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Originally published In Press as doi:10.1074/jbc.M407159200 on July 14, 2004

J. Biol. Chem., Vol. 279, Issue 38, 39240-39250, September 17, 2004
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Redundant Mechanisms Are Used by Ssn6-Tup1 in Repressing Chromosomal Gene Transcription in Saccharomyces cerevisiae*

Zhengjian Zhang and Joseph C. Reese{ddagger}

From the Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802

The Ssn6-Tup1 corepressor complex regulates many genes in Saccharomyces cerevisiae. Three mechanisms have been proposed to explain its repression functions: 1) nucleosome positioning by binding histone tails; 2) recruitment of histone deacetylases; and 3) direct interference with the general transcription machinery or activators. It is unclear if Ssn6-Tup1 utilizes each of these mechanisms at a single gene in a redundant manner or each individually at different loci. A systematic analysis of the contribution of each mechanism at a native promoter has not been reported. Here we employed a genetic strategy to analyze the contributions of nucleosome positioning, histone deacetylation, and Mediator interference in the repression of chromosomal Tup1 target genes in vivo. We exploited the fact that Ssn6-Tup1 requires the ISW2 chromatin remodeling complex to establish nucleosome positioning in vivo to disrupt chromatin structure without affecting other Tup1 repression functions. Deleting ISW2, the histone deacetylase gene HDA1, or genes encoding Mediator subunits individually caused slight or no derepression of RNR3 and HUG1. However, when Mediator mutations were combined with {Delta}isw2 or {Delta}hda1 mutations, enhanced transcription was observed, and the strongest level of derepression was observed in triple {Delta}isw2/{Delta}hda1/Mediator mutants. The increased transcription in the mutants was not due to the loss of Tup1 at the promoter and correlated with increased TBP cross-linking to promoters. Thus, Tup1 utilizes multiple redundant mechanisms to repress transcription of native genes, which may be important for it to act as a global corepressor at a wide variety of promoters.

Received for publication, June 25, 2004 , and in revised form, July 14, 2004.

* This research was supported by funds provided by the National Institutes of Health Grant GM58672 and by an Established Investigator Grant from the American Heart Association (to J. C. R.). 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.

{ddagger} To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, Pennsylvania State University, 203 Althouse Laboratory, University Park, PA 16802. Tel.: 814-865-1976; Fax: 814-863-7024; E-mail: Jcr8{at}psu.edu.


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