Neuregulin-1β induces embryonic stem cell cardiomyogenesis via ErbB3/ErbB2 receptors

Biochemical Journal

Volumn 458, Issue 2, 2014, Pages 335-341

  Hao, Jijun ^a,b   Galindo, Cristi L ^b   Tran, Truc Linh ^b   Sawyer, Douglas B ^b  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac differentiation; ErbB3; ErbB4; Mouse embryonic stem cell; Neuregulin 1 (NRG 1 ); Signalling

Indexed keywords

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EMBRYONIC STEM CELLS; GENE KNOCKDOWN TECHNIQUES; MICE; MYOCYTES, CARDIAC; NERVE TISSUE PROTEINS; NEUREGULIN-1; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84894286214     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130818     Document Type: Article

References (37)

1. Hao, J. J., Daleo, M. A., Murphy, C. K., Yu, P. B., Ho, J. N., Hu, J. Y., Peterson, R. T., Hatzopoulos, A. K. and Hong, C. C. (2008) Dorsomorphin, a selective small molecule inhibitor of BMP signaling, promotes cardiomyogenesis in embryonic stem cells. PLoS ONE 3, e2904
2. Ao, A., Hao, J. J., Hopkins, C. R. and Hong, C. C. (2012) DMH1, a novel BMP small molecule inhibitor, increases cardiomyocyte progenitors and promotes cardiac differentiation in mouse embryonic stem cells. PLoS ONE 7, e41627
3. Wang, H. M., Hao, J. J. and Hong, C. C. (2011) Cardiac induction of embryonic stem cells by a small molecule inhibitor of Wnt/β-catenin signaling. ACS Chem. Biol. 6, 192-197
4. Brutsaert, D. L. (2003) Cardiac endothelial-myocardial signaling: its role in cardiac growth, contractile performance, and rhythmicity. Physiol. Rev. 83, 59-115
5. Cote, G. M., Miller, T. A., Lebrasseur, N. K., Kuramochi, Y. and Sawyer, D. B. (2005) Neuregulin-1α and β isoform expression in cardiac microvascular endothelial cells and function in cardiac myocytes in vitro. Exp. Cell Res. 311, 135-146
6. Gassmann, M., Casagranda, F., Orioli, D., Simon, H., Lai, C., Klein, R. and Lemke, G. (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390-394
7. Meyer, D. and Birchmeier, C. (1995) Multiple essential functions of neuregulin in development. Nature 378, 386-390
8. Lee, K. F., Simon, H., Chen, H., Bates, B., Hung, M. C. and Hauser, C. (1995) Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378, 394-398
9. Rentschler, S., Zander, J., Meyers, K., France, D., Levine, R., Porter, G., Rivkees, S. A., Morley, G. E. and Fishman, G. I. (2002) Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc. Natl. Acad. Sci. U.S.A. 99, 10464-10469
10. Zeisberg, E. M., Tarnavski, O., Zeisberg, M., Dorfman, A. L., McMullen, J. R., Gustafsson, E., Chandraker, A., Yuan, X., Pu, W. T., Roberts, A. B. et al. (2007) Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med. 13, 952-961
11. Pentassuglia, L. and Sawyer, D. B. (2009) The role of Neuregulin-1β/ErbB signaling in the heart. Exp. Cell Res. 315, 627-637
12. Lee, K. F., Simon, H., Chen, H., Bates, B., Hung, M. C. and Hauser, C. (1995) Requirement for neuregulin receptor Erbb2 in neural and cardiac Development. Nature 378, 394-398
13. Erickson, S. L., O'Shea, K. S., Ghaboosi, N., Loverro, L., Frantz, G., Bauer, M., Lu, L. H. and Moore, M. W. (1997) ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124, 4999-5011
14. Zhao, Y. Y., Sawyer, D. R., Baliga, R. R., Opel, D. J., Han, X., Marchionni, M. A. and Kelly, R. A. (1998) Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J. Biol. Chem. 273, 10261-10269
15. Fukazawa, R., Miller, T. A., Kuramochi, Y., Frantz, S., Kim, Y. D., Marchionni, M. A., Kelly, R. A. and Sawyer, D. B. (2003) Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J. Mol. Cell. Cardiol. 35, 1473-1479
16. Baliga, R. R., Pimental, D. R., Zhao, Y. Y., Simmons, W. W., Marchionni, M. A., Sawyer, D. B. and Kelly, R. A. (1999) NRG-1-induced cardiomyocyte hypertrophy. Role of PI-3-kinase, p70(S6K), and MEK-MAPK-RSK. Am. J. Physiol. 277, H2026-H2037
17. Kuramochi, Y., Cote, G. M., Guo, X., Lebrasseur, N. K., Cui, L., Liao, R. and Sawyer, D. B. (2004) Cardiac endothelial cells regulate reactive oxygen species-induced cardiomyocyte apoptosis through neuregulin-1β/erbB4 signaling. J. Biol. Chem. 279, 51141-51147
18. Lemmens, K., Fransen, P., Sys, S. U., Brutsaert, D. L. and De Keulenaer, G. W. (2004) Neuregulin-1 induces a negative inotropic effect in cardiac muscle: role of nitric oxide synthase. Circulation 109, 324-326
19. Bersell, K., Arab, S., Haring, B. and Kuhn, B. (2009) Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 138, 257-270
20. Wadugu, B. and Kuhn, B. (2012) The role of neuregulin/ErbB2/ErbB4 signaling in the heart with special focus on effects on cardiomyocyte proliferation. Am. J. Physiol. Heart Circ. Physiol. 302, H2139-H2147
21. Jabbour, A., Hayward, C. S., Keogh, A. M., Kotlyar, E., McCrohon, J. A., England, J. F., Amor, R., Liu, X., Li, X. Y., Zhou, M. D. et al. (2011) Parenteral administration of recombinant human neuregulin-1 to patients with stable chronic heart failure produces favourable acute and chronic haemodynamic responses. Eur. J. Heart Fail. 13, 83-92
22. Gao, R., Zhang, J., Cheng, L., Wu, X., Dong, W., Yang, X., Li, T., Liu, X., Xu, Y., Li, X. and Zhou, M. (2010) A Phase II, randomized, double-blind, multicenter, based on standard therapy, placebo-controlled study of the efficacy and safety of recombinant human neuregulin-1 in patients with chronic heart failure. J. Am. Coll. Cardiol. 55, 1907-1914
23. Suk Kim, H., Hidaka, K. and Morisaki, T. (2003) Expression of ErbB receptors in ES cell-derived cardiomyocytes. Biochem. Biophys. Res. Commun. 309, 241-246
24. Sun, M., Yan, X., Bian, Y., Caggiano, A. O. and Morgan, J. P. (2011) Improving murine embryonic stem cell differentiation into cardiomyocytes with neuregulin-1: differential expression of microRNA. Am. J. Physiol. Cell. Physiol. 301, C21-C30
25. Wang, Z., Xu, G., Wu, Y., Guan, Y., Cui, L., Lei, X., Zhang, J., Mou, L., Sun, B. and Dai, Q. (2009) Neuregulin-1 enhances differentiation of cardiomyocytes from embryonic stem cells. Med. Biol. Eng. Comput. 47, 41-48
26. Bolstad, B. M., Irizarry, R. A., Astrand, M. and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193
27. Kattman, S. J., Adler, E. D. and Keller, G. M. (2007) Specification of multipotential cardiovascular progenitor cells during embryonic stem cell differentiation and embryonic development. Trends Cardiovasc. Med. 17, 240-246
28. Du, K. Y. and Montminy, M. (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273, 32377-32379
29. Giachino, C., De Marchis, S., Giampietro, C., Parlato, R., Perroteau, I., Schutz, G., Fasolo, A. and Peretto, P. (2005) cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J. Neurosci. 25, 10105-10118
30. Cheng, J. C., Kinjo, K., Judelson, D. R., Chang, J., Wu, W. S., Schmid, I., Shankar, D. B., Kasahara, N., Stripecke, R., Bhatia, R. et al. (2008) CREB is a critical regulator of normal hematopoiesis and leukemogenesis. Blood 111, 1182-1192
31. Bleckmann, S. C., Blendy, J. A., Rudolph, D., Monaghan, A. P., Schmid, W. and Schutz, G. (2002) Activating transcription factor 1 and CREB are important for cell survival during early mouse development. Mol. Cell. Biol. 22, 1919-1925
32. Li, X. Y., Zhan, X. R., Liu, X. M. and Wang, X. C. (2011) CREB is a regulatory target for the protein kinase Akt/PKB in the differentiation of pancreatic ductal cells into islet β-cells mediated by hepatocyte growth factor. Biochem. Biophys Res. Commun. 404, 711-716
33. Zhao, Y. Y., Sawyer, D. R., Baliga, R. R., Opel, D. J., Han, X. Q., Marchionni, M. A. and Kelly, R. A. (1998) Neuregulins promote survival and growth of cardiac myocytes: persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J. Biol. Chem. 273, 10261-10269
34. Fentzke, R. C., Korcarz, C. E., Lang, R. M., Lin, H. and Leiden, J. M. (1998) Dilated cardiomyopathy in transgenic mice expressing a dominant-negative CREB transcription factor in the heart. J. Clin. Invest. 101, 2415-2426
35. Meng, F. J., Jiao, S. M. and Yu, B. (2012) Picroside II protects cardiomyocytes from hypoxia/reoxygenation-induced apoptosis by activating the PI3K/Akt and CREB pathways. Int. J. Mol. Med. 30, 263-270
36. Watson, P. A., Reusch, J. E. B., McCune, S. A., Leinwand, L. A., Luckey, S. W., Konhilas, J. P., Brown, D. A., Chicco, A. J., Sparagna, G. C., Long, C. S. and Moore, R. L. (2007) Restoration of CREB function is linked to completion and stabilization of adaptive cardiac hypertrophy in response to exercise. Am. J. Physiol. Heart Circ. Physiol. 293, H246-H259
37. Zhu, W. Z., Xie, Y., Moyes, K. W., Gold, J. D., Askari, B. and Laflamme, M. A. (2010) Neuregulin/ErbB signaling regulates cardiac subtype specification in differentiating human embryonic stem cells. Circ. Res. 107, 776-786