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J. Biol. Chem., Vol. 281, Issue 32, 22695-22706, August 11, 2006

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Chromatin Remodeling and Transcriptional Activity of the Bone-specific Osteocalcin Gene Require CCAAT/Enhancer-binding Protein -dependent Recruitment of SWI/SNF Activity^*

Alejandro Villagra¹, Fernando Cruzat, Loreto Carvallo, Roberto Paredes, Juan Olate, Andre J. van Wijnen, Gary S. Stein, Jane B. Lian, Janet L. Stein, Anthony N. Imbalzano, and Martin Montecino²

From the Departamento de Bioquimica y Biologia Molecular, Facultad de Ciencias Biologicas, Universidad de Concepcion, Casilla 160-C, 4079100 Concepcion, Chile and the Department of Cell Biology, University of Massachusetts Medical School, Worcester, Massachusetts 01655

Tissue-specific activation of the osteocalcin (OC) gene is associated with changes in chromatin structure at the promoter region. Two nuclease-hypersensitive sites span the key regulatory elements that control basal tissue-specific and vitamin D₃-enhanced OC gene transcription. To gain understanding of the molecular mechanisms involved in chromatin remodeling of the OC gene, we have examined the requirement for SWI/SNF activity. We inducibly expressed an ATPase-defective BRG1 catalytic subunit that forms inactive SWI/SNF complexes that bind to the OC promoter. This interaction results in inhibition of both basal and vitamin D₃-enhanced OC gene transcription and a marked decrease in nuclease hypersensitivity. We find that SWI/SNF is recruited to the OC promoter via the transcription factor CCAAT/enhancer-binding protein , which together with Runx2 forms a stable complex to facilitate RNA polymerase II binding and activation of OC gene transcription. Together, our results indicate that the SWI/SNF complex is a key regulator of the chromatin-remodeling events that promote tissue-specific transcription in osteoblasts.

Received for publication, October 27, 2005 , and in revised form, June 7, 2006.

^* This work has been supported by Fondo Nacional de Investigacion en Ciencia y Tecnologia (FONDECYT) Grant 1030749 and CONICYT-PBCT Grant ACT44 (to M. M.), FIRCA-National Institutes of Health (NIH) Grant 5RO3TW00990 (to G. S. S. and M. M.), and NIH Grants PO1AR48818 (to G. S. S.) and DE12528 (to J. B. L.). 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 supplemental Figs. 1S–4S.

¹ Supported by doctoral fellowships from CONICYT and MECESUP UCH9903.

² To whom correspondence should be addressed: Dept. de Bioquimica y Biologia Molecular, Facultad de Ciencias Biologicas, Universidad de Concepcion, Casilla 160-C, 4079100 Concepcion, Chile. Tel.: 56-41-203815; Fax: 56-41-239687; E-mail: mmonteci{at}udec.cl.

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