Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK

Differentiation

Volumn 76, Issue 4, 2008, Pages 357-370

  Graichen, Ralph ^a   Xu, Xiuqin ^a   Braam, Stefan R ^b   Balakrishnan, Thavamalar ^a   Norfiza, Siti ^a   Sieh, Shirly ^a   Soo, Set Yen ^a   Tham, Su Chin ^a   Mummery, Christine ^b   Colman, Alan ^a   Zweigerdt, Robert ^a   Davidson, Bruce P ^a  

^a ES Cell International   (Singapore)

^b HUBRECHT INSTITUTE   (Netherlands)

Author keywords

Cardiomyocytes; Embryoid bodies; END2; hESC; SB203580

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AMITROLE; ANISOMYCIN; ASCORBIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; SMALL MOLECULAR INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; CULTURE MEDIUM; DRUG MECHANISM; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; HEART ELECTROPHYSIOLOGY; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MESODERM; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PATCH CLAMP; PHENOTYPE; PRIORITY JOURNAL;

EID: 42149094990     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2007.00236.x     Document Type: Article

References (53)

1. Allen, M., Svensson, L., Roach, M., Hambor, J., McNeish, J. Gabel, C.A. (2000) Deficiency of the stress kinase p38alpha results in embryonic lethality: characterization of the kinase dependence of stress responses of enzyme-deficient embryonic stem cells. J Exp Med 191 : 859 870.
2. Androutsellis-Theotokis, A., Leker, R.R., Soldner, F., Hoeppner, D.J., Ravin, R., Poser, S.W., Rueger, M.A., Bae, S.K., Kittappa, R. McKay, R.D. (2006) Notch signaling regulates stem cell numbers in vitro and in vivo. Nature 442 : 823 826.
3. Aouadi, M., Bost, F., Caron, L., Laurent, K., Le Marchand Brustel, Y. Binetruy, B. (2006) P38MAPK activity commits embryonic stem cells to either neurogenesis or cardiomyogenesis. Stem Cells 24 : 1399 1406.
4. 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.
5. Beery, R., Haimsohn, M., Wertheim, N., Hemi, R., Nir, U., Karasik, A., Kanety, H. Geier, A. (2001) Activation of the insulin-like growth factor 1 signaling pathway by the antiapoptotic agents aurintricarboxylic acid and evans blue. Endocrinology 142 : 3098 3107.
6. 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.
7. Binetruy, B., Heasley, L., Bost, F., Caron, L. Aouadi, M. (2007) Regulation of ES cell lineage commitment by mitogen activated protein kinases. Stem Cells 25 : 1090 1095.
8. Bird, S.D., Doevendans, P.A., van Rooijen, M.A., Brutel de la Riviere, A., Hassink, R.J., Passier, R. Mummery, C.L. (2003) The human adult cardiomyocyte phenotype. Cardiovasc Res 58 : 423 434.
9. Bost, F., Caron, L., Marchetti, I., Dani, C., Le Marchand-Brustel, Y. Binetruy, B. (2002) Retinoic acid activation of the ERK pathway is required for embryonic stem cell commitment into the adipocyte lineage. Biochem J 361 : 621 627.
10. Brand, T. (2003) Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol 258 : 1 19.
11. Chuva de Sousa Lopes, S.M., Hassink, R.J., Feijen, A., van Rooijen, M.A., Doevendans, P.A., Tertoolen, L., Brutel de la Riviere, A. Mummery, C.L. (2006) Patterning the heart, a template for human cardiomyocyte development. Dev Dyn 235 : 1994 2002.
12. Costa, M., Dottori, M., Ng, E., Hawes, S.M., Sourris, K., Jamshidi, P., Pera, M.F., Elefanty, A.G. Stanley, E.G. (2005) The hESC line Envy expresses high levels of GFP in all differentiated progeny. Nat Methods 2 : 259 260.
13. Cuenda, A., Rouse, J., Doza, Y.N., Meier, R., Cohen, P., Gallagher, T.F., Young, P.R. Lee, J.C. (1995) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 364 : 229 233.
14. Davidson, S.M. Morange, M. (2000) Hsp25 and the p38 MAPK pathway are involved in differentiation of cardiomyocytes. Dev Biol 218 : 146 160.
15. Denning, C., Allegrucci, C., Priddle, H., Barbadillo-Munoz, M.D., Anderson, D., Self, T., Smith, N.M., Parkin, C.T. Young, L.E. (2006) Common culture conditions for maintenance and cardiomyocyte differentiation of the human embryonic stem cell lines, BG01 and HUES-7. Int J Dev Biol 50 : 27 37.
16. Engel, F.B., Schebesta, M., Duong, M.T., Lu, G., Ren, S., Madwed, J.B., Jiang, H., Wang, Y. Keating, M.T. (2005) p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 19 : 1175 1187.
17. Gilbert, B.A., Lim, Y.H., Ding, J., Badwey, J.A. Rando, R.R. (1995) Farnesyl thiotriazole, a potent neutrophil agonist and structurally novel activator of protein kinase C. Biochemistry 34 : 3916 3920.
18. Hesse, M., Franz, T., Tamai, Y., Taketo, M.M. Magin, T.M. (2000) Targeted deletion of keratins 18 and 19 leads to trophoblast fragility and early embryonic lethality. EMBO J 19 : 5060 5070.
19. Huber, I., Itzhaki, I., Caspi, O., Arbel, G., Tzukerman, M., Gepstein, A., Habib, M., Yankelson, L., Kehat, I. Gepstein, L. (2007) Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J 21 : 2551 2563.
20. Kachinsky, A.M., Dominov, J.A. Miller, J.B. (1995) Intermediate filaments in cardiac myogenesis: nestin in the developing mouse heart. J Histochem Cytochem 43 : 843 847.
21. Kehat, I., Kenyagin-Karsenti, D., Snir, M., Segev, H., Amit, M., Gepstein, A., Livne, E., Binah, O., Itskovitz-Eldor, J. Gepstein, L. (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108 : 407 414.
22. Kupperman, E., An, S., Osborne, N., Waldron, S. Stainier, D.Y. (2000) A sphingosine-1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 406 : 192 195.
23. Lee, J.C., Laydon, J.T., McDonnell, P.C., Gallagher, T.F., Kumar, S., Green, D., McNulty, D., Blumenthal, M.J., Heys, J.R., Landvatter, S.W., Strickler, J.E., McLaughlin, M.M., Siemens, I.R., Fisher, S.M., Livi, G.P., White, J.R., Adams, J.L. Young, P.R 1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372 : 739 7346.
24. Leor, J., Patterson, M., Quinones, M.J., Kedes, L.H. Kloner, R.A. (1996) Transplantation of fetal myocardial tissue into the infracted myocardium of rat. A potential method for repair of infarcted myocardium? Circulation 94 : II332 II336.
25. Liu, Y., Asakura, M., Inoue, H., Nakamura, T., Sano, M., Niu, Z., Chen, M., Schwartz, R.J. Schneider, M.D. (2007) Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells. Proc Natl Acad Sci USA 104 : 3859 3864.
26. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 : 402 408.
27. Moore, J.C., van Laake, L.W., Braam, S.R., Xue, T., Tsang, S.Y., Ward, D., Passier, R., Tertoolen, L.L., Li, R.A. Mummery, C.L. (2005) Human embryonic stem cells: genetic manipulation on the way to cardiac cell therapies. Reprod Toxicol 20 : 377 391.
28. 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, A.B., Passier, R. Tertoolen, L. (2003) Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107 : 2733 2740.
29. Mummery, C.L., van Achterberg, T.A., van den Eijnden-van Raaij, A.J., van Haaster, L., Willemse, A., de Laat, S.W. Piersma, A.H. (1991) Visceral-endoderm-like cell lines induce differentiation of murine P19 embryonal carcinoma cells. Differentiation 46 : 51 60.
30. Murry, C.E., Soonpaa, M.H., Reinecke, H., Nakajima, H., Nakajima, H.O., Rubart, M., Pasumarthi, K.B., Virag, J.I., Bartelmez, S.H., Poppa, V., Bradford, G., Dowell, J.D., Williams, D.A. Field, L.J. (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428 : 664 668.
31. Nir, S.G., David, R., Zaruba, M., Franz, W.M. Itskovitz-Eldor, J. (2003) Human embryonic stem cells for cardiovascular repair. Cardiovasc Res 58 : 313 323.
32. Passier, R., Oostwaard, D.W., Snapper, J., Kloots, J., Hassink, R.J., Kuijk, E., Roelen, B., de la Riviere, A.B. Mummery, C. (2005) Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 23 : 772 780.
33. Perdiguero, E., Ruiz-Bonilla, V., Gresh, L., Hui, L., Ballestar, E., Sousa-Victor, P., Baeza-Raja, B., Jardi, M., Bosch-Comas, A., Esteller, M., Caelles, C., Serrano, A.L., Wagner, E.F. Munoz-Canoves, P. (2007) Genetic analysis of p38 MAP kinases in myogenesis: fundamental role of p38alpha in abrogating myoblast proliferation. EMBO J 26 : 1245 1256.
34. Qu, Y., Rogers, J., Tanada, T., Scheuer, T. Catterall, W.A. (1994) Modulation of cardiac Na+ channels expressed in a mammalian cell line and in ventricular myocytes by protein kinase C. Proc Natl Acad Sci USA 91 : 3289 3293.
35. Reppel, M., Boettinger, C. Hescheler, J. (2004) Beta-adrenergic and muscarinic modulation of human embryonic stem cell-derived cardiomyocytes. Cell Physiol Biochem 14 : 187 196.
36. Reubinoff, B.E., Pera, M.F., Fong, C.Y., Trounson, A. Bongso, A. (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18 : 399 404.
37. Rochat, A., Fernandez, A., Vandromme, M., Moles, J.P., Bouschet, T., Carnac, G. Lamb, N.J. (2004) Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol Biol Cell 15 : 4544 4555.
38. Rubart, M., Pasumarthi, K.B., Nakajima, H., Soonpaa, M.H., Nakajima, H.O. Field, L.J. (2003) Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res 92 : 1217 1224.
39. Saga, Y., Kitajima, S. Miyagawa-Tomita, S. (2000) Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc Med 10 : 345 352.
40. Sauer, H., Rahimi, G., Hescheler, J. Wartenberg, M. (2000) Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells. FEBS Lett 476 : 218 223.
41. Schroeder, M., Niebruegge, S., Werner, A., Willbold, E., Burg, M., Ruediger, M., Field, L.J., Lehmann, J. Zweigerdt, R. (2005) Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol Bioeng 92 : 920 933.
42. Takahashi, T., Lord, B., Schulze, P.C., Fryer, R.M., Sarang, S.S., Gullans, S.R. Lee, R.T. (2003) Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107 : 1912 1916.
43. Tam, P.P. Behringer, R.R. (1997) Mouse gastrulation: the formation of a mammalian body plan. Mech Dev 68 : 3 25.
44. 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.
45. Ueyama, T., Kasahara, H., Ishiwata, T., Nie, Q. Izumo, S. (2003) Myocardin expression is regulated by Nkx2.5, and its function is required for cardiomyogenesis. Mol Cell Biol 23 : 9222 9232.
46. van Laake, L.W., Hassink, R., Doevendans, P.A. Mummery, C. (2006) Heart repair and stem cells. J Physiol 577 : 467 478.
47. van Vliet, P., Sluijter, J.P., Doevendans, P.A. Goumans, M.J. (2007) Isolation and expansion of resident cardiac progenitor cells. Expert Rev Cardiovasc Ther 5 : 33 43.
48. 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 Dev 15 : 631 639.
49. Xu, C., Police, S., Rao, N. Carpenter, M.K. (2002) Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 91 : 501 508.
50. Xu, W., Zhang, X., Qian, H., Zhu, W., Sun, X., Hu, J., Zhou, H. Chen, Y. (2004) Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med 229 : 623 631.
51. Xue, T., Cho, H.C., Akar, F.G., Tsang, S.Y., Jones, S.P., Marban, E., Tomaselli, G.F. Li, R.A. (2005) 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 111 : 11 20.
52. Zohn, I.E., Li, Y., Skolnik, E.Y., Anderson, K.V., Han, J. Niswander, L. (2006) p38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 125 : 957 969.
53. Zweigerdt, R., Burg, M., Willbold, E., Abts, H. Ruediger, M. (2003) Generation of confluent cardiomyocyte monolayers derived from embryonic stem cells in suspension: a cell source for new therapies and screening strategies. Cytotherapy 5 : 399 413.