell Survival

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Abstract

The harsh ischemic and cytokine-rich microenvironment in the infarcted myocardium, infiltrated by the inflammatory and immune cells, offers a significant challenge to the transplanted donor stem cells. Massive cell death occurs during transplantation as well as following engraftment which significantly lowers the effectiveness of the heart cell therapy. Various approaches have been adopted to overcome this problem nevertheless with multiple limitations with each of these current approaches. Cellular preconditioning and reprogramming by physical, chemical, genetic, and pharmacological manipulation of the cells has shown promise and “prime” the cells to the “state of readiness” to withstand the rigors of lethal ischemia in vitro as well as posttransplantation. This review summarizes the past and present novel approaches of ischemic preconditioning, pharmacological and genetic manipulation using preconditioning mimetics, recombinant growth factor protein treatment, and reprogramming of stem cells to overexpress survival signaling molecules, microRNAs, and trophic factors for intracrine, autocrine, and paracrine effects on cytoprotection.

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References

  1. Abbott, J. D., Huang, Y., et al. (2004). Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation, 110(21), 3300–3305.

    Article  PubMed  Google Scholar 

  2. Abdul Kadir, S. H., Ali, N. N., et al. (2009). Embryonic stem cell-derived cardiomyocytes as a model to study fetal arrhythmia related to maternal disease. Journal of Cellular and Molecular Medicine (in press)

  3. Addya, S., Shiroto, K., et al. (2005). Ischemic preconditioning-mediated cardioprotection is disrupted in heterozygous Flt-1 (VEGFR-1) knockout mice. Journal of Molecular and Cellular Cardiology, 38(2), 345–351.

    Article  PubMed  CAS  Google Scholar 

  4. Afzal, M. R., Haider, K. H., et al. (2009). Preconditioning promotes survival and angiomyogenic potential of mesenchymal stem cells in the infarcted heart via NF-kappaB signaling. Antioxidants & redox signalling (in press)

  5. Ahmad, N., Wang, Y., et al. (2006). Cardiac protection by mitoKATP channels is dependent on Akt translocation from cytosol to mitochondria during late preconditioning. American Journal of Physiology. Heart and Circulatory Physiology, 290(6), H2402–H2408.

    Article  PubMed  CAS  Google Scholar 

  6. Akao, M., Ohler, A., et al. (2001). Mitochondrial ATP-sensitive potassium channels inhibit apoptosis induced by oxidative stress in cardiac cells. Circulation Research, 88(12), 1267–1275.

    Article  PubMed  CAS  Google Scholar 

  7. Akita, T., Murohara, T., et al. (2003). Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization. Laboratory Investigation, 83(1), 65–73.

    PubMed  Google Scholar 

  8. Anversa, P., Leri, A., et al. (2006). Cardiac regeneration. Journal of the American College of Cardiology, 47(9), 1769–1776.

    Article  PubMed  Google Scholar 

  9. Asahara, T., Chen, D., et al. (1998). Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circulation Research, 83(3), 233–240.

    PubMed  CAS  Google Scholar 

  10. Askari, A. T., Unzek, S., et al. (2003). Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet, 362(9385), 697–703.

    Article  PubMed  CAS  Google Scholar 

  11. Azarnoush, K., Maurel, A., et al. (2005). Enhancement of the functional benefits of skeletal myoblast transplantation by means of coadministration of hypoxia-inducible factor 1alpha. Journal of Thoracic and Cardiovascular Surgery, 130(1), 173–179.

    Article  PubMed  CAS  Google Scholar 

  12. Baines, C. P., Pass, J. M., et al. (2001). Protein kinases and kinase-modulated effectors in the late phase of ischemic preconditioning. Basic Research in Cardiology, 96(3), 207–218.

    Article  PubMed  CAS  Google Scholar 

  13. Baldi, A., Abbate, A., et al. (2002). Apoptosis and post-infarction left ventricular remodeling. Journal of Molecular and Cellular Cardiology, 34(2), 165–174.

    Article  PubMed  CAS  Google Scholar 

  14. Bartunek, J., Croissant, J. D., et al. (2007). Pretreatment of adult bone marrow mesenchymal stem cells with cardiomyogenic growth factors and repair of the chronically infarcted myocardium. American Journal of Physiology. Heart and Circulatory Physiology, 292(2), H1095–H1104.

    Article  PubMed  CAS  Google Scholar 

  15. Behfar, A., Perez-Terzic, C., Faustino, R. S., Arrell, D. K., Hodgson, D. M., Yamada, S., et al. (2007). Cardiopoietic programming of embryonic stem cells for tumor-free heart repair. Journal of Experimental Medicine, 204, 405–420.

    Article  PubMed  CAS  Google Scholar 

  16. Bellis, A., Castaldo, D., et al. (2009). Cross-talk between PKA and Akt protects endothelial cells from apoptosis in the late ischemic preconditioning. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(8), 1207–1212.

    Article  PubMed  CAS  Google Scholar 

  17. Bolli, R. (2000). The late phase of preconditioning. Circulation Research, 87(11), 972–983.

    PubMed  CAS  Google Scholar 

  18. Budas, G. R., Churchill, E. N., et al. (2007). Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia–reperfusion injury. Pharmacological Research, 55(6), 523–536.

    Article  PubMed  CAS  Google Scholar 

  19. Busija, D. W., Katakam, P., et al. (2005). Effects of ATP-sensitive potassium channel activators diazoxide and BMS-191095 on membrane potential and reactive oxygen species production in isolated piglet mitochondria. Brain Research Bulletin, 66(2), 85–90.

    Article  PubMed  CAS  Google Scholar 

  20. Camirand, G., Caron, N. J., et al. (2002). Treatment with anti-CD154 antibody and donor-specific transfusion prevents acute rejection of myoblast transplantation. Transplantation, 73(3), 453–461.

    Article  PubMed  CAS  Google Scholar 

  21. Chen, M., Xie, H. Q., et al. (2008). Stromal cell-derived factor-1 promotes bone marrow-derived cells differentiation to cardiomyocyte phenotypes in vitro. Cell Proliferation, 41(2), 336–347.

    Article  PubMed  CAS  Google Scholar 

  22. Crisostomo, P. R., Abarbanell, A. M., et al. (2008). Embryonic stem cells attenuate myocardial dysfunction and inflammation after surgical global ischemia via paracrine actions. American Journal of Physiology. Heart and Circulatory Physiology, 295(4), H1726–H1735.

    Article  PubMed  CAS  Google Scholar 

  23. Crosby, M. E., Kulshreshtha, R., et al. (2009). MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Research, 69(3), 1221–1229.

    Article  PubMed  CAS  Google Scholar 

  24. Das, R., Jahr, H., et al. (2009). The role of hypoxia in MSCs: Considerations for regenerative medicine approaches. Tissue Engineering Part B Reviews (in press)

  25. Dawn, B., Abdel-Latif, A., et al. (2009). Cardiac repair with adult bone marrow-derived cells: The clinical evidence. Antioxidants & Redox Signalling, 11, 1865–1882.

    Article  CAS  Google Scholar 

  26. DeBusk, L. M., Hallahan, D. E., et al. (2004). Akt is a major angiogenic mediator downstream of the Ang1/Tie2 signaling pathway. Experimental Cell Research, 298(1), 167–177.

    Article  PubMed  CAS  Google Scholar 

  27. Devarajan, E., & Huang, S. (2009). STAT3 as a central regulator of tumor metastases. Current Molecular Medicine, 9(5), 626–633.

    Article  PubMed  CAS  Google Scholar 

  28. Dzau, V. J., Gnecchi, M., et al. (2005). Enhancing stem cell therapy through genetic modification. Journal of the American College of Cardiology, 46(7), 1351–1353.

    Article  PubMed  Google Scholar 

  29. Elmadbouh, I., Haider, H., et al. (2007). Ex vivo delivered stromal cell-derived factor-1alpha promotes stem cell homing and induces angiomyogenesis in the infarcted myocardium. Journal of Molecular and Cellular Cardiology, 42(4), 792–803.

    Article  PubMed  CAS  Google Scholar 

  30. Farahmand, P., Lai, T. Y., et al. (2008). Skeletal myoblasts preserve remote matrix architecture and global function when implanted early or late after coronary ligation into infarcted or remote myocardium. Circulation, 118(14 Suppl), S130–S137.

    Article  PubMed  Google Scholar 

  31. Fasanaro, P., D’Alessandra, Y., et al. (2008). MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. Journal of Biological Chemistry, 283(23), 15878–15883.

    Article  PubMed  CAS  Google Scholar 

  32. Gross, G. J., & Auchampach, J. A. (1992). Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circulation Research, 70(2), 223–233.

    PubMed  CAS  Google Scholar 

  33. Haider, H., & Ashraf, M. (2008). Strategies to promote donor cell survival: Combining preconditioning approach with stem cell transplantation. Journal of Molecular and Cellular Cardiology, 45(4), 554–566.

    Article  PubMed  CAS  Google Scholar 

  34. Haider, H., Jiang, S. J., et al. (2004). Effectiveness of transient immunosuppression using cyclosporine for xenomyoblast transplantation for cardiac repair. Transplantation Proceedings, 36(1), 232–235.

    Article  PubMed  CAS  Google Scholar 

  35. Haider, H., Jiang, S., et al. (2008). IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circulation Research, 103(11), 1300–1308.

    Article  PubMed  CAS  Google Scholar 

  36. Haider, H., Tan, A. C., et al. (2004). Myoblast transplantation for cardiac repair: A clinical perspective. Molecular Therapy, 9(1), 14–23.

    Article  PubMed  CAS  Google Scholar 

  37. Hausenloy, D. J., & Yellon, D. M. (2006). Survival kinases in ischemic preconditioning and postconditioning. Cardiovascular Research, 70(2), 240–253.

    Article  PubMed  CAS  Google Scholar 

  38. Heads, R. J., Yellon, D. M., et al. (1995). Differential cytoprotection against heat stress or hypoxia following expression of specific stress protein genes in myogenic cells. Journal of Molecular and Cellular Cardiology, 27(8), 1669–1678.

    Article  PubMed  CAS  Google Scholar 

  39. Hiasa, K., Ishibashi, M., et al. (2004). Gene transfer of stromal cell-derived factor-1alpha enhances ischemic vasculogenesis and angiogenesis via vascular endothelial growth factor/endothelial nitric oxide synthase-related pathway: Next-generation chemokine therapy for therapeutic neovascularization. Circulation, 109(20), 2454–2461.

    Article  PubMed  CAS  Google Scholar 

  40. Hodgetts, S. I., Beilharz, M. W., et al. (2000). Why do cultured transplanted myoblasts die in vivo? DNA quantification shows enhanced survival of donor male myoblasts in host mice depleted of CD4+ and CD8+ cells or Nk1.1+ cells. Cell Transplantation, 9(4), 489–502.

    PubMed  CAS  Google Scholar 

  41. Hodgetts, S. I., & Grounds, M. D. (2001). Complement and myoblast transfer therapy: Donor myoblast survival is enhanced following depletion of host complement C3 using cobra venom factor, but not in the absence of C5. Immunology and Cell Biology, 79(3), 231–239.

    Article  PubMed  CAS  Google Scholar 

  42. Hu, X., Dai, S., et al. (2007). Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: Role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation, 116(6), 654–663.

    Article  PubMed  CAS  Google Scholar 

  43. Hu, X., Yu, S. P., et al. (2008). Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. Journal of Thoracic and Cardiovascular Surgery, 135(4), 799–808.

    Article  PubMed  CAS  Google Scholar 

  44. Huangfu, D., Osafune, K., et al. (2008). Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nature Biotechnology, 26(11), 1269–1275.

    Article  PubMed  CAS  Google Scholar 

  45. Ii, M., Nishimura, H., et al. (2005). Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via “imported” nitric oxide synthase activity. Circulation, 111(9), 1114–1120.

    Article  PubMed  Google Scholar 

  46. Ivan, M., Harris, A. L., et al. (2008). Hypoxia response and microRNAs: No longer two separate worlds. Journal of Cellular and Molecular Medicine, 12(5A), 1426–1431.

    Article  PubMed  CAS  Google Scholar 

  47. Jiang, S., Haider, H., et al. (2006). Supportive interaction between cell survival signaling and angiocompetent factors enhances donor cell survival and promotes angiomyogenesis for cardiac repair. Circulation Research, 99(7), 776–784.

    Article  PubMed  CAS  Google Scholar 

  48. Kamota, T., Li, T. S., et al. (2009). Ischemic pre-conditioning enhances the mobilization and recruitment of bone marrow stem cells to protect against ischemia/reperfusion injury in the late phase. Journal of the American College of Cardiology, 53(19), 1814–1822.

    Article  PubMed  CAS  Google Scholar 

  49. Kanemitsu, N., Tambara, K., et al. (2006). Insulin-like growth factor-1 enhances the efficacy of myoblast transplantation with its multiple functions in the chronic myocardial infarction rat model. Journal of Heart and Lung Transplantation, 25(10), 1253–1262.

    Article  PubMed  Google Scholar 

  50. Kharbanda, R. K., Mortensen, U. M., et al. (2002). Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation, 106(23), 2881–2883.

    Article  PubMed  CAS  Google Scholar 

  51. Khoynezhad, A., Jalali, Z., et al. (2004). Apoptosis: Pathophysiology and therapeutic implications for the cardiac surgeon. Annals of Thoracic Surgery, 78(3), 1109–1118.

    Article  PubMed  Google Scholar 

  52. Kicinska, A., & Szewczyk, A. (2003). Protective effects of the potassium channel opener-diazoxide against injury in neonatal rat ventricular myocytes. General Physiology and Biophysics, 22(3), 383–395.

    PubMed  CAS  Google Scholar 

  53. Kim, H. W., Haider, H. K., et al. (2009). Ischemic preconditioning augments survival of stem cells via MIR-210 expression by targeting caspase-8 associated protein 2. Journal of Biological Chemistry, 284, 33161–33168.

    Article  CAS  Google Scholar 

  54. Kim, I., Kim, H. G., et al. (2000). Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circulation Research, 86(9), 952–959.

    PubMed  CAS  Google Scholar 

  55. Kis, B., Nagy, K., et al. (2004). The mitochondrial K(ATP) channel opener BMS-191095 induces neuronal preconditioning. NeuroReport, 15(2), 345–349.

    Article  PubMed  CAS  Google Scholar 

  56. Kofidis, T., de Bruin, J. L., et al. (2004). Insulin-like growth factor promotes engraftment, differentiation, and functional improvement after transfer of embryonic stem cells for myocardial restoration. Stem Cells, 22(7), 1239–1245.

    Article  PubMed  CAS  Google Scholar 

  57. Koh, G. Y., Klug, M. G., et al. (1993). Differentiation and long-term survival of C2C12 myoblast grafts in heart. Journal of Clinical Investigation, 92(3), 1548–1554.

    Article  PubMed  CAS  Google Scholar 

  58. Koh, G. Y., Soonpaa, M. H., et al. (1993). Long-term survival of AT-1 cardiomyocyte grafts in syngeneic myocardium. American Journal of Physiology, 264(5 Pt 2), H1727–H1733.

    PubMed  CAS  Google Scholar 

  59. Kolossov, E., Bostani, T., et al. (2006). Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infarcted myocardium. Journal of Experimental Medicine, 203(10), 2315–2327.

    Article  PubMed  CAS  Google Scholar 

  60. Konstantinov, I. E., Arab, S., et al. (2005). The remote ischemic preconditioning stimulus modifies gene expression in mouse myocardium. Journal of Thoracic and Cardiovascular Surgery, 130(5), 1326–1332.

    Article  PubMed  CAS  Google Scholar 

  61. Kubo, M., Li, T. S., et al. (2008). Hypoxic preconditioning increases survival and angiogenic potency of peripheral blood mononuclear cells via oxidative stress resistance. American Journal of Physiology. Heart and Circulatory Physiology, 294(2), H590–H595.

    Article  PubMed  CAS  Google Scholar 

  62. Kudo, M., Wang, Y., et al. (2002). Adenosine A(1) receptor mediates late preconditioning via activation of PKC-delta signaling pathway. American Journal of Physiology. Heart and Circulatory Physiology, 283(1), H296–H301.

    PubMed  CAS  Google Scholar 

  63. Kudo, M., Wang, Y., et al. (2003). Implantation of bone marrow stem cells reduces the infarction and fibrosis in ischemic mouse heart. Journal of Molecular and Cellular Cardiology, 35(9), 1113–1119.

    Article  PubMed  CAS  Google Scholar 

  64. Kulshreshtha, R., Davuluri, R. V., et al. (2008). A microRNA component of the hypoxic response. Cell Death and Differentiation, 15(4), 667–671.

    Article  PubMed  CAS  Google Scholar 

  65. Kulshreshtha, R., Ferracin, M., et al. (2007). Regulation of microRNA expression: the hypoxic component. Cell Cycle, 6(12), 1426–1431.

    PubMed  CAS  Google Scholar 

  66. Kutschka, I., Chen, I. Y., et al. (2006). Collagen matrices enhance survival of transplanted cardiomyoblasts and contribute to functional improvement of ischemic rat hearts. Circulation, 114(1 Suppl), I167–I173.

    PubMed  Google Scholar 

  67. Kutschka, I., Kofidis, T., et al. (2006). Adenoviral human BCL-2 transgene expression attenuates early donor cell death after cardiomyoblast transplantation into ischemic rat hearts. Circulation, 114(1 Suppl), I174–I180.

    PubMed  Google Scholar 

  68. Laflamme, M. A., Chen, K. Y., et al. (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nature Biotechnology, 25(9), 1015–1024.

    Article  PubMed  CAS  Google Scholar 

  69. Lataillade, J. J., Domenech, J., et al. (2004). Stromal cell-derived factor-1 (SDF-1)\CXCR4 couple plays multiple roles on haematopoietic progenitors at the border between the old cytokine and new chemokine worlds: Survival, cell cycling and trafficking. European Cytokine Network, 15(3), 177–188.

    PubMed  CAS  Google Scholar 

  70. Li, W., Ma, N., et al. (2007). Bcl-2 engineered MSCs inhibited apoptosis and improved heart function. Stem Cells, 25(8), 2118–2127.

    Article  PubMed  CAS  Google Scholar 

  71. Liu, T. B., Fedak, P. W., et al. (2004). Enhanced IGF-1 expression improves smooth muscle cell engraftment after cell transplantation. American Journal of Physiology. Heart and Circulatory Physiology, 287(6), H2840–H2849.

    Article  PubMed  CAS  Google Scholar 

  72. Logue, S. E., Gustafsson, A. B., et al. (2005). Ischemia/reperfusion injury at the intersection with cell death. Journal of Molecular and Cellular Cardiology, 38(1), 21–33.

    Article  PubMed  CAS  Google Scholar 

  73. Lu, G., Haider, H. K., et al. (2009). Sca-1+ stem cell survival and engraftment in the infarcted heart: Dual role for preconditioning-induced connexin-43. Circulation, 119(19), 2587–2596.

    Article  PubMed  Google Scholar 

  74. Mahboubi, K., Biedermann, B. C., et al. (2000). IL-11 activates human endothelial cells to resist immune-mediated injury. Journal of Immunology, 164(7), 3837–3846.

    CAS  Google Scholar 

  75. Makkar, R. R., Price, M. J., et al. (2005). Intramyocardial injection of allogenic bone marrow-derived mesenchymal stem cells without immunosuppression preserves cardiac function in a porcine model of myocardial infarction. Journal of Cardiovascular Pharmacology Therapy, 10(4), 225–233.

    Article  Google Scholar 

  76. Mangi, A. A., Noiseux, N., et al. (2003). Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nature Medicine, 9(9), 1195–1201.

    Article  PubMed  CAS  Google Scholar 

  77. Matsui, T., Tao, J., et al. (2001). Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation, 104(3), 330–335.

    PubMed  CAS  Google Scholar 

  78. Matsumoto, R., Omura, T., et al. (2005). Vascular endothelial growth factor-expressing mesenchymal stem cell transplantation for the treatment of acute myocardial infarction. Arteriosclerosis, Thrombosis, and Vascular Biology, 25(6), 1168–1173.

    Article  PubMed  CAS  Google Scholar 

  79. Muller-Ehmsen, J., Whittaker, P., et al. (2002). Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. Journal of Molecular and Cellular Cardiology, 34(2), 107–116.

    Article  PubMed  CAS  Google Scholar 

  80. Mummery, C., van der Heyden, M. A., et al. (2007). Cardiomyocytes from human and mouse embryonic stem cells. Methods in Molecular Medicine, 140, 249–272.

    Article  PubMed  CAS  Google Scholar 

  81. Murry, C. E., Jennings, R. B., et al. (1986). Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation, 74(5), 1124–1136.

    PubMed  CAS  Google Scholar 

  82. Nadal-Ginard, B., Anversa, P., et al. (2005). Cardiac stem cells and myocardial regeneration. Novartis Foundation Symposium, 265, 142–154.

    Article  PubMed  Google Scholar 

  83. Nakamura, T., & Schneider, M. D. (2003). The way to a human’s heart is through the stomach: Visceral endoderm-like cells drive human embryonic stem cells to a cardiac fate. Circulation, 107(21), 2638–2639.

    Article  PubMed  Google Scholar 

  84. Nakamura, Y., Yasuda, T., et al. (2006). Enhanced cell transplantation: Preventing apoptosis increases cell survival and ventricular function. American Journal of Physiology. Heart and Circulatory Physiology, 291(2), H939–H947.

    Article  PubMed  CAS  Google Scholar 

  85. Nanduri, J., Yuan, G., et al. (2008). Transcriptional responses to intermittent hypoxia. Respiratory Physiology and Neurobiology, 164(1–2), 277–281.

    Article  PubMed  CAS  Google Scholar 

  86. Nelson, T. J., Martinez-Fernandez, A., Yamada, S., Perez-Terzic, C., Ikeda, Y., & Terzic, A. (2009). Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation, 120(5), 408–416.

    Article  PubMed  Google Scholar 

  87. Niagara, M. I., Haider, H., et al. (2007). Pharmacologically preconditioned skeletal myoblasts are resistant to oxidative stress and promote angiomyogenesis via release of paracrine factors in the infarcted heart. Circulation Research, 100(4), 545–555.

    Article  PubMed  CAS  Google Scholar 

  88. Okita, K., Nakagawa, M., et al. (2008). Generation of mouse induced pluripotent stem cells without viral vectors. Science, 322(5903), 949–953.

    Article  PubMed  CAS  Google Scholar 

  89. O’Sullivan, J. C., Yao, X. L., et al. (2007). Diazoxide, as a postconditioning and delayed preconditioning trigger, increases HSP25 and HSP70 in the central nervous system following combined cerebral stroke and hemorrhagic shock. Journal of Neurotrauma, 24(3), 532–546.

    Article  PubMed  Google Scholar 

  90. Pagani, F. D., DerSimonian, H., et al. (2003). Autologous skeletal myoblasts transplanted to ischemia-damaged myocardium in humans. Histological analysis of cell survival and differentiation. Journal of the American College of Cardiology, 41(5), 879–888.

    Article  PubMed  Google Scholar 

  91. Pasha, Z., Wang, Y., et al. (2008). Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovascular Research, 77(1), 134–142.

    Article  PubMed  CAS  Google Scholar 

  92. Patel, H. H., Gross, E. R., et al. (2005). Sarcolemmal KATP channel triggers delayed ischemic preconditioning in rats. American Journal of Physiology. Heart and Circulatory Physiology, 288(1), H445–H447.

    Article  PubMed  CAS  Google Scholar 

  93. Pillarisetti, K., & Gupta, S. K. (2001). Cloning and relative expression analysis of rat stromal cell derived factor-1 (SDF-1)1: SDF-1 alpha mRNA is selectively induced in rat model of myocardial infarction. Inflammation, 25(5), 293–300.

    Article  PubMed  CAS  Google Scholar 

  94. Qu, Z., Balkir, L., et al. (1998). Development of approaches to improve cell survival in myoblast transfer therapy. Journal of Cell Biology, 142(5), 1257–1267.

    Article  PubMed  CAS  Google Scholar 

  95. Rajapakse, N., Kis, B., et al. (2003). Diazoxide pretreatment induces delayed preconditioning in astrocytes against oxygen glucose deprivation and hydrogen peroxide-induced toxicity. Journal of Neuroscience Research, 73(2), 206–214.

    Article  PubMed  CAS  Google Scholar 

  96. Ravingerova, T., Matejikova, J., et al. (2007). Differential role of PI3K/Akt pathway in the infarct size limitation and antiarrhythmic protection in the rat heart. Molecular and Cellular Biochemistry, 297(1–2), 111–120.

    Article  PubMed  CAS  Google Scholar 

  97. Rosova, I., Dao, M., et al. (2008). Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells, 26(8), 2173–2182.

    Article  PubMed  CAS  Google Scholar 

  98. Rothwarf, D. M., & Karin, M. (1999). The NF-kappa B activation pathway: A paradigm in information transfer from membrane to nucleus. Science’s STKE: Signal Transduction Knowledge Environment, 1999(5), RE1.

    PubMed  CAS  Google Scholar 

  99. Saito, T., Kuang, J. Q., et al. (2002). Xenotransplant cardiac chimera: Immune tolerance of adult stem cells. Annals of Thoracic Surgery, 74(1), 19–24. discussion 24.

    Article  PubMed  Google Scholar 

  100. Sato, T., Li, Y., et al. (2004). Minoxidil opens mitochondrial K(ATP) channels and confers cardioprotection. British Journal of Pharmacology, 141(2), 360–366.

    Article  PubMed  CAS  Google Scholar 

  101. Shimizu, M., Tropak, M., et al. (2009). Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: Evidence suggesting cross-species protection. Clinical Science (London), 117(5), 191–200.

    Article  CAS  Google Scholar 

  102. Shintani, S., Kusano, K., et al. (2006). Synergistic effect of combined intramyocardial CD34+ cells and VEGF2 gene therapy after MI. Nature Clinical Practice. Cardiovascular Medicine, 3(Suppl 1), S123–S128.

    Article  PubMed  CAS  Google Scholar 

  103. Shmelkov, S. V., Meeus, S., et al. (2005). Cytokine preconditioning promotes codifferentiation of human fetal liver CD133+ stem cells into angiomyogenic tissue. Circulation, 111(9), 1175–1183.

    Article  PubMed  CAS  Google Scholar 

  104. Shyu, W. C., Lin, S. Z., et al. (2008). Stromal cell-derived factor-1 alpha promotes neuroprotection, angiogenesis, and mobilization/homing of bone marrow-derived cells in stroke rats. Journal of Pharmacology and Experimental Therapeutics, 324(2), 834–849.

    Article  PubMed  CAS  Google Scholar 

  105. Singla, D. K. (2009). Embryonic stem cells in cardiac repair and regeneration. Antioxidants & Redox Signalling, 11, 1857–1863.

    Article  CAS  Google Scholar 

  106. Sommer, C. A., Stadtfeld, M., et al. (2009). Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells, 27(3), 543–549.

    Article  PubMed  CAS  Google Scholar 

  107. Stein, A. B., Bolli, R., et al. (2007). The late phase of ischemic preconditioning induces a prosurvival genetic program that results in marked attenuation of apoptosis. Journal of Molecular and Cellular Cardiology, 42(6), 1075–1085.

    Article  PubMed  CAS  Google Scholar 

  108. Strauer, B. E., Ott, G., et al. (2009). Bone marrow cells to improve ventricular function. Heart, 95(2), 98–99.

    Article  PubMed  Google Scholar 

  109. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126(4), 663–676.

    Article  PubMed  CAS  Google Scholar 

  110. Takashi, E., Wang, Y., et al. (1999). Activation of mitochondrial K(ATP) channel elicits late preconditioning against myocardial infarction via protein kinase C signaling pathway. Circulation Research, 85(12), 1146–1153.

    PubMed  CAS  Google Scholar 

  111. Tang, Y. L., Zhu, W., et al. (2009). Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circulation Research, 104(10), 1209–1216.

    Article  PubMed  CAS  Google Scholar 

  112. Tateishi, K., Takehara, N., et al. (2008). Stemming heart failure with cardiac- or reprogrammed-stem cells. Journal of Cellular and Molecular Medicine, 12(6A), 2217–2232.

    Article  PubMed  CAS  Google Scholar 

  113. Theus, M. H., Wei, L., et al. (2008). In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Experimental Neurology, 210(2), 656–670.

    Article  PubMed  CAS  Google Scholar 

  114. Toma, C., Pittenger, M. F., et al. (2002). Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation, 105(1), 93–98.

    Article  PubMed  Google Scholar 

  115. Wang, Y., & Ashraf, M. (1999). Role of protein kinase C in mitochondrial KATP channel-mediated protection against Ca2+ overload injury in rat myocardium. Circulation Research, 84(10), 1156–1165.

    PubMed  CAS  Google Scholar 

  116. Wang, Y., Takashi, E., et al. (2001). Downregulation of protein kinase C inhibits activation of mitochondrial K(ATP) channels by diazoxide. Circulation, 104(1), 85–90.

    Article  PubMed  CAS  Google Scholar 

  117. Waxman, A. B., Mahboubi, K., et al. (2003). Interleukin-11 and interleukin-6 protect cultured human endothelial cells from H2O2-induced cell death. American Journal of Respiratory Cell and Molecular Biology, 29(4), 513–522.

    Article  PubMed  CAS  Google Scholar 

  118. Winkler, J., Hescheler, J., et al. (2005). Embryonic stem cells for basic research and potential clinical applications in cardiology. Biochimica et Biophysica Acta, 1740(2), 240–248.

    PubMed  CAS  Google Scholar 

  119. Xu, M., Wang, Y., et al. (2001). Mitochondrial K(ATP) channel activation reduces anoxic injury by restoring mitochondrial membrane potential. American Journal of Physiology. Heart and Circulatory Physiology, 281(3), H1295–H1303.

    PubMed  CAS  Google Scholar 

  120. Yamanaka, S. (2007). Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell, 1(1), 39–49.

    Article  PubMed  CAS  Google Scholar 

  121. Yamaoka, M., Yamaguchi, S., et al. (2000). Apoptosis in rat cardiac myocytes induced by Fas ligand: Priming for Fas-mediated apoptosis with doxorubicin. Journal of Molecular and Cellular Cardiology, 32(6), 881–889.

    Article  PubMed  CAS  Google Scholar 

  122. Yao, K., Huang, R., et al. (2008). Administration of intracoronary bone marrow mononuclear cells on chronic myocardial infarction improves diastolic function. Heart, 94(9), 1147–1153.

    Article  PubMed  CAS  Google Scholar 

  123. Yau, T. M., Kim, C., et al. (2005). Increasing transplanted cell survival with cell-based angiogenic gene therapy. Annals of Thoracic Surgery, 80(5), 1779–1786.

    Article  PubMed  Google Scholar 

  124. Yu, H. M., Zhi, J. L., et al. (2006). Role of the JAK–STAT pathway in protection of hydrogen peroxide preconditioning against apoptosis induced by oxidative stress in PC12 cells. Apoptosis, 11(6), 931–941.

    Article  PubMed  CAS  Google Scholar 

  125. Yuan, G., Nanduri, J., et al. (2008). Induction of HIF-1alpha expression by intermittent hypoxia: involvement of NADPH oxidase, Ca2+ signaling, prolyl hydroxylases, and mTOR. Journal of Cellular Physiology, 217(3), 674–685.

    Article  PubMed  CAS  Google Scholar 

  126. Zemani, F., Silvestre, J. S., et al. (2008). Ex vivo priming of endothelial progenitor cells with SDF-1 before transplantation could increase their proangiogenic potential. Arteriosclerosis, Thrombosis, and Vascular Biology, 28(4), 644–650.

    Article  PubMed  CAS  Google Scholar 

  127. Zhao, Z. Q., & Vinten-Johansen, J. (2006). Postconditioning: Reduction of reperfusion-induced injury. Cardiovascular Research, 70(2), 200–211.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Institutes of Health grants # R37-HL074272, HL-23597, HL70062, and HL-080686 (to M.A.) and HL-087288 and HL-089535 (Kh.H.H).

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  1. Department of Pathology and Laboratory Medicine, University of Cincinnati, 231-Albert, Sabin Way, OH, 45267-0529, USA

    Husnain Kh Haider & Muhammad Ashraf

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  1. Husnain Kh Haider
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Correspondence to Husnain Kh Haider.

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Haider, H.K., Ashraf, M. Preconditioning and Stem Cell Survival. J. of Cardiovasc. Trans. Res. 3, 89–102 (2010). https://doi.org/10.1007/s12265-009-9161-2

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