Embryonic stem cells and cardiomyocyte differentiation: Phenotypic and molecular analyses

Journal of Cellular and Molecular Medicine

Volumn 9, Issue 4, 2005, Pages 804-817

  Wei, Hong ^a   Juhasz, Ondrej ^a   Li, Jinliang ^a   Tarasova, Yelena S ^a   Boheler, Kenneth R ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Cardiomyocytes; Differentiation; Embryonic stem cells; Human; Mouse

Indexed keywords

EID: 30944455061     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2005.tb00381.x     Document Type: Review

References (76)

1. Boheler KR, Fiszman M. Can exogenous stem cells be used in transplantation? Cells Tissues Organs 1999; 165: 237-45.
2. Caspi O, Gepstein L. Potential applications of human embryonic stem cell-derived cardiomyocytes. Ann N Y Acad Sci. 2004; 1015: 285-98.
3. Boheler KR, Czyz J, Tweedie D, Yang HT, Anisimov SV, Wobus AM. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res. 2002; 91: 189-201.
4. Kehat I, Gepstein L. Human embryonic stem cells for myocardial regeneration. Heart Fail Rev. 2003; 8: 229-36.
5. Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev. 2005; 85: 635-78.
6. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292: 154-6.
7. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA. 1981; 78: 7634-8.
8. Burdon T, Chambers I, Stracey C, Niwa H, Smith A. Signaling mechanisms regulating self-renewal and differentiation of pluripotent embryonic stem cells. Cells Tissues Organs 1999; 165: 131-43.
9. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, Carpenter MK. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol. 2001; 19:971-974.
10. Solter D, Knowles BB. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA 1978; 75: 5565-9.
11. Niwa H, Burdon T, Chambers I, Smith A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev. 1998; 12: 2048-60.
12. Wobus AM, Holzhausen H, Jakel P, Schoneich J. Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp Cell Res. 1984;152:212-9.
13. Niida H, Matsumoto T, Satoh H, Shiwa M, Tokutake Y, Furuichi Y, Shinkai Y. Severe growth defect in mouse cells lacking the telomerase RNA component. Nat Genet. 1998; 19: 203-6.
14. Pesce M, Anastassiadis K, Schoeler HR. Oct-4: lessons of totipotency from embryonic stem cells. Cells Tissues Organs 1999; 165: 144-52.
15. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113: 643-55.
16. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113: 631-42.
17. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282: 1145-7.
18. Amit M, Itskovitz-Eldor J. Derivation and spontaneous differentiation of human embryonic stem cells. J Anat 2002; 200: 225-32.
19. Itskovitz-Eldor J, Schuldiner M, Karsenti D, Eden A, Yanuka O, Amit M, Soreq H, Benvenisty N. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med. 2000; 6: 88-95.
20. Hwang WS, Roh SI, Lee BC, Kang SK, Kwon DK, Kim S, Kim SJ, Park SW, Kwon HS, Lee CK, Lee JB, Kim JM, Ahn C, Paek SH, Chang SS, Koo JJ, Yoon HS, Hwang JH, Hwang YY, Park YS, Oh SK, Kim HS, Park JH, Moon SY, Schatten G Patient-specific embryonic stem cells derived from human SCNT blastocysts. Science 2005; 308: 1777-83.
21. Snir M, Kehat I, Gepstein A, Coleman R, Itskovitz-Eldor J, Livne E, Gepstein L. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol. 2003; 285: H2355-63.
22. Sjogren-Jansson E, Zetterstrom M, Moya K, Lindqvist J, Strehl R, Eriksson PS. Large-scale propagation of four undifferentiated human embryonic stem cell lines in a feeder-free culture system. Dev Dyn. 2005; 233: 1304-14.
23. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol. 1985; 87: 27-45.
24. Fijnvandraat AC, van Ginneken AC, de Boer PA, Ruijter JM, Christoffels VM, Moorman AF, Lekanne Deprez RH. Cardiomyocytes derived from embryonic stem cells resemble cardiomyocytes of the embryonic heart tube. Cardiovasc Res. 2003; 58: 399-409.
25. Fijnvandraat AC, van Ginneken AC, Schumacher CA, Boheler KR, Lekanne Deprez RH, Christoffels VM, Moorman AF. Cardiomyocytes purified from differentiated embryonic stem cells exhibit characteristics of early chamber myocardium. J Mol Cell Cardiol. 2003; 35: 1461-72.
26. Metzger JM, Lin W-I, Samuelson LC. Vital staining of cardiac myocytes during embryonic stem cell cardiogenesis in vitro. Circ Res. 1996; 78: 547-52.
27. Metzger JM, Samuelson LC, Rust EM, Westfall MV. Embryonic stem cell cardiogenesis: Applications for cardiovascular research. Trends Cardiovasc Med. 1997; 7: 63-8.
28. Hescheler J, Fleischmann BK, Wartenberg M, Bloch W, Kolossov E, Ji G, Addicks K, Sauer H. Establishment of ionic channels and signalling cascades in the embryonic stem cell-derived primitive endoderm and cardiovascular system. Cells Tissues Organs 1999; 165: 153-64.
29. 2+ current in the early stages of cardiomyocyte development. Circ Res. 1999; 84: 136-45.
30. Klug MG Soonpaa MH, Field LJ. DNA synthesis and multinucleation in embryonic stem cell-derived cardiomyocytes. Am J Physiol. 1995; 269: H1913-21.
31. Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere AB, Passier R, Tertoolen L. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 2003; 107: 2733-40.
32. Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest. 2001;108: 407-14.
33. Odorico JS, Kaufman DS, Thomson JA. Multilineage differentiation from human embryonic stem cell lines. Stem Cells 2001; 19: 193-204.
34. Xu RH, Chen X, Li DS, Li R, Addicks GC, Glennon C, Zwaka TP, Thomson JA. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol. 2002; 20: 1261-4.
35. Reppel M, Boettinger C, Hescheler J. β-adrenergic and muscarinic modulation of human embryonic stem cell-derived cardiomyocytes. Cell Physiol Biochem. 2004; 14: 187-96.
36. He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res. 2003; 93: 32-9.
37. Kehat I, Gepstein A, Spira A, Itskovitz-Eldor J, Gepstein L. High-resolution electrophysiological assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction. Circ Res. 2002; 91: 659-61.
38. Satin J, Kehat I, Caspi O, Huber I, Arbel G, Itzhaki I, Magyar J, Schroder EA, Perlman I, Gepstein L. Mechanism of spontaneous excitability in human embryonic stem cell-derived cardiomyocytes. J Physiol. 2004; 559: 479-96.
39. Xu C, Police S, Rao N, Carpenter MK. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res. 2002; 91: 501-8.
40. Gepstein L. Derivation and potential applications of human embryonic stem cells. Circ Res. 2002; 91: 866-76.
41. Sachinidis A, Gissel C, Nierhoff D, Hippler-Altenburg R, Sauer H, Wartenberg M, Hescheler J. Identification of plateled-derived growth factor-BB as cardiogenesis-inducing factor in mouse embryonic stem cells under serum-free conditions. Cell Physiol Biochem. 2003; 13: 423-9.
42. Zaffran S, Frasch M. Early signals in cardiac development. Circ Res. 2002; 91: 457-69.
43. Schneider MD, Gaussin V, Lyons KM. Tempting fate: BMP signals for cardiac morphogenesis. Cytokine Growth Factor Rev. 2003; 14: 1-4.
44. Johansson BM, Wiles MV. Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol Cell Biol. 1995; 15.
45. Gaussin V, Van de Putte T, Mishina Y, Hanks MC, Zwijsen A, Huylebroeck D, Behringer RR, Schneider MD. Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc Natl Acad Sci USA. 2002; 99: 2878-83.
46. Behfar A, Zingman LV, Hodgson DM, Rauzier JM, Kane GC, Terzic A, Puceat M. Stem cell differentiation requires a paracrine pathway in the heart. FASEB J. 2002; 16: 1558-66.
47. Bader A, Al-Dubai H, Weitzer G. Leukemia inhibitory factor modulates cardiogenesis in embryoid bodies in opposite fashions. Circ Res 2000; 86: 787-94.
48. Bader A, Gruss A, Hollrigl A, Al-Dubai H, Capetanaki Y, Weitzer G. Paracrine promotion of cardiomyogenesis in embryoid bodies by LIF modulated endoderm. Differentiation 2001; 68: 31-43.
49. Wobus AM, Kaomei G, Shan J, Wellner MC, Rohwedel J, Ji Guanju, Fleischmann B, Katus HA, Hescheler J, Franz WM. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol Cell Cardiol. 1997; 29: 1525-39.
50. Hidaka K, Lee JK, Kim HS, Ihm CH, Iio A, Ogawa M, Nishikawa S, Kodama I, Morisaki T. Chamber-specific differentiation of Nkx2.5-positive cardiac precursor cells from murine embryonic stem cells. FASEB J. 2003; 17: 740-2.
51. Ciccodicola A, Dono R, Obici S, Simeone A, Zollo M, Persico MG. Molecular characterization of a gene of the 'EGF family' expressed in undifferentiated human NTERA2 teratocarcinoma cells. EMBO J 1989; 8: 1987-991.
52. Xu C, Liguori G, Persico MG, Adamson ED. Abrogation of the Cripto gene in mouse leads to failure of postgastrulation morphogenesis and lack of differentiation of cardiomyocytes. Development 1999; 126: 483-94.
53. Xu C, Liguori G Adamson ED, Persico MG. Specific arrest of cardiogenesis in cultured embryonic stem cells lacking Cripto-1. Dev Biol 1998; 196: 237-47.
54. Ventura C, Zinellu E, Maninchedda E, Maioli M. Dynorphin B is an agonist of nuclear opioid receptors coupling nuclear protein kinase C activation to the transcription of cardiogenic genes in GTR1 embryonic stem cells. Circ Res. 2003; 92: 623-9.
55. Ventura C, Zinellu E, Maninchedda E, Fadda M, Maioli M. Protein kinase C signaling transduces endorphin-primed cardiogenesis in GTR1 embryonic stem cells. Circ Res. 2003; 92: 617-22.
56. Papadimou E, Menard C, Grey C, Puceat M. Interplay between the retinoblastoma protein and LEK1 specifies stem cells toward the cardiac lineage. EMBO J. 2005; 24: 1750-61.
57. Takahashi T, Lord B, Schulze PC, Fryer RM, Sarang SS, Gullans SR, Lee RT. Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 2003; 107: 1912-6.
58. Wu X, Ding S, Ding Q, Gray NS, Schultz PG Small molecules that induce cardiomyogenesis in embryonic stem cells. J Am Chem Soc. 2004; 126: 1590-1.
59. Klug MG, Soonpaa MH, Koh GY, Field LJ. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest 1996; 98: 216-24.
60. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol. 2000; 18: 399-404.
61. Henderson JK, Draper JS, Baillie HS, Fishel S, Thomson JA, Moore H, Andrews PW. Preimplantation human embryos and embryonic stem cells show comparable expression of stage-specific embryonic antigens. Stem Cells 2002; 20: 329-37.
62. Yuan H, Corbi N, Basilico C, Dailey L. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev. 1995; 9: 2635-45.
63. Ginis I, Luo Y, Miura T, Thies S, Brandenberger R, Gerecht-Nir S, Amit M, Hoke A, Carpenter MK, Itskovitz-Eldor J, Rao MS. Differences between human and mouse embryonic stem cells. Dev Biol. 2004; 269: 360-80.
64. Carpenter MK, Rosier ES, Fisk GJ, Brandenberger R, Ares X, Miura T, Lucero M, Rao MS. Properties of four human embryonic stem cell lines maintained in a feeder-free culture system. Dev Dyn. 2004; 229: 243-58.
65. Pera MF, Reubinoff B, Trounson A. Human embryonic stem cells. J Cell Sci. 2000; 113: 5-10.
66. Kania G, Corbeil D, Fuchs J, Tarasov KV, Blyszczuk P, Huttner WB, Boheler KR, Wobus AM. Somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors. Stem Cells 2005; 23: 791-804.
67. Nichols J, Davidson D, Taga T, Yoshida K, Chambers I, Smith A. Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech Dev. 1996; 57: 123-31.
68. Richards M, Tan SP, Tan JH, Chan WK, Bongso A. The transcriptome profile of human embryonic stem cells as defined by SAGE. Stem Cells 2004; 22: 51-64.
69. Ying QL, Stavridis M, Griffiths D, Li M, Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol. 2003; 21: 183-6.
70. Wobus AM, Holzhausen H, Jakel P, Schoneich J. Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp Cell Res. 1984; 152: 212-9.
71. Boheler KR, Wobus AM. Myocardial aging and stem cell biology. In: Mattson MP, van Zant G, editors. Stem Cells: A Cellular Fountain of Youth?: Elsevier Science, 2002: 141-77.
72. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotech. 2004; 22: 1282-9.
73. Xue T, Cho HC, Akar FG, Tsang SY, Jones SP, Marban E, Tomaselli GF, Li RA. Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation 2005; 111: 11-20.
74. Maitra A, Arking D E,Shivapurkar N, Ikeda M, Stastny V, Kassauei K, et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet. 2005; 37: 1099-103.
75. Segev H, Kenyagin-Karsenti D, Fishman B, Gerecht-Nir S, Ziskind A, Amit M, Coleman R, Itskovitz-Eldor J. Molecular analysis of cardiomyocytes derived from human embryonic stem cells. Develop Growth Differ. 2005; 47: 295-306.
76. Dolnikov K, Shilkrut M, Zeevi-Levin N, Danon A, Gerecht-Nir S, Itskovitz-Eldor J, Binah O. Functional properties of human embryonic stem cell-derived cardiomyocytes. Ann N Y Acad Sci 2005; 1047: 66-75.