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J. Biol. Chem., Vol. 281, Issue 21, 14882-14892, May 26, 2006

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p204 Is Required for the Differentiation of P19 Murine Embryonal Carcinoma Cells to Beating Cardiac Myocytes

ITS EXPRESSION IS ACTIVATED BY THE CARDIAC GATA4, NKX2.5, AND TBX5 PROTEINS^*

Bo Ding, Chuan-ju Liu, Yan Huang^¶, Reed P. Hickey^¶, Jin Yu, Weihua Kong, and Peter Lengyel¹

From the Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520-8024, the Department of Orthopedic Surgery and Cell Biology, New York University School of Medicine, New York, New York 10003, and the ^¶Department of Internal Medicine, Cardiology, Yale University School of Medicine, New Haven, Connecticut 06520-8024

Among 10 adult mouse tissues tested, the p204 protein levels were highest in heart and skeletal muscle. We described previously that the MyoD-inducible p204 protein is required for the differentiation of cultured murine C2C12 skeletal muscle myoblasts to myotubes. Here we report that p204 was also required for the differentiation of cultured P19 murine embryonal carcinoma stem cells to beating cardiac myocytes. As shown by others, this process can be triggered by dimethyl sulfoxide (DMSO). We established that DMSO induced the formation of 204RNA and p204. Ectopic p204 could partially substitute for DMSO in inducing differentiation, whereas ectopic 204 antisense RNA inhibited the differentiation. Experiments with reporter constructs, including regulatory regions from the Ifi204 gene (encoding p204) in P19 cells and in cultured newborn rat cardiac myocytes, as well as chromatin coimmunoprecipitations with transcription factors, revealed that p204 expression was synergistically transactivated by the cardiac Gata4, Nkx2.5, and Tbx5 transcription factors. Furthermore, ectopic p204 triggered the expression of Gata4 and Nkx2.5 in P19 cells. p204 contains a nuclear export signal and was partially translocated to the cytoplasm during the differentiation. p204 from which the nuclear export signal was deleted was not translocated, and it did not induce differentiation. The various mechanisms by which p204 promoted the differentiation are reported in the accompanying article (Ding, B., Liu, C., Huang, Y., Yu, J., Kong, W., and Lengyel, P. (2006) J. Biol. Chem. 281, 14893-14906).

Received for publication, October 31, 2005 , and in revised form, February 15, 2006.

^* This work was supported by NIAID Research Grant AI-12320 from the National Institutes of Health. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplement M, Fig. S1, and Videos 1 and 2.

¹ To whom correspondence should be addressed: Dept. of Molecular Biophysics and Biochemistry, Yale University, 333 Cedar St., New Haven, CT 06520-8024. Tel.: 203-737-2061; Fax: 203-785-7979; E-mail: peter.lengyel{at}yale.edu.

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