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J. Biol. Chem., Vol. 281, Issue 29, 20233-20241, July 21, 2006

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The Microphthalmia-associated Transcription Factor Requires SWI/SNF Enzymes to Activate Melanocyte-specific Genes^*

Ivana L. de la Serna¹, Yasuyuki Ohkawa, Chiduru Higashi^¶, Chaitali Dutta, Jules Osias, Naveen Kommajosyula, Taro Tachibana^¶, and Anthony N. Imbalzano

From the Department of Cell Biology, University of Massachusetts Medical School, Worcester, Massachusetts 01655, the Department of Biochemistry and Cancer Biology, Medical University of Ohio, Toledo, Ohio 43614, and the ^¶Department of Bioengineering, Osaka City University, Osaka 558-8585, Japan

The microphthalmia transcription factor (Mitf) activates melanocyte-specific gene expression, is critical for survival and proliferation of melanocytes during development, and has been described as an oncogene in malignant melanoma. SWI/SNF complexes are ATP-dependent chromatin-remodeling enzymes that play a role in many developmental processes. To determine the requirement for SWI/SNF enzymes in melanocyte differentiation, we introduced Mitf into fibroblasts that inducibly express dominant negative versions of the SWI/SNF ATPases, Brahma or Brahma-related gene 1 (BRG1). These dominant negative SWI/SNF components have been shown to inhibit gene activation events that normally require SWI/SNF enzymes. We found that Mitf-mediated activation of a subset of endogenous melanocyte-specific genes required SWI/SNF enzymes but that cell-cycle regulation occurred independently of SWI/SNF function. Activation of tyrosinase-related protein 1, a melanocyte-specific gene, correlated with SWI/SNF-dependent changes in chromatin accessibility at the endogenous locus. Both BRG1 and Mitf could be localized to the tyrosinase-related protein 1 and tyrosinase promoters by chromatin immunoprecipitation, whereas immunofluorescence and immunoprecipitation experiments indicate that Mitf and BRG1 co-localized in the nucleus and physically interacted. Together these results suggest that Mitf can recruit SWI/SNF enzymes to melanocyte-specific promoters for the activation of gene expression via induced changes in chromatin structure at endogenous loci.

Received for publication, November 8, 2005 , and in revised form, April 13, 2006.

^* This work was funded by an American Heart Association Scientist Development Grant and by a grant from the Medical Foundation through support from the June Rockwell Levy Foundation and the Charles A. King Trust (to I. L. D.), and by National Institutes of Health Grant GM56244 and a Scholar Award from the Leukemia and Lymphoma Society (to A. N. I.). Fluorescence-activated cell sorting core resources were supported in part by the University of Massachusetts Medical School Diabetes Endocrinology Research Center (Grant DK32520). 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 Biochemistry and Cancer Biology, Medical University of Ohio, 3035 Arlington Ave., Toledo, OH 43614-5804. Tel.: 419-383-4111; Fax: 419-383-6228; E-mail: idelaserna{at}meduohio.edu.

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