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J. Biol. Chem., Vol. 282, Issue 9, 6564-6570, March 2, 2007

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Myogenin and the SWI/SNF ATPase Brg1 Maintain Myogenic Gene Expression at Different Stages of Skeletal Myogenesis^*

Yasuyuki Ohkawa, Saori Yoshimura, Chiduru Higashi, Concetta G. A. Marfella, Caroline S. Dacwag, Taro Tachibana, and Anthony N. Imbalzano¹

From the Department of Cell Biology, University of Massachusetts Medical School, Worcester, Massachusetts 01655 and Department of Bioengineering, Osaka City University, Osaka 558-8585, Japan

Many studies have examined transcriptional regulation during the initiation of skeletal muscle differentiation; however, there is less information regarding transcriptional control during adult myogenesis and during the maintenance of the differentiated state. MyoD and the mammalian SWI/SNF chromatin-remodeling enzymes containing the Brg1 ATPase are necessary to induce myogenesis in cell culture models and in developing embryonic tissue, whereas myogenin and Brg1 are critical for the expression of the late genes that induce terminal muscle differentiation. Here, we demonstrate that myogenin also binds to its own promoter during the late stages of embryonic muscle development. As is the case during embryonic myogenesis, MyoD and Brg1 co-localize to the myogenin promoter in primary adult muscle satellite cells. However, in mature myofibers, myogenin and Brg1 are preferentially co-localized to the myogenin promoter. Thus, the myogenin promoter is occupied by different myogenic factors at different times of myogenesis. The relevance of myogenin in the continued expression from its own promoter is demonstrated in culture, where we show that myogenin, in the absence of MyoD, is capable of maintaining its own expression by recruiting the Brg1 ATPase to modify promoter chromatin structure and facilitate myogenin expression. Finally, we utilized in vivo electroporation to demonstrate that Brg1 is required for the continued production of the myogenin protein in newborn skeletal muscle tissue. These findings strongly suggest that the skeletal muscle phenotype is maintained by myogenin and the continuous activity of Brg1-based SWI/SNF chromatin-remodeling enzymes.

Received for publication, September 18, 2006 , and in revised form, December 21, 2006.

^* This work was supported by National Institutes of Health Grant GM56244 (to A. N. I.). 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.

¹ To whom correspondence should be addressed: Dept. of Cell Biology, University of Massachusetts Medical School, 55 Lake Ave. North, Worcester, MA 01655. Tel.: 508-856-1029; Fax: 508-856-5612; E-mail: anthony.imbalzano{at}umassmed.edu.

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