Cardiomyocytes develop from anterior primitive streak cells induced by β-catenin activation and the blockage of BMP signaling in hESCs

Genes to Cells

Volumn 15, Issue 12, 2010, Pages 1216-1227

  Yamauchi, Kaori ^a,d   Sumi, Tomoyuki ^a   Minami, Itsunari ^b   Otsuji, Tomomi G ^b   Kawase, Eihachiro ^a   Nakatsuji, Norio ^a,c   Suemori, Hirofumi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Kyoto Research Park Building 2 Room 412   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; ALPHA ACTININ 2; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 2; MYOCYTE ENHANCER FACTOR 2; NOGGIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR TBX5;

ARTICLE; CELL AGGREGATION; CELL CULTURE; CELL DIFFERENTIATION; CELL FRACTIONATION; CLINICAL ASSESSMENT; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME PURIFICATION; GENE EXPRESSION; HEART CONTRACTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PRIMITIVE STREAK; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE;

BETA CATENIN; BONE MORPHOGENETIC PROTEINS; EMBRYONIC STEM CELLS; HUMANS; MYOCYTES, CARDIAC; PRIMITIVE STREAK; SIGNAL TRANSDUCTION;

EID: 78649704164     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2010.01455.x     Document Type: Article

References (36)

1. Alsan, B.H. & Schultheiss, T.M. (2002) Regulation of avian cardiogenesis by Fgf8 signaling. Development 129, 1935-1943.
2. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C.J., McLauchlan, H., Klevernic, I., Arthur, J.S., Alessi, D.R. & Cohen, P. (2007) The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315.
3. Cho, H., Takano, M. & Noma, A. (2003) The electrophysiological properties of spontaneously beating pacemaker cells isolated from mouse sinoatrial node. J. Physiol. 550, 169-180.
4. Cline, G.W., Johnson, K., Regittnig, W., Perret, P., Tozzo, E., Xiao, L., Damico, C. & Shulman, G.I. (2002) Effects of a novel glycogen synthase kinase-3 inhibitor on insulin-stimulated glucose metabolism in Zucker diabetic fatty (fa/fa) rats. Diabetes 51, 2903-2910.
5. Foley, A.C. & Mercola, M. (2005) Heart induction by Wnt antagonists depends on the homeodomain transcription factor Hex. Genes Dev. 19, 387-396.
6. Gadue, P., Huber, T.L., Nostro, M.C., Kattman, S. & Keller, G.M. (2005) Germ layer induction from embryonic stem cells. Exp. Hematol. 33, 955-964.
7. Hao, J., Daleo, M.A., Murphy, C.K., Yu, P.B., Ho, J.N., Hu, J., Peterson, R.T., Hatzopoulos, A.K. & Hong, C.C. (2008) Dorsomorphin, a Selective Small Molecule Inhibitor of BMP Signaling, Promotes Cardiomyogenesis in Embryonic Stem Cells. PLoS ONE 3, e2904.
8. 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. Circ. Res. 93, 32-39.
9. Kami, D., Shiojima, I., Makino, H., Matsumoto, K., Takahashi, Y., Ishii, R., Naito, A.T., Toyoda, M., Saito, H., Watanabe, M., Komuro, I. & Umezawa, A. (2008) Gremlin enhances the determined path to cardiomyogenesis. PLoS ONE 3, e2407.
10. 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.
11. Laflamme, M.A., Gold, J., Xu, C., Hassanipour, M., Rosler, E., Police, S., Muskheli, V. & Murry, C.E. (2005) Formation of human myocardium in the rat heart from human embryonic stem cells. Am. J. Pathol. 167, 663-671.
12. Lickert, H., Kutsch, S., Kanzler, B., Tamai, Y., Taketo, M.M. & Kemler, R. (2002) Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev. Cell 3, 171-181.
13. Lindsley, R.C., Gill, J.G., Kyba, M., Murphy, T.L. & Murphy, K.M. (2006) Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 33, 3787-3796.
14. MacDonald, B.T., Tamai, K. & He, X. (2009) Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
15. Martin-Puig, S., Wang, Z. & Chien, K.R. (2008) Lives of a Heart Cell: tracing the Origins of Cardiac Progenitors. Cell Stem Cell 2, 320-331.
16. 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 Dev. 15, 316-327.
17. 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.
18. Murry, C.E. & Keller, G. (2008) Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132, 661-680.
19. Olson, E.N. (2006) Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927.
20. Osafune, K., Caron, L., Borowiak, M., Martinez, R.J., Fitz-Gerald, C.S., Sato, Y., Cowan, C.A., Chien, K.R. & Melton, D.A. (2008) Marked differences in differentiation propensity among human embryonic stem cell lines. Nat. Biotechnol. 26, 313-315.
21. Paige, S.L., Osugi, T., Afanasiev, O.K., Pabon, L., Reinecke, H. & Murry, C.E. (2010) Endogenous Wnt/β-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS ONE 5, e11134.
22. Rossant, J. & Tam, P.P. (2004) Emerging asymmetry and embryonic patterning in early mouse development. Dev. Cell 7, 155-164.
23. Satin, J., Kehat, I., Caspi, O., Huber, I., Arbel, G., Itzhaki, I., Magyar, J., Schroder, E.A., Perlman, I. & Gepstein, L. (2004) Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. J. Physiol. 559, 479-496.
24. Schneider, V.A. & Mercola, M. (2001) Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 15, 304-315.
25. Schultheiss, T.M., Burch, J.B. & Lassar, A.B. (1997) A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11, 451-462.
26. Suemori, H., Yasuchika, K., Hasegawa, K., Fujioka, T., Tsuneyoshi, N. & Nakatsuji, N. (2006) Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochem. Biophys. Res. Commun. 345, 926-932.
27. Sumi, T., Tsuneyoshi, N., Nakatsuji, N. & Suemori, H. (2008) Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135, 2969-2979.
28. Takei, S., Ichikawa, H., Johkura, K., Mogi, A., No, H., Yoshie, S., Tomotsune, D. & Sasaki, K. (2009) Bone morphogenetic protein-4 promotes induction of cardiomyocytes from human embryonic stem cells in serum-based embryoid body development. Am. J. Physiol. Heart Circ. Physiol. 296, H1793-H1803.
29. Tam, P.P. & Loebel, D.A. (2007) Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 8, 368-381.
30. Tran, T.H., Wang, X., Browne, C., Zhang, Y., Schinke, M., Izumo, S. & Burcin, M. (2009) Wnt3a Induced Mesoderm Formation and Cardiomyogenesis in Human Embryonic Stem Cells. Stem Cells 27, 1869-1878.
31. Tzahor, E. & Lassar, A.B. (2001) Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev. 15, 255-260.
32. Willert, K. & Jones, K.A. (2006) Wnt signaling: is the party in the nucleus? Genes Dev. 20, 1394-1404.
33. 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.
34. Yamauchi, K., Hasegawa, K., Chuma, S., Nakatsuji, N. & Suemori, H. (2009) In vitro germ cell differentiation from cynomolgus monkey embryonic stem cells. PLoS ONE 4, e5338.
35. Yang, L., Soonpaa, M.H., Adler, E.D., Roepke, T.K., Kattman, S.J., Kennedy, M., Henckaerts, E., Bonham, K., Abbott, G.W., Linden, R.M., Field, L.J. & Keller, G.M. (2008) Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453, 524-528.
36. Yuasa, S., Itabashi, Y., Koshimizu, U., Tanaka, T., Sugimura, K., Kinoshita, M., Hattori, F., Fukami, S., Shimazaki, T., Ogawa, S., Okano, H. & Fukuda, K. (2005) Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat. Biotechnol. 23, 607-611.