Table of Contents
International Journal of Tissue Engineering
Volume 2013, Article ID 198762, 15 pages
http://dx.doi.org/10.1155/2013/198762
Research Article

Engineered Human Muscle Tissue from Skeletal Muscle Derived Stem Cells and Induced Pluripotent Stem Cell Derived Cardiac Cells

1Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15219, USA
2Department of Medicine, University of Pittsburgh, Pittsburgh, PA 15261, USA
3Department of Biomedical Engineering, Duke University, Durham, NC 27708, USA
4Department of Developmental Biology, University of Pittsburgh, Pittsburgh, PA 15224, USA
5McGowan Institute of Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA
6Rangos Research Center, Room 8121, 4401 Pennsylvania Avenue, Pittsburgh, PA 15224, USA

Received 30 May 2013; Revised 19 September 2013; Accepted 28 September 2013

Academic Editor: Tianqing Liu

Copyright © 2013 Jason Tchao 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. O. Bergmann, R. D. Bhardwaj, S. Bernard et al., “Evidence for cardiomyocyte renewal in humans,” Science, vol. 324, no. 5923, pp. 98–102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. A. S. Go, D. Mozaffarian, V. L. Roger et al., “Heart disease and stroke statistics—2013 update: a report from the American heart association,” Circulation, vol. 127, no. 1, pp. e6–e245, 2013. View at Publisher · View at Google Scholar
  3. M. Lavasani, A. Lu, S. D. Thompson, P. D. Robbins, J. Huard, and L. J. Niedernhofer, “Isolation of muscle-derived stem/progenitor cells based on adhesion characteristics to collagen-coated surfaces,” Methods in Molecular Biology, vol. 976, pp. 53–65, 2013. View at Publisher · View at Google Scholar
  4. A. Usas, J. Mačiulaitis, R. Mačiulaitis, N. Jakuboniene, A. Milašius, and J. Huard, “Skeletal muscle-derived stem cells: implications for cell-mediated therapies,” Medicina, vol. 47, no. 9, pp. 469–479, 2011. View at Google Scholar · View at Scopus
  5. K. C. Clause, J. P. Tinney, L. J. Liu et al., “A three-dimensional gel bioreactor for assessment of cardiomyocyte induction in skeletal muscle-derived stem cells,” Tissue Engineering C, vol. 16, no. 3, pp. 375–385, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. K. L. Fujimoto, K. C. Clause, L. J. Liu et al., “Engineered fetal cardiac graft preserves its cardiomyocyte proliferation within postinfarcted myocardium and sustains cardiac function,” Tissue Engineering A, vol. 17, no. 5-6, pp. 585–596, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Lewitzky and S. Yamanaka, “Reprogramming somatic cells towards pluripotency by defined factors,” Current Opinion in Biotechnology, vol. 18, no. 5, pp. 467–473, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. 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
  9. L. Yang, M. H. Soonpaa, E. D. Adler et al., “Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population,” Nature, vol. 453, no. 7194, pp. 524–528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Lin, J. Kim, Y. Li et al., “High-purity enrichment of functional cardiovascular cells from human iPS cells,” Cardiovascular Research, vol. 95, no. 3, pp. 327–335, 2012. View at Publisher · View at Google Scholar
  11. C. Jopling, S. Boue, and J. C. I. Belmonte, “Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration,” Nature Reviews Molecular Cell Biology, vol. 12, no. 2, pp. 79–89, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Rajabi, C. Kassiotis, P. Razeghi, and H. Taegtmeyer, “Return to the fetal gene program protects the stressed heart: a strong hypothesis,” Heart Failure Reviews, vol. 12, no. 3-4, pp. 331–343, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Kuwahara, T. Nishikimi, and K. Nakao, “Transcriptional regulation of the fetal cardiac gene program,” Journal of Pharmacological Sciences, vol. 119, no. 3, pp. 198–203, 2012. View at Publisher · View at Google Scholar
  14. K. C. Clause, J. Tchao, M. C. Powell et al., “Developing cardiac and skeletal muscle share fast-skeletal myosin heavy chain and cardiac troponin-I expression,” PLoS ONE, vol. 7, no. 7, Article ID e40725, 2012. View at Publisher · View at Google Scholar
  15. F. S. Apple, “Tissue specificity of cardiac troponin I, cardiac troponin T and creatine kinase-MB,” Clinica Chimica Acta, vol. 284, no. 2, pp. 151–159, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Saggin, L. Gorza, S. Ausoni, and S. Schiaffino, “Troponin I switching in the developing heart,” The Journal of Biological Chemistry, vol. 264, no. 27, pp. 16299–16302, 1989. View at Google Scholar · View at Scopus
  17. S. Schiaffino, L. Gorza, and S. Ausoni, “Troponin isoform switching in the developing heart and its functional consequences,” Trends in Cardiovascular Medicine, vol. 3, no. 1, pp. 12–17, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Zheng, B. Cao, M. Crisan et al., “Prospective identification of myogenic endothelial cells in human skeletal muscle,” Nature Biotechnology, vol. 25, no. 9, pp. 1025–1034, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Zheng, C. W. Chen, G. Li et al., “Isolation of myogenic stem cells from cultures of cryopreserved human skeletal muscle,” Cell Transplantation, vol. 21, no. 6, pp. 1087–1093, 2012. View at Publisher · View at Google Scholar
  20. C. W. Chen, M. Corselli, B. Péault, and J. Huard, “Human blood-vessel-derived stem cells for tissue repair and regeneration,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 597439, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Crisan, S. Yap, L. Casteilla et al., “A perivascular origin for mesenchymal stem cells in multiple human organs,” Cell Stem Cell, vol. 3, no. 3, pp. 301–313, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Grajales, J. Garcia, and D. L. Geenen, “Induction of cardiac myogenic lineage development differs between mesenchymal and satellite cells and is accelerated by bone morphogenetic protein-4,” Journal of Molecular and Cellular Cardiology, vol. 53, no. 3, pp. 382–391, 2012. View at Publisher · View at Google Scholar
  23. A. Fabiato and F. Fabiato, “Dependence of the contractile activation of skinned cardiac cells on the sarcomere length,” Nature, vol. 256, no. 5512, pp. 54–56, 1975. View at Publisher · View at Google Scholar · View at Scopus
  24. L. M. Hanft and K. S. McDonald, “Length dependence of force generation exhibit similarities between rat cardiac myocytes and skeletal muscle fibres,” The Journal of Physiology, vol. 588, no. 15, pp. 2891–2903, 2010. View at Google Scholar · View at Scopus
  25. G. Brown, E. Bülbring, and B. D. Burns, “The action of adrenaline on mammalian skeletal muscle,” The Journal of Physiology, vol. 107, pp. 115–128, 1948. View at Google Scholar
  26. U. R. Mikkelsen, H. Gissel, A. Fredsted, and T. Clausen, “Excitation-induced cell damage and β2-adrenoceptor agonist stimulated force recovery in rat skeletal muscle,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 290, no. 2, pp. R265–R272, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. D. C. Andersson, M. J. Betzenhauser, S. Reiken, A. Umanskaya, T. Shiomi, and A. R. Marks, “Stress-induced increase in skeletal muscle force requires protein kinase A phosphorylation of the ryanodine receptor,” The Journal of Physiology, vol. 590, part 24, pp. 6381–6387, 2012. View at Publisher · View at Google Scholar
  28. K. Tobita, L. J. Liu, A. M. Janczewski et al., “Engineered early embryonic cardiac tissue retains proliferative and contractile properties of developing embryonic myocardium,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 291, no. 4, pp. H1829–H1837, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. A. F. Dulhunty and P. W. Gage, “Effects of extracellular calcium concentration and dihydropyridines on contraction in mammalian skeletal muscle,” The Journal of Physiology, vol. 399, pp. 63–80, 1988. View at Google Scholar · View at Scopus
  30. B. Fraysse, T. Rouaud, M. Millour, J. Fontaine-Pérus, M. Gardahaut, and D. O. Levitsky, “Expression of the Na+/Ca2+ exchanger in skeletal muscle,” The American Journal of Physiology—Cell Physiology, vol. 280, no. 1, pp. C146–C154, 2001. View at Google Scholar · View at Scopus
  31. M. Arai, K. Otsu, D. H. MacLennan, and M. Periasamy, “Regulation of sarcoplasmic reticulum gene expression during cardiac and skeletal muscle development,” The American Journal of Physiology—Cell Physiology, vol. 262, no. 3, pp. C614–C620, 1992. View at Google Scholar · View at Scopus
  32. W. Liu, K. Yasui, T. Opthof et al., “Developmental changes of Ca2+ handling in mouse ventricular cells from early embryo to adulthood,” Life Sciences, vol. 71, no. 11, pp. 1279–1292, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. T. L. Creazzo, J. Burch, and R. E. Godt, “Calcium buffering and excitation-contraction coupling in developing avian myocardium,” Biophysical Journal, vol. 86, no. 2, pp. 966–977, 2004. View at Google Scholar · View at Scopus
  34. T. S. Klitzner, “Maturational changes in excitation-contraction coupling in mammalian myocardium,” Journal of the American College of Cardiology, vol. 17, no. 1, pp. 218–225, 1991. View at Google Scholar · View at Scopus
  35. J. P. Louboutin, V. Fichter-Gagnepain, and J. Noireaud, “Comparison of contractile properties between developing and regenerating soleus muscle: influence of external calcium concentration upon the contractility,” Muscle and Nerve, vol. 18, no. 11, pp. 1292–1299, 1995. View at Publisher · View at Google Scholar · View at Scopus
  36. S. O. Winitsky, T. V. Gopal, S. Hassanzadeh et al., “Adult murine skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro,” PLoS Biology, vol. 3, no. 4, article e87, 2005. View at Google Scholar · View at Scopus
  37. O. Binah, “Tetanus in the mammalian heart: studies in the shrew myocardium,” Journal of Molecular and Cellular Cardiology, vol. 19, no. 12, pp. 1247–1252, 1987. View at Google Scholar · View at Scopus
  38. W. Burridge, “Cardiac tetanus,” The Journal of Physiology, vol. 54, pp. 248–252, 1920. View at Google Scholar
  39. D. G. Edmondson, G. E. Lyons, J. F. Martin, and E. N. Olson, “Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis,” Development, vol. 120, no. 5, pp. 1251–1263, 1994. View at Google Scholar · View at Scopus
  40. P. A. W. Anderson, N. N. Malouf, A. E. Oakeley, E. D. Pagani, and P. D. Allen, “Troponin T isoform expression in humans: a comparison among normal and failing adult heart, fetal heart, and adult and fetal skeletal muscle,” Circulation Research, vol. 69, no. 5, pp. 1226–1233, 1991. View at Google Scholar · View at Scopus
  41. Y. Mayer, H. Czosnek, P. E. Zeelon, D. Yaffe, and U. Nudel, “Expression of the genes coding for the skeletal muscle and cardiac actins in the heart,” Nucleic Acids Research, vol. 12, no. 2, pp. 1087–1100, 1984. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Saggin, S. Ausoni, L. Gorza, S. Sartore, and S. Schiaffino, “Troponin T switching in the developing rat heart,” The Journal of Biological Chemistry, vol. 263, no. 34, pp. 18488–18492, 1988. View at Google Scholar · View at Scopus
  43. C. Cognard, M. Rivet-Bastide, B. Contantin, and G. Raymond, “Progressive predominance of “skeletal” versus “cardiac” types of excitation-contraction coupling during in vitro skeletal myogenesis,” Pflugers Archiv, vol. 422, no. 2, pp. 207–209, 1992. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Tamaki, A. Akatsuka, Y. Okada et al., “Cardiomyocyte formation by skeletal muscle-derived multi-myogenic stem cells after transplantation into infarcted myocardium,” PLoS ONE, vol. 3, no. 3, Article ID e1789, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Iijima, T. Nagai, M. Mizukami et al., “Beating is necessary for transdifferentiation of skeletal muscle-derived cells into cardiomyocytes,” The FASEB Journal, vol. 17, no. 10, pp. 1361–1363, 2003. View at Google Scholar · View at Scopus
  46. G. Invernici, S. Cristini, P. Madeddu et al., “Human adult skeletal muscle stem cells differentiate into cardiomyocyte phenotype in vitro,” Experimental Cell Research, vol. 314, no. 2, pp. 366–376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Krueger and F. M. Hoffmann, “Identification of retinoic acid in a high content screen for agents that overcome the anti-myogenic effect of TGF-beta-1,” PLoS ONE, vol. 5, no. 11, Article ID e15511, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Ryan, J. Liu, A. Chu, L. Wang, A. Blais, and I. S. Skerjanc, “Retinoic acid enhances skeletal myogenesis in human embryonic stem cells by expanding the premyogenic progenitor population,” Stem Cell Reviews and Reports, vol. 8, no. 2, pp. 482–493, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. H. H. Arnold, C. D. Gerharz, H. E. Gabbert, and A. Salminen, “Retinoic acid induces myogenin synthesis and myogenic differentiation in the rat rhabdomyosarcoma cell line BA-Han-1C,” Journal of Cell Biology, vol. 118, no. 4, pp. 877–887, 1992. View at Google Scholar · View at Scopus
  50. A. M. Wobus, G. Kaomei, J. Shan et al., “Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes,” Journal of Molecular and Cellular Cardiology, vol. 29, no. 6, pp. 1525–1539, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. B. R. Keegan, J. L. Feldman, G. Begemann, P. W. Ingham, and D. Yelon, “Retinoic acid signaling restricts the cardiac progenitor pool,” Science, vol. 307, no. 5707, pp. 247–249, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Crippa, M. Cassano, G. Messina et al., “miR669a and miR669q prevent skeletal muscle differentiation in postnatal cardiac progenitors,” Journal of Cell Biology, vol. 193, no. 7, pp. 1197–1212, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. I. S. Skerjanc, “Cardiac and skeletal muscle development in P19 embryonal carcinoma cells,” Trends in Cardiovascular Medicine, vol. 9, no. 5, pp. 139–143, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. E. N. Olson, “Regulation of muscle transcription by the MyoD family: the heart of the matter,” Circulation Research, vol. 72, no. 1, pp. 1–6, 1993. View at Google Scholar · View at Scopus
  55. J. D. Fu, N. R. Stone, L. Liu et al., “Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state,” Stem Cell Reports, vol. 1, no. 3, pp. 235–247, 2013. View at Publisher · View at Google Scholar
  56. S. Crippa, M. Cassano, G. Messina et al., “miR669a and miR669q prevent skeletal muscle differentiation in postnatal cardiac progenitors,” Journal of Cell Biology, vol. 193, no. 7, pp. 1197–1212, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Tirosh-Finkel, H. Elhanany, A. Rinon, and E. Tzahor, “Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract,” Development, vol. 133, no. 10, pp. 1943–1953, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. T. K. Kim, J. Sul, N. B. Peternko et al., “Transcriptome transfer provides a model for understanding the phenotype of cardiomyocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 29, pp. 11918–11923, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. 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
  60. P. Menasché, “Skeletal myoblasts for cardiac repair: act II?” Journal of the American College of Cardiology, vol. 52, no. 23, pp. 1881–1883, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Suzuki, N. J. Brand, S. Allen et al., “Overexpression of connexin 43 in skeletal myoblasts: relevance to cell transplantation to the heart,” Journal of Thoracic and Cardiovascular Surgery, vol. 122, no. 4, pp. 759–766, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. O. Tolmachov, Y. L. Ma, M. Themis et al., “Overexpression of connexin 43 using a retroviral vector improves electrical coupling of skeletal myoblasts with cardiac myocytes in vitro,” BMC Cardiovascular Disorders, vol. 6, article 25, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Reinecke, E. Minami, J. I. Virag, and C. E. Murry, “Gene transfer of connexin43 into skeletal muscle,” Human Gene Therapy, vol. 15, no. 7, pp. 627–636, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Neef, Y. H. Choi, S. Perumal Srinivasan et al., “Mechanical preconditioning enables electrophysiologic coupling of skeletal myoblast cells to myocardium,” Journal of Thoracic and Cardiovascular Surgery, vol. 144, no. 5, pp. 1176.e1–1184.e1, 2012. View at Publisher · View at Google Scholar
  65. S. P. Srinivasan, K. Neef, P. Treskes et al., “Enhanced gap junction expression in myoblast-containing engineered tissue,” Biochemical and Biophysical Research Communications, vol. 422, no. 3, pp. 462–468, 2012. View at Publisher · View at Google Scholar
  66. K. L. Kreutziger and C. E. Murry, “Engineered human cardiac tissue,” Pediatric Cardiology, vol. 32, no. 3, pp. 334–341, 2011. View at Publisher · View at Google Scholar · View at Scopus