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Natural ECM as Biomaterial for Scaffold Based Cardiac Regeneration Using Adult Bone Marrow Derived Stem Cells

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Abstract

Cellular therapy using stem cells for cardiac diseases has recently gained much interest in the scientific community due to its potential in regenerating damaged and even dead tissue and thereby restoring the organ function. Stem cells from various sources and origin are being currently used for regeneration studies directly or along with differentiation inducing agents. Long term survival and minimal side effects can be attained by using autologous cells and reduced use of inducing agents. Cardiomyogenic differentiation of adult derived stem cells has been previously reported using various inducing agents but the use of a potentially harmful DNA demethylating agent 5-azacytidine (5-azaC) has been found to be critical in almost all studies. Alternate inducing factors and conditions/stimulant like physical condition including electrical stimulation, chemical inducers and biological agents have been attempted by numerous groups to induce cardiac differentiation. Biomaterials were initially used as artificial scaffold in in vitro studies and later as a delivery vehicle. Natural ECM is the ideal biological scaffold since it contains all the components of the tissue from which it was derived except for the living cells. Constructive remodeling can be performed using such natural ECM scaffolds and stem cells since, the cells can be delivered to the site of infraction and once delivered the cells adhere and are not “lost”. Due to the niche like conditions of ECM, stem cells tend to differentiate into tissue specific cells and attain several characteristics similar to that of functional cells even in absence of any directed differentiation using external inducers. The development of niche mimicking biomaterials and hybrid biomaterial can further advance directed differentiation without specific induction. The mechanical and electrical integration of these materials to the functional tissue is a problem to be addressed. The search for the perfect extracellular matrix for therapeutic applications including engineering cardiac tissue structures for post ischemic cardiac tissue regeneration continues.

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Abbreviations

BMSC:

Bone marrow derived stem cells

5azaC:

5-azacytidine

References

  1. Braunwald, E., & Bristow, M. R. (2000). Congestive heart failure: fifty years of progress. Circulation, 102, IV-14–IV-23.

    Article  CAS  Google Scholar 

  2. American Heart Association. (1999). Heart and stroke statistical update. Dallas: American Heart Association.

    Google Scholar 

  3. Lloyd-Jones, D., Adams, R. J., Brown, T. M., et al. (2010). Heart disease and stroke statistics—2010 update. Circulation, 121, e46–e215.

    Article  PubMed  Google Scholar 

  4. Roger, V. L., Go, A. S., Lloyd-Jones, D. M., et al. (2012). Heart disease and stroke statistics-2012 update. Circulation, 125, e2–e220.

    Article  PubMed  Google Scholar 

  5. Orlic, D., Hill, J. M., & Arai, A. E. (2002). Stem cells for myocardial regeneration. Circulation Research, 91, 1092–1102.

    Article  PubMed  CAS  Google Scholar 

  6. Caplice, N. M. (2006). The future of cell therapy for acute myocardial infarction. Nature Clinical Practice. Cardiovascular Medicine, 3, S129–S132.

    Article  PubMed  CAS  Google Scholar 

  7. National Institutes of Health. (2006). Regenerative medicine. NIH Fact Sheet 092106.

  8. Mason, C., & Dunnill, P. (2008). A brief definition of regenerative medicine. Regenerative Medicine, 3, 1–5.

    Article  PubMed  Google Scholar 

  9. Mason, C., & Manzotti, E. (2010). Regenerative medicine cell therapies: numbers of units manufactured and patients treated between 1988 and 2010. Regenerative Medicine, 5, 307–313.

    Article  PubMed  Google Scholar 

  10. Langer, R., & Vacanti, J. P. (1993). Tissue engineering. Science, 260, 920–926.

    Article  PubMed  CAS  Google Scholar 

  11. Lanza, R. P., Langer, R., & Vacanti, J. P. (2000). Principles of tissue engineering. New York: Academic.

    Google Scholar 

  12. MacArthur, B. D., & Oreffo, R. O. C. (2005). Bridging the gap. Nature 433:19-.

    Google Scholar 

  13. Wu, K. H., Liu, Y. L., Zhou, B., & Han, Z. C. (2006). Cellular therapy and myocardial tissue engineering: the role of adult stem and progenitor cells. European Journal of Cardiothoracic Surgery, 30, 770–781.

    Article  PubMed  Google Scholar 

  14. O’Brien, T., & Barry, F. P. (2009). Stem cell therapy and regenerative medicine. Mayo Clinic Proceedings, 84, 859–861.

    Article  PubMed  Google Scholar 

  15. Gersh, B. J., Simari, R. D., Behfar, A., Terzic, C. M., & Terzic, A. (2009). Cardiac cell repair therapy: a clinical perspective. Mayo Clinic Proceedings, 84, 876–892.

    Article  PubMed  CAS  Google Scholar 

  16. Laflamme, M. A., & Murry, C. E. (2005). Regenerating the heart. Nature Biotechnology, 23, 845–856.

    Article  PubMed  CAS  Google Scholar 

  17. Yacoub, M., Suzuki, K., & Rosenthal, N. (2006). The future of regenerative therapy in patients with chronic heart failure. Nature Clinical Practice. Cardiovascular Medicine, 3, S133–S135.

    Article  PubMed  Google Scholar 

  18. Ptaszek, L. M., Mansour, M., Ruskin, J. N., & Chien, K. R. (2012). Towards regenerative therapy for cardiac disease. The Lancet, 379, 933–942.

    Article  Google Scholar 

  19. Traverse, J. (2012). Using biomaterials to improve the efficacy of cell therapy following acute myocardial infarction. Journal of Cardiovascular Translational Research, 5, 67–72.

    Article  PubMed  Google Scholar 

  20. Laflamme, M. A., & Murry, C. E. (2011). Heart regeneration. Nature, 473, 326–335.

    Article  PubMed  CAS  Google Scholar 

  21. Sánchez, P. L., Román, J. A. S., Villa, A., Eugenia, F. M., & Fernández-Avilés, F. (2006). Contemplating the bright future of stem cell therapy for cardiovascular disease. Nature Clinical Practice. Cardiovascular Medicine, 3, S133.

    Article  Google Scholar 

  22. Christman, K. L., & Lee, R. J. (2006). Biomaterials for the treatment of myocardial infarction. Journal of the American College of Cardiology, 48, 907–913.

    Article  PubMed  CAS  Google Scholar 

  23. Chen, Q.-Z., Harding, S. E., Ali, N. N., Lyon, A. R., & Boccaccini, A. R. (2008). Biomaterials in cardiac tissue engineering: ten years of research survey. Materials Science and Engineering: R: Reports, 59, 1–37.

    Article  CAS  Google Scholar 

  24. Murry, C. E., Reinecke, H., & Pabon, L. M. (2006). Regeneration gaps: observations on stem cells and cardiac repair. Journal of the American College of Cardiology, 47, 1777–1785.

    Article  PubMed  Google Scholar 

  25. van Laake, L. W., Hassink, R., Doevendans, P. A., & Mummery, C. (2006). Heart repair and stem cells. The Journal of Physiology, 577, 467–478.

    Article  PubMed  CAS  Google Scholar 

  26. Reinecke, H., Minami, E., Zhu, W.-Z., & Laflamme, M. A. (2008). Cardiogenic differentiation and transdifferentiation of progenitor cells. Circulation Research, 103, 1058–1071.

    Article  PubMed  CAS  Google Scholar 

  27. van Laake, L. W., van Hoof, D., & Mummery, C. L. (2005). Cardiomyocytes derived from stem cells. Annals of Medicine, 37, 499–512.

    Article  PubMed  CAS  Google Scholar 

  28. Jones, D. A., Choudry, F., & Mathur, A. (2012). Cell therapy in cardiovascular disease: the national society journals present selected research that has driven recent advances in clinical cardiology. Heart, 98, 1626–1631.

    Article  PubMed  CAS  Google Scholar 

  29. Chavakis, E., Koyanagi, M., & Dimmeler, S. (2010). Enhancing the outcome of cell therapy for cardiac repair. Circulation, 121, 325–335.

    Article  PubMed  Google Scholar 

  30. Jeevanantham, V., Butler, M., Saad, A., Abdel-Latif, A., Zuba-Surma, E. K., & Dawn, B. (2012). Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters / clinical perspective. Circulation, 126, 551–568.

    Article  PubMed  Google Scholar 

  31. van der Spoel, T. I. G., Jansen of Lorkeers, S. J., & Agostoni, P. (2011). Human relevance of pre-clinical studies in stem cell therapy: systematic review and meta-analysis of large animal models of ischaemic heart disease. Cardiovascular Research, 91, 649–658.

    Article  PubMed  CAS  Google Scholar 

  32. Giraud, M.-N., Guex, A. G., & Tevaearai, H. T. (2012). Cell therapies for heart function recovery: focus on myocardial tissue engineering and nanotechnologies. Cardiology Research and Practice, 2012, 10.

    Article  Google Scholar 

  33. Meyer, G. P., Wollert, K. C., Lotz, J., et al. (2009). Intracoronary bone marrow cell transfer after myocardial infarction: five-year follow-up from the randomized-controlled BOOST trial. European Heart Journal, 30, 2978–2984.

    Article  PubMed  Google Scholar 

  34. Yousef, M., Schannwell, C. M., Köstering, M., Zeus, T., Brehm, M., & Strauer, B. E. (2009). The BALANCE study clinical benefit and long-term outcome after intracoronary autologous bone marrow cell transplantation in patients with acute myocardial infarction. Journal of the American College of Cardiology, 53, 2262–2269.

    Article  PubMed  Google Scholar 

  35. Segers, V. F. M., & Lee, R. T. (2008). Stem-cell therapy for cardiac disease. Nature, 451, 937–942.

    Article  PubMed  CAS  Google Scholar 

  36. Dimarakis, I., Habib, N. A., & Gordon, M. Y. A. (2005). Adult bone marrow-derived stem cells and the injured heart: just the beginning? European Journal of Cardiothoracic Surgery, 28, 665–676.

    Article  PubMed  Google Scholar 

  37. Beltrami, A. P., Barlucchi, L., Torella, D., et al. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell, 114, 763–776.

    Article  PubMed  CAS  Google Scholar 

  38. Oh, H., Bradfute, S. B., Gallardo, T. D., et al. (2003). 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, 100, 12313–12318.

    Article  PubMed  CAS  Google Scholar 

  39. Narmoneva, D. A., Vukmirovic, R., Davis, M. E., Kamm, R. D., & Lee, R. T. (2004). Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration. Circulation, 110, 962–968.

    Article  PubMed  Google Scholar 

  40. Rubart, M., & Field, L. J. (2006). Cardiac regeneration: repopulating the heart. Annual Review of Physiology, 68, 29–49.

    Article  PubMed  CAS  Google Scholar 

  41. Young, P. P., Vaughan, D. E., & Hatzopoulos, A. K. (2007). Biologic properties of endothelial progenitor cells and their potential for cell therapy. Progress in Cardiovascular Diseases, 49, 421–429.

    Article  PubMed  CAS  Google Scholar 

  42. Léobon, B., Garcin, I., Menasché, P., Vilquin, J.-T., Audinat, E., & Charpak, S. (2003). Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proceedings of the National Academy of Sciences of the United States of America, 100, 7808–7811.

    Article  PubMed  CAS  Google Scholar 

  43. Reinecke, H., Minami, E., Poppa, V., & Murry, C. E. (2004). Evidence for fusion between cardiac and skeletal muscle cells. Circulation Research, 94, e56–e60.

    Article  PubMed  CAS  Google Scholar 

  44. Menasché, P. (2007). Skeletal myoblasts as a therapeutic agent. Progress in Cardiovascular Diseases, 50, 7–17.

    Article  PubMed  Google Scholar 

  45. Bettiol, E., Clement, S., Krause, K. H., & Jaconi, M. E. (2007). Embryonic and adult stem cell-derived cardiomyocytes: lessons from in vitro models. In K. Kramer, O. Krayer, E. Lehnartz, A. V. Muralt, & H. H. Weber (Eds.), Reviews of physiology biochemistry and pharmacology (pp. 1–30). Heidelberg: Springer Berlin.

    Google Scholar 

  46. van Laake, L. W., Passier, R., Doevendans, P. A., & Mummery, C. L. (2008). Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circulation Research, 102, 1008–1010.

    Article  PubMed  CAS  Google Scholar 

  47. McLaren, A. (2001). Ethical and social considerations of stem cell research. Nature, 414, 129–131.

    Article  PubMed  CAS  Google Scholar 

  48. Zwi, L., Caspi, O., Arbel, G., et al. (2009). Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation, 120, 1513–1523.

    Article  PubMed  CAS  Google Scholar 

  49. Bianco, P., Riminucci, M., Gronthos, S., & Robey, P. G. (2001). Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells, 19, 180–192.

    Article  PubMed  CAS  Google Scholar 

  50. Phinney, D. G., & Prockop, D. J. (2007). Concise review: Mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—Current views. Stem Cells, 25, 2896–2902.

    Article  PubMed  Google Scholar 

  51. Pittenger, M. F., Mackay, A. M., Beck, S. C., et al. (1999). Multilineage potential of adult mesenchymal stem cells. Science, 284, 143–147.

    Article  PubMed  CAS  Google Scholar 

  52. Krause, D. S., Theise, N. D., Collector, M. I., et al. (2001). Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell, 105, 369–377.

    Article  PubMed  CAS  Google Scholar 

  53. Jiang, Y., Jahagirdar, B. N., Reinhardt, R. L., et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature, 418, 41–49.

    Article  PubMed  CAS  Google Scholar 

  54. Körbling, M., & Estrov, Z. (2003). Adult stem cells for tissue repair—a new therapeutic concept? The New England Journal of Medicine, 349, 570–582.

    Article  PubMed  Google Scholar 

  55. Kocher, A. A., Schuster, M. D., Szabolcs, M. J., et al. (2001). Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nature Medicine, 7, 430–436.

    Article  PubMed  CAS  Google Scholar 

  56. Wang, J. S., Shum-Tim, D., Chedrawy, E., & Chiu, R. C. J. (2001). The coronary delivery of marrow stromal cells for myocardial regeneration: Pathophysiologic and therapeutic implications. The Journal of Thoracic and Cardiovascular Surgery, 122, 699–705.

    Article  PubMed  CAS  Google Scholar 

  57. Kajstura, J., Rota, M., Whang, B., et al. (2005). Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circulation Research, 96, 127–137.

    Article  PubMed  CAS  Google Scholar 

  58. Antonitsis, P., Ioannidou-Papagiannaki, E., Kaidoglou, A., & Papakonstantinou, C. (2007). In vitro cardiomyogenic differentiation of adult human bone marrow mesenchymal stem cells. The role of 5-azacytidine. Interactive Cardiovascular and Thoracic Surgery, 6, 593–597.

    Article  PubMed  Google Scholar 

  59. Maulik, N., & Thirunavukkarasu, M. (2008). Growth factor/s and cell therapy in myocardial regeneration. Journal of Molecular and Cellular Cardiology, 44, 219–227.

    Article  PubMed  CAS  Google Scholar 

  60. Zipori, D. (2005). The stem state: plasticity is essential, whereas self-renewal and hierarchy are optional. Stem Cells, 23, 719–726.

    Article  PubMed  CAS  Google Scholar 

  61. Fukuda, K. (2001). Development of regenerative cardiomyocytes from mesenchymal stem cells for cardiovascular tissue engineering. Artificial Organs, 25, 187–193.

    Article  PubMed  CAS  Google Scholar 

  62. Xu, W., Zhang, X., Qian, H., et al. (2004). Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Experimental Biology and Medicine, 229, 623–631.

    PubMed  CAS  Google Scholar 

  63. Rangappa, S., Fen, C., Lee, E. H., Bongso, A., & Wei, E. S. K. (2003). Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. The Annals of Thoracic Surgery, 75, 775–779.

    Article  PubMed  Google Scholar 

  64. Planat-Benard, V., Menard, C., Andre, M., et al. (2004). Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circulation Research, 94, 223–229.

    Article  PubMed  CAS  Google Scholar 

  65. Wei-xin, L., Jian, S., Yu, W., et al. (2004). A microenvironment, rather than chemical, initiates the cardiomyogenic differentiation of marrow stromal cells. Journal of Wuhan University (Natural sciences edition), 9, 513–521.

    Article  Google Scholar 

  66. Nygren, J. M., Jovinge, S., Breitbach, M., et al. (2004). Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nature Medicine, 10, 494–501.

    Article  PubMed  CAS  Google Scholar 

  67. Terada, N., Hamazaki, T., Oka, M., et al. (2002). Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature, 416, 542–545.

    Article  PubMed  CAS  Google Scholar 

  68. Matsuura, K., Wada, H., Nagai, T., et al. (2004). Cardiomyocytes fuse with surrounding noncardiomyocytes and reenter the cell cycle. The Journal of Cell Biology, 167, 351–363.

    Article  PubMed  CAS  Google Scholar 

  69. Balsam, L. B., Wagers, A. J., Christensen, J. L., Kofidis, T., Weissman, I. L., & Robbins, R. C. (2004). Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature, 428, 668–673.

    Article  PubMed  CAS  Google Scholar 

  70. Murry, C. E., Soonpaa, M. H., Reinecke, H., et al. (2004). Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature, 428, 664–668.

    Article  PubMed  CAS  Google Scholar 

  71. Makino, S., Fukuda, K., Miyoshi, S., et al. (1999). Cardiomyocytes can be generated from marrow stromal cells in vitro. The Journal of Clinical Investigation, 103, 697–705.

    Article  PubMed  CAS  Google Scholar 

  72. Fukuda, K. (2003). Use of adult marrow mesenchymal stem cells for regeneration of cardiomyocytes. Bone Marrow Transplantation, 32, S25–S27.

    Article  PubMed  CAS  Google Scholar 

  73. Čihák, A. (1974). Biological effects of 5-azacytidine in eukaryotes. Oncology, 30, 405–422.

    Article  PubMed  Google Scholar 

  74. Konieczny, S. F., & Emerson, C. P. (1984). 5-azacytidine induction of stable mesodermal stem cell lineages from 10 T1/2 cells: Evidence for regulatory genes controlling determination. Cell, 38, 791–800.

    Article  PubMed  CAS  Google Scholar 

  75. Rosca, A. M., & Burlacu, A. (2011). The effect of 5-azacytidine: evidence for alteration of the multipotent ability of mesenchymal stem cells. Stem Cells and Development, 20, 1213–1221.

    Article  PubMed  CAS  Google Scholar 

  76. van der Heyden, M. A. G., & Defize, L. H. K. (2003). Twenty one years of P19 cells: what an embryonal carcinoma cell line taught us about cardiomyocyte differentiation. Cardiovascular Research, 58, 292–302.

    Article  PubMed  CAS  Google Scholar 

  77. Wong, S. S., & Bernstein, H. S. (2010). Cardiac regeneration using human embryonic stem cells: producing cells for future therapy. Regenerative Medicine, 5, 763–775.

    Article  PubMed  Google Scholar 

  78. Kraehenbuehl, T. P., Zammaretti, P., Van der Vlies, A. J., et al. (2008). Three-dimensional extracellular matrix-directed cardioprogenitor differentiation: systematic modulation of a synthetic cell-responsive PEG-hydrogel. Biomaterials, 29, 2757–2766.

    Article  PubMed  CAS  Google Scholar 

  79. Heng, B. C., Haider, H. K., Sim, E. K.-W., Cao, T., & Ng, S. C. (2004). Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovascular Research, 62, 34–42.

    Article  PubMed  CAS  Google Scholar 

  80. Tathe, A., Ghodke, M., & Nikalje, A. P. (2010). A brief review: biomaterials and their application. International Journal of Pharmacy and Pharmaceutical Sciences, 2, 19–23.

    CAS  Google Scholar 

  81. Wang, F., & Guan, J. (2010). Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Advanced Drug Delivery Reviews, 62, 784–797.

    Article  PubMed  CAS  Google Scholar 

  82. Davis, R. L., Weintraub, H., & Lassar, A. B. (1987). Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell, 51, 987–1000.

    Article  PubMed  CAS  Google Scholar 

  83. Huang, N. F., Yu, J., Sievers, R., Li, S., & Lee, R. J. (2005). Injectable biopolymers enhance angiogenesis after myocardial infarction. Tissue Engineering, 11, 1860–1866.

    Article  PubMed  CAS  Google Scholar 

  84. Chai, C., & Leong, K. W. (2007). Biomaterials approach to expand and direct differentiation of stem cells. Molecular Therapy, 15, 467–480.

    Article  PubMed  CAS  Google Scholar 

  85. Langer, R., & Tirrell, D. A. (2004). Designing materials for biology and medicine. Nature, 428, 487–492.

    Article  PubMed  CAS  Google Scholar 

  86. Leor, J., Amsalem, Y., & Cohen, S. (2005). Cells, scaffolds, and molecules for myocardial tissue engineering. Pharmacology and Therapeutics, 105, 151–163.

    Article  PubMed  CAS  Google Scholar 

  87. Bartunek, J., Sherman, W., Vanderheyden, M., Fernandez-Aviles, F., Wijns, W., & Terzic, A. (2009). Delivery of biologics in cardiovascular regenerative medicine. Clinical Pharmacology and Therapeutics, 85, 548–552.

    Article  PubMed  CAS  Google Scholar 

  88. Kang, H. J., & Kim, H. S. (2008). Safety and efficacy of intracoronary infusion of mobilized peripheral blood stem cell in patients with myocardial infarction: MAGIC Cell-1 and MAGIC Cell-3-DES-trials. European Heart Journal Supplements, 10, K39–K43.

    Article  CAS  Google Scholar 

  89. Wollert, K. C., & Drexler, H. (2005). Clinical applications of stem cells for the heart. Circulation Research, 96, 151–163.

    Article  PubMed  CAS  Google Scholar 

  90. Papadaki, M., Bursac, N., Langer, R., Merok, J., Vunjak-Novakovic, G., & Freed, L. E. (2001). Tissue engineering of functional cardiac muscle: molecular, structural, and electrophysiological studies. American Journal of Physiology - Heart and Circulatory Physiology, 280, H168–H178.

    PubMed  CAS  Google Scholar 

  91. Radisic, M., Park, H., Shing, H., et al. (2004). Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proceedings of the National Academy of Sciences of the United States of America, 101, 18129–18134.

    Article  PubMed  CAS  Google Scholar 

  92. Yang, J., Yamato, M., & Okano, T. (2005). Cell-sheet engineering using intelligent surfaces. MRS Bulletin, 30, 189–193.

    Article  CAS  Google Scholar 

  93. Eschenhagen, T., Fink, C., Remmers, U., et al. (1997). Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. The FASEB Journal, 11, 683–694.

    CAS  Google Scholar 

  94. Fujimoto, K. L., Tobita, K., Merryman, W. D., et al. (2007). An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. Journal of the American College of Cardiology, 49, 2292–2300.

    Article  PubMed  CAS  Google Scholar 

  95. Wall, S. T., Walker, J. C., Healy, K. E., Ratcliffe, M. B., & Guccione, J. M. (2006). Theoretical impact of the injection of material into the myocardium: a finite element model simulation. Circulation, 114, 2627–2635.

    Article  PubMed  Google Scholar 

  96. Robert, P. L., Robert, L., & Joseph, V. (Eds.). (2000). Principles of tissue engineering (2nd ed.). San Diego: Academic.

    Google Scholar 

  97. Giraud, M.-N., Armbruster, C., Carrel, T., & Tevaearai, H. T. (2007). Current state of the art in myocardial tissue engineering. Tissue Engineering, 13, 1825–1836.

    Article  PubMed  Google Scholar 

  98. Wei, H. J., Chen, C. H., Lee, W. Y., et al. (2008). Bioengineered cardiac patch constructed from multilayered mesenchymal stem cells for myocardial repair. Biomaterials, 29, 3547–3556.

    Article  PubMed  CAS  Google Scholar 

  99. Schmidt, D., & Hoerstrup, S. P. (2006). Tissue engineered heart valves based on human cells. Swiss Medical Weekly, 136, 618–623.

    PubMed  Google Scholar 

  100. Du, C., Cui, F. Z., Zhu, X. D., & de Groot, K. (1999). Three-dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture. Journal of Biomedical Materials Research, 44, 407–415.

    Article  PubMed  CAS  Google Scholar 

  101. Atala, A., & Lanza, R. P. (2002). Methods of tissue engineering. San Diego: Academic.

    Google Scholar 

  102. Seal, B. L., Otero, T. C., & Panitch, A. (2001). Polymeric biomaterials for tissue and organ regeneration. Materials Science and Engineering: R: Reports, 34, 147–230.

    Article  Google Scholar 

  103. Badylak, S. F. (2007). The extracellular matrix as a biologic scaffold material. Biomaterials, 28, 3587–3593.

    Article  PubMed  CAS  Google Scholar 

  104. Zimmermann, W.-H., Melnychenko, I., & Eschenhagen, T. (2004). Engineered heart tissue for regeneration of diseased hearts. Biomaterials, 25, 1639–1647.

    Article  PubMed  CAS  Google Scholar 

  105. Bissell, M. J., & Aggeler, J. (1987). Dynamic reciprocity: how do extracellular matrix and hormones direct gene expression? Progress in Clinical and Biological Research, 249, 251–262.

    PubMed  CAS  Google Scholar 

  106. Kleinman, H. K., Philp, D., & Hoffman, M. P. (2003). Role of the extracellular matrix in morphogenesis. Current Opinion in Biotechnology, 14, 526–532.

    Article  PubMed  CAS  Google Scholar 

  107. Rosso, F., Giordano, A., Barbarisi, M., & Barbarisi, A. (2004). From Cell–ECM interactions to tissue engineering. Journal of Cellular Physiology, 199, 174–180.

    Article  PubMed  CAS  Google Scholar 

  108. Memon, I. A., Sawa, Y., Fukushima, N., et al. (2005). Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. The Journal of Thoracic and Cardiovascular Surgery, 130, 1333–1341.

    Article  PubMed  Google Scholar 

  109. Kutschka, I., Chen, I. Y., Kofidis, T., et al. (2006). Collagen matrices enhance survival of transplanted cardiomyoblasts and contribute to functional improvement of ischemic rat hearts. Circulation, 114, I-167–I-173.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  111. VanWinkle, W. B., Snuggs, M. B., & Buja, L. M. (1996). Cardiogel: a biosynthetic extracellular matrix for cardiomyocyte culture. In Vitro Cellular & Developmental Biology. Animal, 32, 478–485.

    Article  CAS  Google Scholar 

  112. Bick, R. J., Snuggs, M. B., Poindexter, B. J., Buja, L. M., & Van Winkle, W. B. (1998). Physical, contractile and calcium handling properties of neonatal cardiac myocytes cultured on different matrices. Cell Adhesion and Communication, 6, 301–310.

    Article  PubMed  CAS  Google Scholar 

  113. Song, H., Chang, W., Lim, S., et al. (2007). Tissue transglutaminase is essential for integrin-mediated survival of bone marrow-derived mesenchymal stem cells. Stem Cells, 25, 1431–1438.

    Article  PubMed  CAS  Google Scholar 

  114. Beqqali, A., van Eldik, W., Mummery, C., & Passier, R. (2009). Human stem cells as a model for cardiac differentiation and disease. Cellular and Molecular Life Sciences, 66, 800–813.

    Article  PubMed  CAS  Google Scholar 

  115. Baharvand, H., Azarnia, M., Parivar, K., & Ashtiani, S. K. (2005). The effect of extracellular matrix on embryonic stem cell-derived cardiomyocytes. Journal of Molecular and Cellular Cardiology, 38, 495–503.

    Article  PubMed  CAS  Google Scholar 

  116. Chang, W., Lim, S., Song, H., et al. (2007). In vitro expansion of mesenchymal stem cells using 3-D matrix derived from cardiac fibroblast. Tissue Engineering and Regenerative Medicine, 4, 370–375.

    CAS  Google Scholar 

  117. Sreejit, P., & Verma, R. S. (2011). Cardiogel supports adhesion, proliferation and differentiation of stem cells with increased oxidative stress protection. European Cells & Materials, 21, 107–121.

    CAS  Google Scholar 

  118. Marelli, D., Desrosiers, C., el-Alfy, M., Kao, R. L., & Chiu, R. C. (1992). Cell transplantation for myocardial repair: an experimental approach. Cell Transplantation, 1, 383–390.

    PubMed  CAS  Google Scholar 

  119. Koh, G. Y., Klug, M. G., Soonpaa, M. H., & Field, L. J. (1993). Differentiation and long-term survival of C2C12 myoblast grafts in heart. The Journal of Clinical Investigation, 92, 1548–1554.

    Article  PubMed  CAS  Google Scholar 

  120. Chiu, R. C. J., Zibaitis, A., & Kao, R. L. (1995). Cellular cardiomyoplasty: myocardial regeneration with satellite cell Implantation. The Annals of Thoracic Surgery, 60, 12–18.

    PubMed  CAS  Google Scholar 

  121. Murry, C. E., Field, L. J., & Menasche, P. (2005). Cell-based cardiac repair: reflections at the 10-year point. Circulation, 112, 3174–3183.

    Article  PubMed  Google Scholar 

  122. Assmus, B., Schachinger, V., Teupe, C., et al. (2002). Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation, 106, 3009–3017.

    Article  PubMed  Google Scholar 

  123. Strauer, B. E., Brehm, M., Zeus, T., et al. (2002). Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation, 106, 1913–1918.

    Article  PubMed  Google Scholar 

  124. Perin, E. C., Dohmann, H. F. R., Borojevic, R., et al. (2003). Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation, 107, 2294–2302.

    Article  PubMed  Google Scholar 

  125. Janssens, S., Dubois, C., Bogaert, J., et al. (2006). Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. The Lancet, 367, 113–121.

    Article  Google Scholar 

  126. Chen, S. L., Fang, W. W., Ye, F., et al. (2004). Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. The American Journal of Cardiology, 94, 92–95.

    Article  PubMed  Google Scholar 

  127. Melo, L. G., Pachori, A. S., Kong, D., et al. (2004). Molecular and cell-based therapies for protection, rescue, and repair of ischemic myocardium: reasons for cautious optimism. Circulation, 109, 2386–2393.

    Article  PubMed  Google Scholar 

  128. Wollert, K. C., Meyer, G. P., Lotz, J., et al. (2004). Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. The Lancet, 364, 141–148.

    Article  Google Scholar 

  129. Song, H., Song, B. W., Cha, M. J., Choi, I. G., & Hwang, K. C. (2010). Modification of mesenchymal stem cells for cardiac regeneration. Expert Opinion on Biological Therapy, 10, 309–319.

    Article  PubMed  Google Scholar 

  130. Li, R. K., Jia, Z. Q., Weisel, R. D., et al. (1996). Cardiomyocyte transplantation improves heart function. The Annals of Thoracic Surgery, 62, 654–661.

    Article  PubMed  CAS  Google Scholar 

  131. Taylor, D. A., Atkins, B. Z., Hungspreugs, P., et al. (1998). Regenerating functional myocardium: Improved performance after skeletal myoblast transplantation. Nature Medicine, 4, 929–933.

    Article  PubMed  CAS  Google Scholar 

  132. Toma, C., Pittenger, M. F., Cahill, K. S., Byrne, B. J., & Kessler, P. D. (2002). Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation, 105, 93–98.

    Article  PubMed  Google Scholar 

  133. Kehat, I., Kenyagin-Karsenti, D., Snir, M., et al. (2001). Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. The Journal of Clinical Investigation, 108, 407–414.

    PubMed  CAS  Google Scholar 

  134. Wagers, A. J., & Weissman, I. L. (2004). Plasticity of adult stem cells. Cell, 116, 639–648.

    Article  PubMed  CAS  Google Scholar 

  135. Kumar, S., Chanda, D., & Ponnazhagan, S. (2008). Therapeutic potential of genetically modified mesenchymal stem cells. Gene Therapy, 15, 711–715.

    Article  PubMed  CAS  Google Scholar 

  136. Katritsis, D. G., Sotiropoulou, P. A., Karvouni, E., et al. (2005). Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Catheterization and Cardiovascular Interventions, 65, 321–329.

    Article  PubMed  Google Scholar 

  137. Schuleri, K. H., Boyle, A. J., & Hare, J. M. (2007). Mesenchymal Stem Cells for Cardiac Regenerative Therapy. In K. Kauser & A.-M. Zeiher (Eds.), Bone marrow-derived progenitors (pp. 195–218). Heidelberg: Springer Berlin.

    Chapter  Google Scholar 

  138. Shim, W., Mehta, A., Lim, S. Y., et al. (2011). G-CSF for stem cell therapy in acute myocardial infarction: friend or foe? Cardiovascular Research, 89, 20–30.

    Article  PubMed  CAS  Google Scholar 

  139. Jackson, K. A., Majka, S. M., Wang, H., et al. (2001). Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. The Journal of Clinical Investigation, 107, 1395–1402.

    Article  PubMed  CAS  Google Scholar 

  140. Müller-Ehmsen, J., Whittaker, P., Kloner, R. A., et al. (2002). Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. Journal of Molecular and Cellular Cardiology, 34, 107–116.

    Article  PubMed  CAS  Google Scholar 

  141. Singelyn, J. M., DeQuach, J. A., Seif-Naraghia, S. B., Littlefield, R. B., Schup-Magoffina, P. J., & Christman, K. L. (2009). Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials, 30, 5409–5416.

    Article  PubMed  CAS  Google Scholar 

  142. Duan, Y., Liu, Z., O’Neill, J., Wan, L., Freytes, D., & Vunjak-Novakovic, G. (2011). Hybrid gel composed of native heart matrix and collagen induces cardiac differentiation of human embryonic stem cells without supplemental growth factors. Journal of Cardiovascular Translational Research, 4, 605–615.

    Article  PubMed  Google Scholar 

  143. Segers, V. F. M., & Lee, R. T. (2011). Biomaterials to enhance stem cell function in the heart. Circulation Research, 109, 910–922.

    Article  PubMed  CAS  Google Scholar 

  144. Eshghi, S., & Schaffer, D. V. (2008). Engineering microenvironments to control stem cell fate and function. Cambridge: Harvard Stem Cell Institute.

    Google Scholar 

  145. Burdick, J. A., & Vunjak-Novakovic, G. (2009). Engineered microenvironments for controlled stem cell differentiation. Tissue Engineering. Part A, 15, 205–219.

    Article  PubMed  CAS  Google Scholar 

  146. DeQuach, J. A., Mezzano, V., Miglani, A., et al. (2010). Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One, 5, e13039.

    Article  PubMed  CAS  Google Scholar 

  147. Tous, E., Purcell, B., Ifkovits, J., & Burdick, J. (2011). Injectable acellular hydrogels for cardiac repair. Journal of Cardiovascular Translational Research, 4, 528–542.

    Article  PubMed  Google Scholar 

  148. Landa, N., Miller, L., Feinberg, M. S., et al. (2008). Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation, 117, 1388–1396.

    Article  PubMed  CAS  Google Scholar 

  149. Leor, J., Tuvia, S., Guetta, V., et al. (2009). Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in swine. Journal of the American College of Cardiology, 54, 1014–1023.

    Article  PubMed  Google Scholar 

  150. Wu, J., Zeng, F., Huang, X.-P., et al. (2011). Infarct stabilization and cardiac repair with a VEGF-conjugated, injectable hydrogel. Biomaterials, 32, 579–586.

    Article  PubMed  CAS  Google Scholar 

  151. Dobner, S., Bezuidenhout, D., Govender, P., Zilla, P., & Davies, N. (2009). A synthetic non-degradable polyethylene glycol hydrogel retards adverse post-infarct left ventricular remodeling. Journal of Cardiac Failure, 15, 629–636.

    Article  PubMed  CAS  Google Scholar 

  152. Tous, E., Ifkovits, J. L., Koomalsingh, K. J., et al. (2011). Influence of injectable hyaluronic acid hydrogel degradation behavior on infarction-induced ventricular remodeling. Biomacromolecules, 12, 4127–4135.

    Article  PubMed  CAS  Google Scholar 

  153. Davis, M. E., Hsieh, P. C. H., Grodzinsky, A. J., & Lee, R. T. (2005). Custom design of the cardiac microenvironment with biomaterials. Circulation Research, 97, 8–15.

    Article  PubMed  CAS  Google Scholar 

  154. Boyang, Z., Yun, X., Anne, H., Nimalan, T., & Milica, R. (2011). Micro- and nanotechnology in cardiovascular tissue engineering. Nanotechnology, 22, 494003.

    Article  Google Scholar 

  155. Macfelda, K., Kapeller, B., Wilbacher, I., & Losert, U. M. (2007). Behavior of cardiomyocytes and skeletal muscle cells on different extracellular matrix components—Relevance for cardiac tissue engineering. Artificial Organs, 31, 4–12.

    Article  PubMed  CAS  Google Scholar 

  156. Jawad, H., Ali, N. N., Lyon, A. R., Chen, Q. Z., Harding, S. E., & Boccaccini, A. R. (2007). Myocardial tissue engineering: a review. Journal of Tissue Engineering and Regenerative Medicine, 1, 327–342.

    Article  PubMed  CAS  Google Scholar 

  157. Simpson, D. G., Terracio, L., Terracio, M., Price, R. L., Turner, D. C., & Borg, T. K. (1994). Modulation of cardiac myocyte phenotype in vitro by the composition and orientation of the extracellular matrix. Journal of Cellular Physiology, 161, 89–105.

    Article  PubMed  CAS  Google Scholar 

  158. Guan, J., Wang, F., Li, Z., et al. (2011). The stimulation of the cardiac differentiation of mesenchymal stem cells in tissue constructs that mimic myocardium structure and biomechanics. Biomaterials, 32, 5568–5580.

    Article  PubMed  CAS  Google Scholar 

  159. Kurdi, M., Chidiac, R., Hoemann, C., Zouein, F., Zgheib, C., & Booz, G. W. (2010). Hydrogels as a platform for stem cell delivery to the heart. Congestive Heart Failure, 16, 132–135.

    Article  PubMed  Google Scholar 

  160. Madden, L. R., Mortisen, D. J., Sussman, E. M., et al. (2010). Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proceedings of the National Academy of Sciences of the United States of America, 107, 15211–15216.

    Article  PubMed  CAS  Google Scholar 

  161. Rota, M., Kajstura, J., Hosoda, T., et al. (2007). Bone marrow cells adopt the cardiomyogenic fate in vivo. Proceedings of the National Academy of Sciences USA, 104, 17783–17788.

    Article  CAS  Google Scholar 

  162. Schenke-Layland, K., Nsair, A., Van Handel, B., et al. (2011). Recapitulation of the embryonic cardiovascular progenitor cell niche. Biomaterials, 32, 2748–2756.

    Article  PubMed  CAS  Google Scholar 

  163. Wollert, K. C., & Drexler, H. (2010). Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nature Reviews Cardiology, 7, 204–215.

    Article  PubMed  Google Scholar 

  164. Zimmermann, W.-H., Melnychenko, I., Wasmeier, G., et al. (2006). Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nature Medicine, 12, 452–458.

    Article  PubMed  CAS  Google Scholar 

  165. van Laake, L., van Donselaar, E., Monshouwer-Kloots, J., et al. (2010). Extracellular matrix formation after transplantation of human embryonic stem cell-derived cardiomyocytes. Cellular and Molecular Life Science, 67, 277–290.

    Article  CAS  Google Scholar 

  166. Adler, E. D., Chen, V. C., Bystrup, A., et al. (2010). The cardiomyocyte lineage is critical for optimization of stem cell therapy in a mouse model of myocardial infarction. The FASEB Journal, 24, 1073–1081.

    Article  CAS  Google Scholar 

  167. Miner, E. C., & Miller, W. L. (2006). A look between the cardiomyocytes: the extracellular matrix in heart failure. Mayo Clinic Proceedings, 81, 71–76.

    Article  PubMed  CAS  Google Scholar 

  168. Jabbari, E. (2010). Biologically-responsive hybrid biomaterials: A reference for material scientists and bioengineers. In E. Jabbari, & Khademhosseini, A. (Eds.), Singapore: World Scientific Publishing Co.

  169. Minato, A., Ise, H., Goto, M., & Akaike, T. (2011). Cardiac differentiation of embryonic stem cells by substrate immobilization of insulin-like growth factor binding protein 4 with elastin-like polypeptides. Biomaterials, 33, 515–523.

    Article  PubMed  CAS  Google Scholar 

  170. Loke, W. K., Khor, E., Wee, A., Teoh, S. H., & Chian, K. S. (1996). Hybrid biomaterials based on the interaction of polyurethane oligomers with porcine pericardium. Biomaterials, 17, 2163–2172.

    Article  PubMed  CAS  Google Scholar 

  171. Jawad, H., Lyon, A. R., Harding, S. E., Ali, N. N., & Boccaccini, A. R. (2008). Myocardial tissue engineering. British Medical Bulletin, 87, 31–47.

    Article  PubMed  CAS  Google Scholar 

  172. Yang, M.-C., Wang, S.-S., Chou, N.-K., et al. (2009). The cardiomyogenic differentiation of rat mesenchymal stem cells on silk fibroin–polysaccharide cardiac patches in vitro. Biomaterials, 30, 3757–3765.

    Article  PubMed  CAS  Google Scholar 

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Sreejit, P., Verma, R.S. Natural ECM as Biomaterial for Scaffold Based Cardiac Regeneration Using Adult Bone Marrow Derived Stem Cells. Stem Cell Rev and Rep 9, 158–171 (2013). https://doi.org/10.1007/s12015-013-9427-6

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