Cardiac specific differentiation of mouse embryonic stem cells

Cardiovascular Research

Volumn 58, Issue 2, 2003, Pages 278-291

  Sachinidis, Agapios ^a   Fleischmann, Bernd K ^a   Kolossov, Eugen ^a   Wartenberg, Maria ^a   Sauer, Heinrich ^a   Hescheler, Jürgen ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cardiomyocytes; Embryonic stem cells; Growth factors; Signalling molecules

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BONE MORPHOGENETIC PROTEIN 2; DIMETHYL SULFOXIDE; FIBROBLAST GROWTH FACTOR; GREEN FLUORESCENT PROTEIN; IMMUNOSUPPRESSIVE AGENT; MYOSIN HEAVY CHAIN; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; SERUM RESPONSE FACTOR; SOMATOMEDIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 5; TRANSCRIPTION FACTOR GATA 6; WNT PROTEIN;

ANIMAL EMBRYO; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINE; CELL LINEAGE; CULTURE MEDIUM; DRUG TOXICITY; EMBRYO CELL; GENETIC MANIPULATION; GRAFT REJECTION; HEART DEVELOPMENT; HEART MUSCLE CELL; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOMA; NONHUMAN; OPPORTUNISTIC INFECTION; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SERUM RESPONSIVE ELEMENT; SIDE EFFECT; SIGNAL TRANSDUCTION; SKIN CANCER; STEM CELL; STEM CELL TRANSPLANTATION; WOUND HEALING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BONE MORPHOGENETIC PROTEINS; CARDIOMYOPATHIES; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; EMBRYONIC INDUCTION; GRAFT REJECTION; GROWTH SUBSTANCES; HEART; MICE; MYOBLASTS, CARDIAC; NITRIC OXIDE; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; SERUM RESPONSE FACTOR; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS; ZEBRAFISH PROTEINS;

EID: 0038030960     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(03)00248-7     Document Type: Review

References (115)

1. Delcarpio J.B., Claycomb W.C. Cardiomyocyte transfer into the mammalian heart. Cell-to-cell interactions in vivo and in vitro. Ann NY Acad Sci. 752:1995;267-285.
2. Koh G.Y., Soonpaa M.H., Klug M.G., Field L.J. Long-term survival of AT-1 cardiomyocyte grafts in syngeneic myocardium. Am J Physiol. 264:1993;H1727-1733.
3. Koh G.Y., Soonpaa M.H., Klug M.G., et al. Stable fetal cardiomyocyte grafts in the hearts of dystrophic mice and dogs. J Clin Invest. 96:1995;2034-2042.
4. Roell W., Lu Z.J., Bloch W., et al. Cellular cardiomyoplasty improves survival after myocardial injury. Circulation. 105:2002;2435-2441.
5. Muller-Ehmsen J., Peterson K.L., Kedes L., et al. Rebuilding a damaged heart: long-term survival of transplanted neonatal rat cardiomyocytes after myocardial infarction and effect on cardiac function. Circulation. 105:2002;1720-1726.
6. Odorico J.S., Kaufman D.S., Thomson J.A. Multilineage differentiation from human embryonic stem cell lines. Stem Cells. 19:2001;193-204.
7. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., et al. Embryonic stem cell lines derived from human blastocysts. Science. 282:1998;1145-1147.
8. Jacobson A.G. Influences of ectoderm and endoderm on heart differentiation in the newt. Dev Biol. 2:1960;138-154.
9. Smith A.G., Heath J.K., Donaldson D.D., et al. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature. 336:1988;688-690.
10. Itskovitz-Eldor J., Schuldiner M., Karsenti D., et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med. 6:2000;88-95.
11. Tzahor E., Lassar A.B. Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev. 15:2001;255-260.
12. Marvin M.J., Di Rocco G., Gardiner A., Bush S.M., Lassar A.B. Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev. 15:2001;316-327.
13. Antin P.B., Taylor R.G., Yatskievych T. Precardiac mesoderm is specified during gastrulation in quail. Dev Dyn. 200:1994;144-154.
14. Montgomery M.O., Litvin J., Gonzalez-Sanchez A., Bader D. Staging of commitment and differentiation of avian cardiac myocytes. Dev Biol. 164:1994;63-71.
15. Sugi Y., Lough J. Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region. Dev Dyn. 200:1994;155-162.
16. Schultheiss T.M., Xydas S., Lassar A.B. Induction of avian cardiac myogenesis by anterior endoderm. Development. 121:1995;4203-4214.
17. Schultheiss T.M., Burch J.B., Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11:1997;451-462.
18. Schlange T., Andree B., Arnold H.H., Brand T. BMP2 is required for early heart development during a distinct time period. Mech Dev. 91:2000;259-270.
19. Andree B., Duprez D., Vorbusch B., Arnold H.H., Brand T. BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech Dev. 70:1998;119-131.
20. Kazanskaya O., Glinka A., Niehrs C. The role of Xenopus dickkopf1 in prechordal plate specification and neural patterning. Development. 127:2000;4981-4992.
21. Orkin S.H. GATA-binding transcription factors in hematopoietic cells. Blood. 80:1992;575-581.
22. Simon M.C. Gotta have GATA. Nat Genet. 11:1995;9-11.
23. Zhu J., Hill R.J., Heid P.J., et al. End-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos. Genes Dev. 11:1997;2883-2896.
24. Merika M., Orkin S.H. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol. 13:1993;3999-4010.
25. Svensson E.C., Tufts R.L., Polk C.E., Leiden J.M. Molecular cloning of FOG-2: a modulator of transcription factor GATA-4 in cardiomyocytes. Proc Natl Acad Sci USA. 96:1999;956-961.
26. Lee Y., Shioi T., Kasahara H., et al. The cardiac tissue-restricted homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol Cell Biol. 18:1998;3120-3129.
27. Sepulveda J.L., Belaguli N., Nigam V., et al. GATA-4 and Nkx-2.5 coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol Cell Biol. 18:1998;3405-3415.
28. Molkentin J.D., Lu J.R., Antos C.L., et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:1998;215-228.
29. Durocher D., Charron F., Warren R., Schwartz R.J., Nemer M. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J. 16:1997;5687-5696.
30. Schott J.J., Benson D.W., Basson C.T., et al. Congenital heart disease caused by mutations in the transcription factor NKX2-5. Science. 281:1998;108-111.
31. Benson D.W., Silberbach G.M., Kavanaugh-McHugh A., et al. Mutations in the cardiac transcription factor NKX2.5 affect diverse cardiac developmental pathways. J Clin Invest. 104:1999;1567-1573.
32. Ventura C., Maioli M. Opioid peptide gene expression primes cardiogenesis in embryonal pluripotent stem cells. Circ Res. 87:2000;189-194.
33. Ko L.J., Engel J.D. DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol. 13:1993;4011-4022.
34. Wang G.F., Nikovits W. Jr., Schleinitz M., Stockdale F.E. A positive GATA element and a negative vitamin D receptor-like element control atrial chamber-specific expression of a slow myosin heavy-chain gene during cardiac morphogenesis. Mol Cell Biol. 18:1998;6023-6034.
35. Molkentin J.D., Lin Q., Duncan S.A., Olson E.N. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1997;1061-1072.
36. Kuo C.T., Morrisey E.E., Anandappa R., et al. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11:1997;1048-1060.
37. Schlange T., Arnold H.H., Brand T. BMP2 is a positive regulator of Nodal signaling during left-right axis formation in the chicken embryo. Development. 129:2002;3421-3429.
38. Piedra M.E., Ros M.A. BMP signaling positively regulates Nodal expression during left right specification in the chick embryo. Development. 129:2002;3431-3440.
39. Zhou X., Sasaki H., Lowe L., Hogan B.L., Kuehn M.R. Nodal is a novel TGF-β-like gene expressed in the mouse node during gastrulation. Nature. 361:1993;543-547.
40. Conlon F.L., Lyons K.M., Takaesu N., et al. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development. 120:1994;1919-1928.
41. Pfendler K.C., Yoon J., Taborn G.U., Kuehn M.R., Iannaccone P.M. Nodal and bone morphogenetic protein 5 interact in murine mesoderm formation and implantation. Genesis. 28:2000;1-14.
42. Lowe L.A., Yamada S., Kuehn M.R. Genetic dissection of nodal function in patterning the mouse embryo. Development. 128:2001;1831-1843.
43. Bodmer R, Frasch M. Genetic determination of Drosophila heart development. In: Rosenthal N, Harvey R, editors, Heart development, San Diego: Acadeimc Press, 1999, pp. 65-90.
44. Adamson E.D., Minchiotti G., Salomon D.S. Cripto: a tumor growth factor and more. J Cell Physiol. 190:2002;267-278.
45. Bamford R.N., Roessler E., Burdine R.D., et al. Loss-of-function mutations in the EGF-CFC gene CFC1 are associated with human left-right laterality defects. Nat Genet. 26:2000;365-369.
46. Behfar A., Zingman L.V., Hodgson D.M., et al. Stem cell differentiation requires a paracrine pathway in the heart. FASEB J. 16:2002;1558-1566.
47. Azpiazu N., Frasch M. Tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 7:1993;1325-1340.
48. Bodmer R. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development. 118:1993;719-729.
49. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature. 374:1995;464-467.
50. Su M.T., Fujioka M., Goto T., Bodmer R. The Drosophila homeobox genes zfh-1 and even-skipped are required for cardiac-specific differentiation of a numb-dependent lineage decision. Development. 126:1999;3241-3251.
51. Wakefield L.M., Roberts A.B. TGF-β signaling: positive and negative effects on tumorigenesis. Curr Opin Genet Dev. 12:2002;22-29.
52. Whitman M. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12:1998;2445-2462.
53. Powell-Braxton L., Hollingshead P., Warburton C., et al. IGF-I is required for normal embryonic growth in mice. Genes Dev. 7:1993;2609-2617.
54. Fishman M.C., Chien K.R. Fashioning the vertebrate heart: earliest embryonic decisions. Development. 124:1997;2099-2117.
55. Siddle K., Urso B., Niesler C.A., et al. Specificity in ligand binding and intracellular signalling by insulin and insulin-like growth factor receptors. Biochem Soc Trans. 29:2001;513-525.
56. Cantley L.C. The phosphoinositide 3-kinase pathway. Science. 296:2002;1655-1657.
57. Klinz F., Bloch W., Addicks K., Hescheler J. Inhibition of phosphatidylinositol-3-kinase blocks development of functional embryonic cardiomyocytes. Exp Cell Res. 247:1999;79-83.
58. Sauer H., Rahimi G., Hescheler J., Wartenberg M. Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells. FEBS Lett. 476:2000;218-223.
59. Reifers F., Walsh E.C., Leger S., Stainier D.Y., Brand M. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development. 127:2000;225-235.
60. Antin P.B., Yatskievych T., Dominguez J.L., Chieffi P. Regulation of avian precardiac mesoderm development by insulin and insulin-like growth factors. J Cell Physiol. 168:1996;42-50.
61. Powers C.J., McLeskey S.W., Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer. 7:2000;165-197.
62. Wu H., Lee S.H., Gao J., Liu X., Iruela-Arispe M.L. Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development. 126:1999;3597-3605.
63. Krantz S.B. Erythropoietin. Blood. 77:1991;419-434.
64. Ishibashi T., Koziol J.A., Burstein S.A. Human recombinant erythropoietin promotes differentiation of murine megakaryocytes in vitro. J Clin Invest. 79:1987;286-289.
65. Broudy V.C., Lin N.L., Kaushansky K. Thrombopoietin (c-mpl ligand) acts synergistically with erythropoietin, stem cell factor, and interleukin-11 to enhance murine megakaryocyte colony growth and increases megakaryocyte ploidy in vitro. Blood. 85:1995;1719-1726.
66. Papayannopoulou T., Brice M., Farrer D., Kaushansky K. Insights into the cellular mechanisms of erythropoietin-thrombopoietin synergy. Exp Hematol. 24:1996;660-669.
67. Anagnostou A., Liu Z., Steiner M., et al. Erythropoietin receptor mRNA expression in human endothelial cells. Proc Natl Acad Sci USA. 91:1994;3974-3978.
68. Yoshimura A., Misawa H. Physiology and function of the erythropoietin receptor. Curr Opin Hematol. 5:1998;171-176.
69. Cheung J.Y., Miller B.A. Molecular mechanisms of erythropoietin signaling. Nephron. 87:2001;215-222.
70. Wobus A.M., Kaomei G., Shan J., et al. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol Cell Cardiol. 29:1997;1525-1539.
71. McBurney M.W., Jones-Villeneuve E.M., Edwards M.K., Anderson P.J. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature. 299:1982;165-167.
72. Skerjanc I.S., Petropoulos H., Ridgeway A.G., Wilton S. Myocyte enhancer factor 2C and Nkx2-5 upregulate each other's expression and initiate cardiomyogenesis in P19 cells. J Biol Chem. 273:1998;34904-34910.
73. Treisman R., Marais R., Wynne J. Spatial flexibility in ternary complexes between SRF and its accessory proteins. EMBO J. 11:1992;4631-4640.
74. Weinhold B., Schratt G., Arsenian S., et al. Srf(-/-) ES cells display noncell-autonomous impairment in mesodermal differentiation. EMBO J. 19:2000;5835-5844.
75. Orsulic S., Peifer M. An in vivo structure-function study of armadillo, the β-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for wingless signaling. J Cell Biol. 134:1996;1283-1300.
76. Miller J.R., Moon R.T. Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev. 10:1996;2527-2539.
77. Moon R.T., Brown J.D., Torres M. WNTs modulate cell fate and behavior during vertebrate development. Trends Genet. 13:1997;157-162.
78. Dale T.C. Signal transduction by the Wnt family of ligands. Biochem J. 329:1998;209-223.
79. Herz J., Bock H.H. Lipoprotein receptors in the nervous system. Annu Rev Biochem. 71:2002;405-434.
80. Bhanot P., Brink M., Samos C.H., et al. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature. 382:1996;225-230.
81. Yanagawa S., van Leeuwen F., Wodarz A., Klingensmith J., Nusse R. The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 9:1995;1087-1097.
82. Eisenberg C.A., Gourdie R.G., Eisenberg L.M. Wnt-11 is expressed in early avian mesoderm and required for the differentiation of the quail mesoderm cell line QCE-6. Development. 124:1997;525-536.
83. Eisenberg C.A., Eisenberg L.M. WNT11 promotes cardiac tissue formation of early mesoderm. Dev Dyn. 216:1999;45-58.
84. Pandur P., Lasche M., Eisenberg L.M., Kuhl M. Wnt-11 activation of a noncanonical Wnt signalling pathway is required for cardiogenesis. Nature. 418:2002;636-641.
85. Krupnik V.E., Sharp J.D., Jiang C., et al. Functional and structural diversity of the human Dickkopf gene family. Gene. 238:1999;301-313.
86. Grotewold L., Ruther U. The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and c-Jun and modulates programmed cell death. EMBO J. 21:2002;966-975.
87. Kyriakis J.M., Banerjee P., Nikolakaki E., et al. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 369:1994;156-160.
88. Sauer H., Wartenberg M., Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem. 11:2001;173-186.
89. Tanaka K., Honda M., Takabatake T. Redox regulation of MAPK pathways and cardiac hypertrophy in adult rat cardiac myocyte. J Am Coll Cardiol. 37:2001;676-685.
90. Nakamura K., Fushimi K., Kouchi H., et al. Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-α and angiotensin II. Circulation. 98:1998;794-799.
91. Sorescu D., Griendling K.K. Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail. 8:2002;132-140.
92. Li J.M., Gall N.P., Grieve D.J., Chen M., Shah A.M. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertension. 40:2002;477-484.
93. Zhan Y., Virbasius J.V., Song X., Pomerleau D.P., Zhou G.W. The p40phox and p47phox PX domains of NADPH oxidase target cell membranes via direct and indirect recruitment by phosphoinositides. J Biol Chem. 277:2002;4512-4518.
94. Sauer H., Rahimi G., Hescheler J., Wartenberg M. Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J Cell Biochem. 75:1999;710-723.
95. Bloch W., Fleischmann B.K., Lorke D.E., et al. Nitric oxide synthase expression and role during cardiomyogenesis. Cardiovasc Res. 43:1999;675-684.
96. 2+ channel blockers. Differentiation. 48:1991;173-182.
97. Maltsev V.A., Wobus A.M., Rohwedel J., Bader M., Hescheler J. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ Res. 75:1994;233-244.
98. Hescheler J., Fleischmann B.K., Lentini S., et al. Embryonic stem cells: a model to study structural and functional properties in cardiomyogenesis. Cardiovasc Res. 36:1997;149-162.
99. 2+ channel during cardiomyogenesis: switch from NO to adenylyl cyclase-mediated inhibition. FASEB J. 13:1999;313-324.
100. Fischmeister R., Hartzell H.C. Mechanism of action of acetylcholine on calcium current in single cells from frog ventricle. J Physiol. 376:1986;183-202.
101. Hescheler J., Kameyama M., Trautwein W. On the mechanism of muscarinic inhibition of the cardiac Ca current. Pflugers Arch. 407:1986;182-189.
102. Peunova N., Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature. 375:1995;68-73.
103. Kuzin B., Roberts I., Peunova N., Enikolopov G. Nitric oxide regulates cell proliferation during Drosophila development. Cell. 87:1996;639-649.
104. Abi-Gerges N., Ji G.J., Lu Z.J., et al. Functional expression and regulation of the hyperpolarisation activated nonselective cation current in embryonic stem cell-derived cardiomyocytes. J Physiol. 523:(Pt 2):2000;377-389.
105. Kolossov E., Fleischmann B.K., Liu Q., et al. Functional characteristics of ES cell-derived cardiac precursor cells identified by tissue-specific expression of the green fluorescent protein. J Cell Biol. 143:1998;2045-2056.
106. Gryschenko O., Lu Z.J., Fleischmann B.K., Hescheler J. Outwards currents in embryonic stem cell-derived cardiomyocytes. Pflugers Arch. 439:2000;798-807.
107. 2+ oscillations drive spontaneous contractions in cardiomyocytes during early development. Proc Natl Acad Sci USA. 96:1999;8259-8264.
108. Opie L.H., Clusin W.T. Cellular mechanism for ischemic ventricular arrhythmias. Annu Rev Med. 41:1990;231-238.
109. Maltsev V.A., Rohwedel J., Hescheler J., Wobus A.M. Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev. 44:1993;41-50.
110. Wobus A.M., Rohwedel J., Maltsev V., Hescheler J. Development of cardiomyocytes expressing cardiac-specific genes, action potentials, and ionic channels during embryonic stem cell-derived cardiogenesis. Ann NY Acad Sci. 752:1995;460-469.
111. Muller M., Fleischmann B.K., Selbert S., et al. Selection of ventricular-like cardiomyocytes from ES cells in vitro. FASEB J. 14:2000;2540-2548.
112. Robbins J. Altering cardiac functions via transgenesis. Trends Cardiovasc Med. 7:1997;185-191.
113. Wartenberg M., Gunther J., Hescheler J., Sauer H. The embryoid body as a novel in vitro assay system for antiangiogenic agents. Lab Invest. 78:1998;1301-1314.
114. Klug M.G., Soonpaa M.H., Koh G.Y., Field L.J. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest. 98:1996;216-224.
115. Grusby M.J., Auchincloss H. Jr., Lee R., et al. Mice lacking major histocompatibility complex class I and class II molecules. Proc Natl Acad Sci USA. 90:1993;3913-3917.