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Molecular and Cellular Biology, April 2007, p. 3199-3210, Vol. 27, No. 8
0270-7306/07/$08.00+0     doi:10.1128/MCB.02311-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Histone Deacetylases RPD3 and HOS2 Regulate the Transcriptional Activation of DNA Damage-Inducible Genes{triangledown}

Vishva Mitra Sharma,{dagger} 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, Pennsylvania 16802

Received 11 December 2006/ Returned for modification 22 January 2007/ Accepted 29 January 2007

DNA microarray and genetic studies of 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 HDACs, RPD3 and HOS2, are required for the activation of DNA damage-inducible genes RNR3 and HUG1. Using mutants specific for the Rpd3L complex, we show that the complex is responsible for regulating RNR3. Furthermore, unlike what was described for the GAL genes, Rpd3L regulates the activation of RNR3 by deacetylating nucleosomes at the promoter, not at the open reading frame. Rpd3 is recruited to the upstream repression sequence of RNR3, which surprisingly does not require Tup1 or Crt1. Chromatin remodeling and TFIID recruitment are largely unaffected in the {Delta}rpd3/{Delta}hos2 mutant, but the recruitment of RNA polymerase II is strongly reduced, arguing that Rpd3 and Hos2 regulate later stages in the assembly of the preinitiation complex or facilitate multiple rounds of polymerase recruitment. Furthermore, the histone H4 acetyltransferase Esa1 is required for the activation of RNR3 and HUG1. Thus, reduced or unregulated 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.

* Corresponding author. Mailing address: Penn State University, Department of Biochemistry and Molecular Biology, 203 Althouse Lab, University Park, PA 16802. Phone: (814) 865-1976. Fax: (814) 863-7024. E-mail: Jcr8{at}psu.edu

{triangledown} Published ahead of print on 12 February 2007.

{dagger} Present address: University of Massachusetts Medical School, Department of Molecular Genetics and Microbiology, 55 Lake Ave., Worcester, MA 01655.

Molecular and Cellular Biology, April 2007, p. 3199-3210, Vol. 27, No. 8
0270-7306/07/$08.00+0     doi:10.1128/MCB.02311-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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