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J. Biol. Chem., Vol. 280, Issue 26, 25298-25303, July 1, 2005

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Transcription-induced Chromatin Remodeling at the c-myc Gene Involves the Local Exchange of Histone H2A.Z^*

Stephen D. Farris, Eric D. Rubio, James J. Moon¶, Wendy M. Gombert, Brad H. Nelson||, and Anton Krumm**

From the Department of Radiation Oncology, University of Washington School of Medicine, Seattle, Washington 98104, ^¶Center for Immunology, University of Minnesota, Minneapolis, Minnesota 55455, and ^||Deeley Research Centre, British Columbia Cancer Agency, Victoria, British Columbia V8R 6V5, Canada

The post-translational modification of histones and the incorporation of core histone variants play key roles in governing gene expression. Many eukaryotic genes regulate their expression by limiting the escape of RNA polymerase from promoter-proximal pause sites. Here we report that elongating RNA polymerase II complexes encounter distinct chromatin landscapes that are marked by methylation of lysine residues Lys⁴, Lys⁷⁹, and Lys³⁶ of histone H3. However, neither histone methylation nor acetylation directly regulates the release of elongation complexes stalled at promoter-proximal pause sites of the c-myc gene. In contrast, transcriptional activation is associated with local displacement of the histone variant H2A.Z within the transcribed region and incorporation of the major histone variant H2A. This result indicates that transcribing RNA polymerase II remodels chromatin in part through coincident displacement of H2A.Z-H2B dimers and incorporation of H2A-H2B dimers. In combination, these results suggest a new model in which the incorporation of H2A.Z into nucleosomes down-regulates transcription; at the same time it may act as a cellular memory for transcriptionally poised gene domains.

Received for publication, February 16, 2005 , and in revised form, May 5, 2005.

^* This work was supported by Research Scholar Grant RSG-01-163-01-GMC from the American Cancer Society (to A. K.). 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.

These authors contributed equally.

^** To whom correspondence should be addressed: University of Washington, Veterans Affairs Medical Center, 1660 S. Columbian Way R151, Seattle, WA 98108. Tel.: 206-764-2381; Fax: 206-764-2827; E-mail: akrumm{at}u.washington.edu.

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