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Stem Cells International
Volume 2012, Article ID 414038, 13 pages
http://dx.doi.org/10.1155/2012/414038
Research Article

Directed Fusion of Mesenchymal Stem Cells with Cardiomyocytes via VSV-G Facilitates Stem Cell Programming

1Department of Biomedical Engineering, University of Wisconsin at Madison, Madison, WI 53706, USA
2Department of Pathobiological Sciences, University of Wisconsin at Madison, Madison, WI 53711, USA
3Department of Medicine, University of Wisconsin at Madison, Madison, WI 53706, USA
4The Laboratory for Optical and Computational Instrumentation, University of Wisconsin at Madison, Madison, WI 53706, USA
5The Material Sciences Program, University of Wisconsin at Madison, Madison, WI 53706, USA

Received 19 January 2012; Accepted 22 February 2012

Academic Editor: Selim Kuçi

Copyright © 2012 Nicholas A. Kouris 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. S. Tomita, R. K. Li, R. D. Weisel et al., “Autologous transplantation of bone marrow cells improves damaged heart function,” Circulation, vol. 100, no. 19, supplement 2, pp. II247–II256, 1999. View at Google Scholar · View at Scopus
  2. 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
  3. 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
  4. 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
  5. J. G. Shake, P. J. Gruber, W. A. Baumgartner et al., “Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects,” Annals of Thoracic Surgery, vol. 73, no. 6, pp. 1919–1926, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Mouiseddine, S. François, A. Semont et al., “Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model,” British Journal of Radiology, vol. 80, no. 1, pp. S49–S55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Nagaya, T. Fujii, T. Iwase et al., “Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis,” American Journal of Physiology, vol. 287, no. 6, pp. H2670–H2676, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Chen, M. Nayan, M. Duong et al., “Marrow stromal cells for cell-based therapy: the role of antiinflammatory cytokines in cellular cardiomyoplasty,” Annals of Thoracic Surgery, vol. 90, no. 1, pp. 190–197, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Kamihata, H. Matsubara, T. Nishiue et al., “Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines,” Circulation, vol. 104, no. 9, pp. 1046–1052, 2001. View at Google Scholar · View at Scopus
  10. T. Kinnaird, E. Stabile, M. S. Burnett et al., “Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms,” Circulation Research, vol. 94, no. 5, pp. 678–685, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. H. Kawada, J. Fujita, K. Kinjo et al., “Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction,” Blood, vol. 104, no. 12, pp. 3581–3587, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Deb, S. Wang, K. A. Skelding, D. Miller, D. Simper, and N. M. Caplice, “Bone marrow-derived cardiomyocytes are present in adult human heart: a study of gender-mismatched bone marrow transplantation patients,” Circulation, vol. 107, no. 9, pp. 1247–1249, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. 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 Scopus
  14. H. P. Lin, C. Vincenz, K. W. Eliceiri, T. K. Kerppola, and B. M. Ogle, “Bimolecular fluorescence complementation analysis of eukaryotic fusion products,” Biology of the Cell, vol. 102, no. 9, pp. 525–537, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Matsuura, H. Wada, T. Nagai et al., “Cardiomyocytes fuse with surrounding noncardiomyocytes and reenter the cell cycle,” Journal of Cell Biology, vol. 167, no. 2, pp. 351–363, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Oh, S. B. Bradfute, T. D. Gallardo et al., “Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 21, pp. 12313–12318, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Zhang, D. Wang, Z. Estrov et al., “Both cell fusion and transdifferentiation account for the transformation of human peripheral blood CD34-positive cells into cardiomyocytes in vivo,” Circulation, vol. 110, no. 25, pp. 3803–3807, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. C. H. Waddington, The Strategy of Genes, Allen & Unwin, London, 1957.
  19. R. Briggs and T. J. King, “Transplantation of living nuclei from blastula cells into enucleated frogs' eggs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 38, no. 5, pp. 455–463, 1952. View at Google Scholar
  20. I. Wilmut, A. E. Schnieke, J. McWhir, A. J. Kind, and K. H. S. Campbell, “Viable offspring derived from fetal and adult mammalian cells,” Nature, vol. 385, no. 6619, pp. 810–813, 1997. View at Publisher · View at Google Scholar · View at Scopus
  21. N. M. Matveeva, A. G. Shilov, E. M. Kaftanovskaya et al., “In vitro and in vivo study of pluripotency in intraspecific hybrid cells obtained by fusion of murine embryonic stem cells with splenocytes,” Molecular Reproduction and Development, vol. 50, no. 2, pp. 128–138, 1998. View at Google Scholar
  22. J. Yu, M. A. Vodyanik, K. Smuga-Otto et al., “Induced pluripotent stem cell lines derived from human somatic cells,” Science, vol. 318, no. 5858, pp. 1917–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Maherali, R. Sridharan, W. Xie et al., “Directly reprogrammed fibroblasts showglobalepigeneticremodeling andwidespreadtissuecontribution,” Cell Stem Cell, vol. 1, no. 1, pp. 55–70, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Okita, T. Ichisaka, and S. Yamanaka, “Generation of germline-competent induced pluripotent stem cells,” Nature, vol. 448, no. 7151, pp. 313–317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Wernig, A. Meissner, R. Foreman et al., “In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state,” Nature, vol. 448, no. 7151, pp. 318–324, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Huppertz, C. Bartz, and M. Kokozidou, “Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion,” Micron, vol. 37, no. 6, pp. 509–517, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Oren-Suissa and B. Podbilewicz, “Cell fusion during development,” Trends in Cell Biology, vol. 17, no. 11, pp. 537–546, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. U. Zimmermann and J. Vienken, “Electric field-induced cell-to-cell fusion,” Journal of Membrane Biology, vol. 67, no. 3, pp. 165–182, 1982. View at Google Scholar · View at Scopus
  30. H. Schneckenburger, A. Hendinger, R. Sailer et al., “Cell viability in optical tweezers: high power red laser diode versus Nd:YAG laser,” Journal of Biomedical Optics, vol. 5, no. 1, pp. 40–44, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. R. W. Steubing, S. Cheng, W. H. Wright, Y. Numajiri, and M. W. Berns, “Laser induced cell fusion in combination with optical tweezers: the laser cell fusion trap,” Cytometry, vol. 12, no. 6, pp. 505–510, 1991. View at Google Scholar · View at Scopus
  32. A. H. Bartal and Y. Hirshaut, Methods of Hybridoma Formation, vol. 7, Humana Press, 1987.
  33. H. S. Radomska and L. A. Eckhardt, “Mammalian cell fusion in an electroporation device,” Journal of Immunological Methods, vol. 188, no. 2, pp. 209–217, 1995. View at Publisher · View at Google Scholar · View at Scopus
  34. B. R. Lentz and J. Lee, “Poly(ethylene glycol) (PEG)-mediated fusion between pure lipid bilayers: a mechanism in common with viral fusion and secretory vesicle release?” Molecular Membrane Biology, vol. 16, no. 4, pp. 279–296, 1999. View at Google Scholar · View at Scopus
  35. D. M. Eckert and P. S. Kim, “Mechanisms of viral membrane fusion and its inhibition,” Annual Review of Biochemistry, vol. 70, pp. 777–810, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Sapir, O. Avinoam, B. Podbilewicz, and L. V. Chernomordik, “Viral and developmental cell fusion mechanisms: conservation and divergence,” Developmental Cell, vol. 14, no. 1, pp. 11–21, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. E. H. Chen and E. N. Olson, “Unveiling the mechanisms of cell-cell fusion,” Science, vol. 308, no. 5720, pp. 369–373, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Jeetendra, C. S. Robison, L. M. Albritton, and M. A. Whitt, “The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion,” Journal of Virology, vol. 76, no. 23, pp. 12300–12311, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Sun, S. Belouzard, and G. R. Whittaker, “Molecular architecture of the bipartite fusion loops of vesicular stomatitis virus glycoprotein G, a class III viral fusion protein,” Journal of Biological Chemistry, vol. 283, no. 10, pp. 6418–6427, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Dunning, S. Hunter, S. W. H. Kendall, J. Wallis, and W. A. Owens, “Coronary bypass grafting using crossclamp fibrillation does not result in reliable reperfusion of the myocardium when the crossclamp is intermittently released: a prospective cohort study,” Journal of Cardiothoracic Surgery, vol. 1, no. 1, article 45, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. M. L. L. Boumans, J. H. C. Diris, M. Nap et al., “Creatine kinase isoenzyme MB (CKMB) controversy: perimortal tissue acidosis may explain the absence of CKMB in myocardium at autopsy,” Clinical Chemistry, vol. 47, no. 9, pp. 1733–1735, 2001. View at Google Scholar · View at Scopus
  42. R. Lange, R. A. Kloner, and M. Zierler, “Time course of ischemic alterations during normothermic and hypothermic arrest and its reflection by on-line monitoring of tissue pH,” Journal of Thoracic and Cardiovascular Surgery, vol. 86, no. 3, pp. 418–434, 1983. View at Google Scholar · View at Scopus
  43. P. Trivedi and P. Hematti, “Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells,” Experimental Hematology, vol. 36, no. 3, pp. 350–359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. W. C. Claycomb, N. A. Lanson, B. S. Stallworth et al., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 6, pp. 2979–2984, 1998. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Takada, C. Robison, H. Goto et al., “A system for functional analysis of Ebola virus glycoprotein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 26, pp. 14764–14769, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. B. L. Fredericksen and M. A. Whitt, “Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity,” Journal of Virology, vol. 69, no. 3, pp. 1435–1443, 1995. View at Google Scholar · View at Scopus
  47. L. H. Michael, M. L. Entman, C. J. Hartley et al., “Myocardial ischemia and reperfusion: a murine model,” American Journal of Physiology, vol. 269, no. 6, part 6, pp. H2147–H2154, 1995. View at Google Scholar · View at Scopus
  48. N. A. Kouris, J. M. Squirrell, J. P. Jung et al., “A nondenatured, noncrosslinked collagen matrix to deliver stem cells to the heart,” Regenerative Medicine, vol. 6, no. 5, pp. 569–582, 2011. View at Google Scholar
  49. B. M. Ogle, K. A. Butters, T. B. Plummer et al., “Spontaneous fusion of cells between species yields transdifferentiation and retroviral transfer in vivo.,” The FASEB Journal, vol. 18, no. 3, pp. 548–550, 2004. View at Google Scholar · View at Scopus
  50. M. D. Snider and P. W. Robbins, “Transmembrane organization of protein glycosylation. Mature oligosaccharide-lipid is located on the luminal side of microsomes from Chinese hamster ovary cells,” Journal of Biological Chemistry, vol. 257, no. 12, pp. 6796–6801, 1982. View at Google Scholar · View at Scopus
  51. G. Simmons, D. N. Gosalia, A. J. Rennekamp, J. D. Reeves, S. L. Diamond, and P. Bates, “Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 33, pp. 11876–11881, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. F. N. Katz, J. E. Rothman, and V. R. Lingappa, “Membrane assembly in vitro: synthesis, glycosylation, and asymmetric insertion of a transmembrane protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 8, pp. 3278–3282, 1977. View at Google Scholar · View at Scopus
  53. R. Bajpai, J. Lesperance, M. Kim, and A. V. Terskikh, “Efficient propagation of single cells accutase-dissociated human embryonic stem cells,” Molecular Reproduction and Development, vol. 75, no. 5, pp. 818–827, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. F. A. Carneiro, A. S. Ferradosa, and A. T. Da Poian, “Low pH-induced conformational changes in vesicular stomatitis virus glycoprotein involve dramatic structure reorganization,” Journal of Biological Chemistry, vol. 276, no. 1, pp. 62–67, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. M. J. Clague, C. Schoch, L. Zech, and R. Blumenthal, “Gating kinetics of pH-activated membrane fusion of vesicular stomatitis virus with cells: stopped-flow measurements by dequenching of octadecylrhodamine fluorescence,” Biochemistry, vol. 29, no. 5, pp. 1303–1308, 1990. View at Google Scholar · View at Scopus
  56. C. S. Chen, M. Mrksich, S. Huang, G. M. Whitesides, and D. E. Ingber, “Geometric control of cell life and death,” Science, vol. 276, no. 5317, pp. 1425–1428, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Oh, K. S. Brammer, Y. S. J. Li et al., “Stem cell fate dictated solely by altered nanotube dimension,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 7, pp. 2130–2135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. R. McBeath, D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen, “Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment,” Developmental Cell, vol. 6, no. 4, pp. 483–495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. M. A. Laflamme, K. Y. Chen, A. V. Naumova et al., “Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts,” Nature Biotechnology, vol. 25, no. 9, pp. 1015–1024, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. 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 Scopus
  61. N. Noiseux, M. Gnecchi, M. Lopez-Ilasaca et al., “Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation,” Molecular Therapy, vol. 14, no. 6, pp. 840–850, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. 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
  63. B. Balana, C. Nicoletti, I. Zahanich et al., “5-azacytidine induces changes in electrophysiological properties of human mesenchymal stem cells,” Cell Research, vol. 16, no. 12, pp. 949–960, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Wakitani, T. Saito, and A. I. Caplan, “Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine,” Muscle and Nerve, vol. 18, no. 12, pp. 1417–1426, 1995. View at Publisher · View at Google Scholar · View at Scopus
  65. J. A. Santiago, R. Pogemiller, and B. M. Ogle, “Heterogeneous differentiation of human mesenchymal stem cells in response to extended culture in extracellular matrices,” Tissue Engineering A, vol. 15, no. 12, pp. 3911–3922, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Xu, M. Wani, Y. S. Dai et al., “Differentiation of bone marrow stromal cells into the cardiac phenotype requires intercellular communication with myocytes,” Circulation, vol. 110, no. 17, pp. 2658–2665, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. R. Metzele, C. Alt, X. Bai et al., “Human adipose tissue-derived stem cells exhibit proliferation potential and spontaneous rhythmic contraction after fusion with neonatal rat cardiomyocytes,” The FASEB Journal, vol. 25, no. 3, pp. 830–839, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Zhang and D. C. Chan, “New insights into mitochondrial fusion,” FEBS Letters, vol. 581, no. 11, pp. 2168–2173, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Acquistapace, T. Bru, P. F. Lesault et al., “Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer,” Stem Cells, vol. 29, no. 5, pp. 812–824, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. N. Terada, T. Hamazaki, M. Oka et al., “Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion,” Nature, vol. 416, no. 6880, pp. 542–545, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Pomerantz and H. M. Blau, “Nuclear reprogramming: a key to stem cell function in regenerative medicine,” Nature Cell Biology, vol. 6, no. 9, pp. 810–816, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. P. Anversa, A. Leri, and J. Kajstura, “Cardiac Regeneration,” Journal of the American College of Cardiology, vol. 47, no. 9, pp. 1769–1776, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. H. Reinecke, E. Minami, V. Poppa, and C. E. Murry, “Evidence for fusion between cardiac and skeletal muscle cells.,” Circulation Research, vol. 94, no. 6, pp. e56–60, 2004. View at Google Scholar · View at Scopus
  74. D. A. Taylor, B. Z. Atkins, P. Hungspreugs et al., “Regenerating functional myocardium: improved performance after skeletal myoblast transplantation,” Nature Medicine, vol. 4, no. 8, pp. 929–933, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. A. A. Hagège, C. Carrion, P. Menasché et al., “Viability and differentiation of autologous skeletal myoblast grafts in ischaemic cardiomyopathy,” The Lancet, vol. 361, no. 9356, pp. 491–492, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. 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 Scopus
  77. D. K. Singla, T. A. Hacker, L. Ma et al., “Transplantation of embryonic stem cells into the infarcted mouse heart: formation of multiple cell types,” Journal of Molecular and Cellular Cardiology, vol. 40, no. 1, pp. 195–200, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. J. Zhang, G. F. Wilson, A. G. Soerens et al., “Functional cardiomyocytes derived from human induced pluripotent stem cells,” Circulation Research, vol. 104, no. 4, pp. e30–e41, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Ieda, J. D. Fu, P. Delgado-Olguin et al., “Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors,” Cell, vol. 142, no. 3, pp. 375–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Zhang, D. Methot, V. Poppa, Y. Fujio, K. Walsh, and C. E. Murry, “Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies,” Journal of Molecular and Cellular Cardiology, vol. 33, no. 5, pp. 907–921, 2001. View at Publisher · View at Google Scholar · View at Scopus
  81. D. Hou, E. A. S. Youssef, T. J. Brinton et al., “Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials,” Circulation, vol. 112, no. 9, pp. I150–I156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Freyman, G. Polin, H. Osman et al., “A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction,” European Heart Journal, vol. 27, no. 9, pp. 1114–1122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. N. Bursac, Y. Loo, K. Leong, and L. Tung, “Novel anisotropic engineered cardiac tissues: studies of electrical propagation,” Biochemical and Biophysical Research Communications, vol. 361, no. 4, pp. 847–853, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. P. V. Kochupura, E. U. Azeloglu, D. J. Kelly et al., “Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function,” Circulation, vol. 112, no. 9, pp. I144–I149, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Mauney, B. R. Olsen, and V. Volloch, “Matrix remodeling as stem cell recruitment event: a novel in vitro model for homing of human bone marrow stromal cells to the site of injury shows crucial role of extracellular collagen matrix,” Matrix Biology, vol. 29, no. 8, pp. 657–663, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. D. J. Etherington, “Collagen degradation,” Annals of the Rheumatic Diseases, vol. 36, supplement 2, p. 14, 1977. View at Google Scholar
  87. E. B. Flanagan, L. A. Ball, and G. W. Wertz, “Moving the glycoprotein gene of vesicular stomatitis virus to promoter-proximal positions accelerates and enhances the protective immune response,” Journal of Virology, vol. 74, no. 17, pp. 7895–7902, 2000. View at Publisher · View at Google Scholar · View at Scopus
  88. G. Goodman-Snitkoff, R. J. Mannino, and J. J. McSharry, “The glycoprotein isolated from vesicular stomatitis virus is mitogenic for mouse B lymphocytes,” Journal of Experimental Medicine, vol. 153, no. 6, pp. 1489–1502, 1981. View at Google Scholar · View at Scopus
  89. A. F. Ochsenbein, D. D. Pinschewer, B. Odermatt, A. Ciurea, H. Hengartner, and R. M. Zinkernagel, “Correlation of T cell independence of antibody responses with antigen dose reaching secondary lymphoid organs: implications for splenectomized patients and vaccine design,” Journal of Immunology, vol. 164, no. 12, pp. 6296–6302, 2000. View at Google Scholar · View at Scopus
  90. C. Stocking, U. Bergholz, J. Friel et al., “Distinct classes of factor-independent mutants can be isolated after retroviral mutagenesis of a human myeloid stem cell line,” Growth Factors, vol. 8, no. 3, pp. 197–209, 1993. View at Google Scholar · View at Scopus
  91. O. S. Kustikova, A. Wahlers, K. Kühlcke et al., “Dose finding with retroviral vectors: correlation of retroviral vector copy numbers in single cells with gene transfer efficiency in a cell population,” Blood, vol. 102, no. 12, pp. 3934–3937, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. C. C. Shih, J. P. Stoye, and J. M. Coffin, “Highly preferred targets for retrovirus integration,” Cell, vol. 53, no. 4, pp. 531–537, 1988. View at Google Scholar · View at Scopus
  93. Z. Li, J. Düllmann, B. Schiedlmeier et al., “Murine leukemia induced by retroviral gene marking,” Science, vol. 296, no. 5567, p. 497, 2002. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Hacein-Bey-Abina, C. Von Kalle, M. Schmidt et al., “LMO2-Associated Clonal T Cell Proliferation in Two Patients after Gene Therapy for SCID-X1,” Science, vol. 302, no. 5644, pp. 415–419, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Hacein-Bey-Abina, C. Von Kalle, M. Schmidt et al., “A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency,” The New England Journal of Medicine, vol. 348, no. 3, pp. 255–256, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. S. J. Howe, M. R. Mansour, K. Schwarzwaelder et al., “Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients,” Journal of Clinical Investigation, vol. 118, no. 9, pp. 3143–3150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. F. D. Bushman, “Retroviral integration and human gene therapy,” Journal of Clinical Investigation, vol. 117, no. 8, pp. 2083–2086, 2007. View at Publisher · View at Google Scholar · View at Scopus