MCB Accepts, published online ahead of print on 12 February 2007

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Mol. Cell. Biol. doi:10.1128/MCB.02311-06
Copyright (c) 2007, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Histone deacetylases RPD3 and HOS2 regulate the transcriptional activation of DNA damage inducible genes

Vishva Mitra Sharma, Raghuvir S. Tomar, Alison E. Dempsey, and Joseph C. Reese^*

Department of Biochemistry and Molecular Biology, Center for Gene Regulation, The Pennsylvania State University, University Park, PA 16802, USA

^* To whom correspondence should be addressed. Email: Jcr8{at}psu.edu.

DNA microarray and genetic studies in Saccharomyces cerevisiae have demonstrated that histone deacetylases (HDACs) are required for transcriptional activation and repression, but the mechanism by which they activate transcription remains poorly understood. We show that two histone deacetylases, RPD3 and HOS2, are required for the activation of the DNA damage inducible genes RNR3 and HUG1. Using mutants specific for the Rpd3L complex, we show that it is responsible for regulating RNR3. Furthermore, unlike what was described at the GAL genes, Rpd3L regulates the activation of RNR3 by deacetylating nucleosomes at the promoter, not the ORF. Rpd3 is recruited to the upstream repression sequences (URS) of RNR3, which, surprisingly, does not require Tup1 or Crt1. Chromatin remodeling and TFIID recruitment is largely unaffected in the rpd3/hos2 mutant, but RNA polymerase II recruitment is strongly reduced, arguing that Rpd3 and Hos2 regulate later stages in preinitiation complex assembly or facilitate multiple rounds of polymerase recruitment. Furthermore, the histone H4 acetyltransferase Esa1 is required for activation of RNR3 and HUG1. Thus, reduced or un-regulated, constitutive histone H4 acetylation is detrimental to promoter activity, suggesting that HDAC-dependent mechanisms are in place to reset promoters to allow high levels of transcription.

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