Differentiation of human embryonic stem cells to cardiomyocytes for in vitro and in vivo applications

Stem Cell Reviews and Reports

Volumn 6, Issue 1, 2010, Pages 108-120

  Vidarsson, Hilmar ^a   Hyllner, Johan ^a   Sartipy, Peter ^a  

^a Cellartis AB   (Sweden)

Author keywords

Cardiomyocytes; Differentiation; Drug discovery; Human embryonic stem cells; Regenerative medicine

Indexed keywords

ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DRUG DEVELOPMENT; DRUG EFFECT; EMBRYONIC STEM CELL; HEART DISEASE; HEART MUSCLE CELL; HUMAN; METHODOLOGY; PHYSIOLOGY; REGENERATIVE MEDICINE; REVIEW; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; DRUG DISCOVERY; EMBRYONIC STEM CELLS; HEART DISEASES; HUMANS; MYOCYTES, CARDIAC; REGENERATIVE MEDICINE;

EID: 77949293236     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-010-9113-x     Document Type: Review

References (100)

1. Meyer, T., Sartipy, P., Blind, F., Leisgen, C., & Guenther, E. (2007). New cell models and assays in cardiac safety profiling. Expert Opinion on Drug Metabolism and Toxicology, 3, 507-517.
2. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282, 1145-1147.
3. Bongso, A., & Tan, S. (2005). Human blastocyst culture and derivation of embryonic stem cell lines. Stem Cell Review, 1, 87-98.
4. Daley, G. Q. (2007). L, Auerbach JM, et al. Ethics. The ISSCR guidelines for human embryonic stem cell research. Science, 315, 603-604.
5. Ameen, C., Strehl, R., Bjorquist, P., Lindahl, A., Hyllner, J., & Sartipy, P. (2008). Human embryonic stem cells: current technologies and emerging industrial applications. Critical Reviews in Oncology/hematology, 65, 54-80.
6. Dimmeler, S., Burchfield, J., & Zeiher, A. M. (2008). Cell-based therapy of myocardial infarction. Arteriosclerosis, Thrombosis, and Vascular Biology, 28, 208-216.
7. Murry, C. E., Field, L. J., & Menasche, P. (2005). Cell-based cardiac repair: reflections at the 10-year point. Circulation, 112, 3174-3183.
8. Anversa, P., Leri, A., Rota, M., et al. (2007). Concise review: stem cells, myocardial regeneration, and methodological artifacts. Stem Cells, 25, 589-601.
9. Zhang, J., Wilson, G. F., Soerens, A. G., et al. (2009). Functional cardiomyocytes derived from human induced pluripotent stem cells. Circulation Research, 104, e30-e41.
10. Zwi, L., Caspi, O., Arbel, G., et al. (2009). Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation, 120, 1513-1523.
11. Bruneau, B. G. (2008). The developmental genetics of congenital heart disease. Nature, 451, 943-948.
12. Buckingham, M., Meilhac, S., & Zaffran, S. (2005). Building the mammalian heart from two sources of myocardial cells. Nature Reviews Genetics, 6, 826-835.
13. Mummery, C., van der Heyden, M. A., de Boer, T. P., et al. (2007). Cardiomyocytes from human and mouse embryonic stem cells. Methods in Molecular Medicine, 140, 249-272.
14. He, J. Q., January, C. T., Thomson, J. A., & Kamp, T. J. (2007). Human embryonic stem cell-derived cardiomyocytes: drug discovery and safety pharmacology. Expert Opinion on Drug Discovery, 2, 739-753.
15. Murry, C. E., & Keller, G. (2008). Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell, 132, 661-680.
16. Torella, D., Indolfi, C., Goldspink, D. F., & Ellison, G. M. (2008). Cardiac stem cell-based myocardial regeneration: towards a translational approach. Cardiovascular and Hematological Agents in Medicinal Chemistry, 6, 53-59.
17. Xu, Y., Shi, Y., & Ding, S. (2008). A chemical approach to stem-cell biology and regenerative medicine. Nature, 453, 338-344.
18. Itskovitz-Eldor, J., Schuldiner, M., Karsenti, D., et al. (2000). Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Molecular Medicine, 6, 88-95.
19. 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. Journal of clinical investigation, 108, 407-414.
20. Mummery, C., Ward-van Oostwaard, D., Doevendans, P., et al. (2003). Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation, 107, 2733-2740.
21. Graichen, R., Xu, X., Braam, S. R., et al. (2008). Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation, 76, 357-370.
22. Xu, X. Q., Graichen, R., Soo, S. Y., et al. (2008). Chemically defined medium supporting cardiomyocyte differentiation of human embryonic stem cells. Differentiation, 76, 958-970.
23. Zaffran, S., & Frasch, M. (2002). Early signals in cardiac development. Circulation Research, 91, 457-469.
24. Olson, E. N. (2004). A decade of discoveries in cardiac biology. Nature Medicine, 10, 467-474.
25. Filipczyk, A. A., Passier, R., Rochat, A., & Mummery, C. L. (2007). Regulation of cardiomyocyte differentiation of embryonic stem cells by extracellular signalling. Cellular and Molecular Life Sciences, 64, 704-718.
26. Yoon, B. S., Yoo, S. J., Lee, J. E., You, S., Lee, H. T., & Yoon, H. S. (2006). Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and 5-azacytidine treatment. Differentiation, 74, 149-159.
27. Ng, E. S., Davis, R. P., Azzola, L., Stanley, E. G., & Elefanty, A. G. (2005). Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood, 106, 1601-1603.
28. Burridge, P. W., Anderson, D., Priddle, H., et al. (2007). Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells, 25, 929-938.
29. Marvin, M. J., Di Rocco, G., Gardiner, A., Bush, S. M., & Lassar, A. B. (2001). Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes and Development, 15, 316-327.
30. Schneider, V. A., & Mercola, M. (2001). Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes and Development, 15, 304-315.
31. Klaus, A., & Birchmeier, W. (2009). Developmental signaling in myocardial progenitor cells: a comprehensive view of Bmp-and Wnt/beta-catenin signaling. Pediatric Cardiology, 30, 609-616.
32. Tran, T. H., Wang, X., Browne, C., et al. (2009). Wnt3a-induced mesoderm formation and cardiomyogenesis in human embryonic stem cells. Stem Cells, 27, 1869-1878.
33. Passier, R., Oostwaard, D. W., Snapper, J., et al. (2005). Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells, 23, 772-780.
34. 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.
35. Takahashi, T., Lord, B., Schulze, P. C., et al. (2003). Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation, 107, 1912-1916.
36. Wu, X., Ding, S., Ding, Q., Gray, N. S., & Schultz, P. G. (2004). Small molecules that induce cardiomyogenesis in embryonic stem cells. Journal of the American Chemical Society, 126, 1590-1591.
37. Willems, E., Bushway, P. J., & Mercola, M. (2009). Natural and synthetic regulators of embryonic stem cell cardiogenesis. Pediatric Cardiology, 30, 635-642.
38. Passier, R., van Laake, L. W., & Mummery, C. L. (2008). Stem-cell-based therapy and lessons from the heart. Nature, 453, 322-329.
39. Bu, L., Jiang, X., Martin-Puig, S., et al. (2009). Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature, 460, 113-117.
40. Kattman, S. J., Huber, T. L., & Keller, G. M. (2006). Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Developmental Cell, 11, 723-732.
41. Yang, L., Soonpaa, M. H., Adler, E. D., et al. (2008). Human cardiovascular progenitor cells develop from a KDR + embryonic-stem-cell-derived population. Nature, 453, 524-528.
42. Moretti, A., Caron, L., Nakano, A., et al. (2006). Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell, 127, 1151-1165.
43. Christoforou, N., Miller, R. A., Hill, C. M., Jie, C. C., McCallion, A. S., & Gearhart, J. D. (2008). Mouse ES cell-derived cardiac precursor cells are multipotent and facilitate identification of novel cardiac genes. Journal of clinical investigation, 118, 894-903.
44. Xu, C., Police, S., Rao, N., & Carpenter, M. K. (2002). Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circulation Research, 91, 501-508.
45. Xu, C., Police, S., Hassanipour, M., & Gold, J. D. (2006). Cardiac bodies: a novel culture method for enrichment of cardiomyocytes derived from human embryonic stem cells. Stem Cells and Development, 15, 631-639.
46. Rust, W., Balakrishnan, T., & Zweigerdt, R. (2009). Cardiomyocyte enrichment from human embryonic stem cell cultures by selection of ALCAM surface expression. Regenerative Medicine, 4, 225-237.
47. Kolossov, E., Lu, Z., Drobinskaya, I., et al. (2005). Identification and characterization of embryonic stem cell-derived pacemaker and atrial cardiomyocytes. FASEB journal, 19, 577-579.
48. Anderson, D., Self, T., Mellor, I. R., Goh, G., Hill, S. J., & Denning, C. (2007). Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Molecular Theraphy, 15, 2027-2036.
49. Huber, I., Itzhaki, I., Caspi, O., et al. (2007). Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. Faseb Journal, 21, 2551-2563.
50. Fu JD, Jiang P, Rushing S, Liu J, Chiamvimonvat N, Li RA. Na+/Ca2+ exchanger is a determinant of excitation-contraction coupling in human embryonic stem cell-derived ventricular cardiomyocytes. Stem Cells Dev 2009.
51. Xu, X. Q., Zweigerdt, R., Soo, S. Y., et al. (2008). Highly enriched cardiomyocytes from human embryonic stem cells. Cytotherapy, 10, 376-389.
52. Kita-Matsuo, H., Barcova, M., Prigozhina, N., et al. (2009). Lentiviral vectors and protocols for creation of stable hESC lines for fluorescent tracking and drug resistance selection of cardiomyocytes. PLoS ONE, 4, e5046.
53. Snir, M., Kehat, I., Gepstein, A., et al. (2003). Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. American Journal of Physiology Heart and Circulatory Physiology, 285, H2355-H2363.
54. He, J. Q., Ma, Y., Lee, Y., Thomson, J. A., & Kamp, T. J. (2003). Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circulation Research, 93, 32-39.
55. Satin, J., Kehat, I., Caspi, O., et al. (2004). Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. Journal of physiology, 559, 479-496.
56. Dolnikov, K., Shilkrut, M., Zeevi-Levin, N., et al. (2005). Functional properties of human embryonic stem cell-derived cardiomyocytes. Annals of the New York Academy of Sciences, 1047, 66-75.
57. Sartiani, L., Bettiol, E., Stillitano, F., Mugelli, A., Cerbai, E., & Jaconi, M. E. (2007). Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells, 25, 1136-1144.
58. Reppel, M., Boettinger, C., & Hescheler, J. (2004). Beta-adrenergic and muscarinic modulation of human embryonic stem cell-derived cardiomyocytes. Cell Physiology and Biochemistry, 14, 187-196.
59. Norstrom, A., Akesson, K., Hardarson, T., Hamberger, L., Bjorquist, P., & Sartipy, P. (2006). Molecular and pharmacological properties of human embryonic stem cell-derived cardiomyocytes. Experimental Biology and Medicine (Maywood), 231, 1753-1762.
60. Binah, O., Dolnikov, K., Sadan, O., et al. (2007). Functional and developmental properties of human embryonic stem cells-derived cardiomyocytes. Journal of electrocardiology, 40, S192-S196.
61. Brito-Martins, M., Harding, S. E., & Ali, N. N. (2008). beta(1)-and beta(2)-adrenoceptor responses in cardiomyocytes derived from human embryonic stem cells: comparison with failing and non-failing adult human heart. British Journal of Pharmacology, 153, 751-759.
62. Beqqali, A., Kloots, J., Ward-van Oostwaard, D., Mummery, C., & Passier, R. (2006). Genome-wide transcriptional profiling of human embryonic stem cells differentiating to cardiomyocytes. Stem Cells, 24, 1956-1967.
63. Synnergren, J., Adak, S., Englund, M. C., et al. (2008). Cardiomyogenic gene expression profiling of differentiating human embryonic stem cells. Journal of biotechnology, 134, 162-170.
64. Synnergren J, Akesson K, Dahlenborg K, et al. Molecular signature of cardiomyocyte clusters derived from human embryonic stem cells. Stem Cells 2008.
65. Cao, F., Wagner, R. A., Wilson, K. D., et al. (2008). Transcriptional and functional profiling of human embryonic stem cell-derived cardiomyocytes. PLoS ONE, 3, e3474.
66. Xu, X. Q., Soo, S. Y., Sun, W., & Zweigerdt, R. (2009). Global Expression Profile of Highly Enriched Cardiomyocytes Derived from Human Embryonic Stem Cells. Stem Cells, 27, 2163-2174.
67. Kola, I., & Landis, J. (2004). Can the pharmaceutical industry reduce attrition rates? Nature Reviews Drug Discovery, 3, 711-715.
68. Jonsson, M. K. B., van Veen, T. A. B., Goumans, M. J., Vos, M. A., Duker, G., & Sartipy, P. (2009). Improvement of cardiac efficacy and safety models in drug discovery by the use of stem cell-derived cardiomyocytes. Expert Opinion Drug Discovery, 4, 357-372.
69. Kimes, B. W., & Brandt, B. L. (1976). Properties of a clonal muscle cell line from rat heart. Experimental Cell Research, 98, 367-381.
70. Claycomb, W. C., Lanson, N. A., Jr., Stallworth, B. S., et al. (1998). 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, 95, 2979-2984.
71. Reppel, M., Pillekamp, F., Brockmeier, K., et al. (2005). The electrocardiogram of human embryonic stem cell-derived cardiomyocytes. Journal of electrocardiology, 38, 166-170.
72. Caspi O, Itzhaki I, Arbel G, et al. In Vitro Electrophysiological Drug Testing using Human Embryonic Stem Cell Derived Cardiomyocytes. Stem Cells Dev 2008.
73. Tanaka, T., Tohyama, S., Murata, M., et al. (2009). In vitro pharmacologic testing using human induced pluripotent stem cell-derived cardiomyocytes. Biochemical and Biophysical Research Communications, 385, 497-502.
74. Altena, R., Perik, P. J., van Veldhuisen, D. J., de Vries, E. G., & Gietema, J. A. (2009). Cardiovascular toxicity caused by cancer treatment: strategies for early detection. Lancet oncology, 10, 391-399.
75. Dolci, A., Dominici, R., Cardinale, D., Sandri, M. T., & Panteghini, M. (2008). Biochemical markers for prediction of chemotherapy-induced cardiotoxicity: systematic review of the literature and recommendations for use. American Journal of Clinical Pathology, 130, 688-695.
76. Kloner, R. A., & Jennings, R. B. (2001). Consequences of brief ischemia: stunning, preconditioning, and their clinical implications: part 1. Circulation, 104, 2981-2989.
77. Braam SR, Denning C, van den Brink S, et al. Improved genetic manipulation of human embryonic stem cells. Nat Methods 2008.
78. Sartipy, P., Olsson, B., Hyllner, J., & Synnergren, J. (2009). Regulation of 'stemness' and stem cell differentiation by microRNAs. IDrugs, 12, 492-496.
79. Dimos, J. T., Rodolfa, K. T., Niakan, K. K., et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science, 321, 1218-1221.
80. Park, I. H., Arora, N., Huo, H., et al. (2008). Disease-specific induced pluripotent stem cells. Cell, 134, 877-886.
81. Bergmann, O., Bhardwaj, R. D., Bernard, S., et al. (2009). Evidence for cardiomyocyte renewal in humans. Science, 324, 98-102.
82. Kubo, H., Jaleel, N., Kumarapeli, A., et al. (2008). Increased cardiac myocyte progenitors in failing human hearts. Circulation, 118, 649-657.
83. Kehat, I., Khimovich, L., Caspi, O., et al. (2004). Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nature Biotechnology, 22, 1282-1289.
84. Laflamme, M. A., Gold, J., Xu, C., et al. (2005). Formation of human myocardium in the rat heart from human embryonic stem cells. American Journal of Pathology, 167, 663-671.
85. Leor, J., Gerecht, S., Cohen, S., et al. (2007). Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart, 93, 1278-1284.
86. Caspi, O., Huber, I., Kehat, I., et al. (2007). Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. Journal of the American College of Cardiology, 50, 1884-1893.
87. van Laake, L. W., Passier, R., Monshouwer-Kloots, J., et al. (2007). Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Research, 1, 9-24.
88. van Laake LW, Passier R, den Ouden K, et al. Improvement of mouse cardiac function by hESC-derived cardiomyocytes correlates with vascularity but not graft size. Stem Cell Res 2009.
89. Stevens, K. R., Pabon, L., Muskheli, V., & Murry, C. E. (2009). Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Engineering: Part A, 15, 1211-1222.
90. Stevens, K. R., Kreutziger, K. L., Dupras, S. K., et al. (2009). Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proceedings of the National Academy of Sciences of the United States of America, 106, 16568-16573.
91. 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, 408-416.
92. Messina, E., De Angelis, L., Frati, G., et al. (2004). Isolation and expansion of adult cardiac stem cells from human and murine heart. Circulation Research, 95, 911-921.
93. Bearzi, C., Rota, M., Hosoda, T., et al. (2007). Human cardiac stem cells. Proceedings of the National Academy of Sciences of the United States of America, 104, 14068-14073.
94. Laugwitz, K. L., Moretti, A., Lam, J., et al. (2005). Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature, 433, 647-653.
95. van Vliet, P., Roccio, M., Smits, A. M., et al. (2008). Progenitor cells isolated from the human heart: a potential cell source for regenerative therapy. Netherlands Heart Journal, 16, 163-169.
96. Martin, C. M., Meeson, A. P., Robertson, S. M., et al. (2004). Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Developmental Biology, 265, 262-275.
97. Reinecke, H., Zhang, M., Bartosek, T., & Murry, C. E. (1999). Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation, 100, 193-202.
98. Chen, S., Zhang, Q., Wu, X., Schultz, P. G., & Ding, S. (2004). Dedifferentiation of lineage-committed cells by a small molecule. Journal of the American Chemical Society, 126, 410-411.
99. Thomas, R. J., Anderson, D., Chandra, A., et al. (2009). Automated, scalable culture of human embryonic stem cells in feeder-free conditions. Biotechnology and Bioengineering, 102, 1636-1644.
100. Goswami, J., & Rao, M. (2007). Embryonic stem cell therapy. IDrugs, 10, 713-719.