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J. Biol. Chem., Vol. 278, Issue 44, 43041-43050, October 31, 2003

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Involvement of the Histone Deacetylase SIRT1 in Chicken Ovalbumin Upstream Promoter Transcription Factor (COUP-TF)-interacting Protein 2-mediated Transcriptional Repression^*

Thanaset Senawong¶, Valerie J. Peterson, Dorina Avram||, David M. Shepherd**, Roy A. Frye, Saverio Minucci, and Mark Leid¶¶||||

From the Program in Molecular and Cellular Biology, Laboratory of Molecular Pharmacology, Department of Pharmaceutical Sciences, College of Pharmacy, ^¶¶Environmental Health Sciences Center, Oregon State University, Corvallis, Oregon 97331, the ^||Center for Cell Biology and Cancer Research, Albany Medical College, Albany, New York 12208, the ^**Center for Environmental Health Sciences Department of Pharmaceutical Sciences, College of Pharmacy, The University of Montana, Missoula, Montana 59812, the Pittsburgh Veterans Affairs Medical Center (132L), Department of Pathology, University of Pittsburgh, Pittsburgh, Pennsylvania 15240, and the Department of Experimental Oncology, European Institute of Oncology, Department of Physiology and Biochemistry, University of Milan, 20126 Milan, Italy

Chicken ovalbumin upstream promoter transcription factor (COUP-TF)-interacting proteins 1 and 2 (CTIP1 and CTIP2) enhance transcriptional repression mediated by COUP-TF II and have been implicated in hematopoietic cell development and malignancies. CTIP1 and CTIP2 are also sequence-specific DNA-binding proteins that repress transcription through direct, COUP-TF-in-dependent binding to a GC-rich response element. CTIP1- and CTIP2-mediated transcriptional repression is insensitive to trichostatin A, an inhibitor of known class I and II histone deacetylases. However, chromatin immunoprecipitation assays revealed that expression of CTIP2 in mammalian cells resulted in deacetylation of histones H3 and/or H4 that were associated with the promoter region of a reporter gene. CTIP2-mediated transcriptional repression, as well as deacetylation of promoter-associated histones H3/H4 in CTIP2-transfected cells, was reversed by nicotinamide, an inhibitor of class III histone deacetylases such as the mammalian homologs of yeast Silent Information Regulator 2 (Sir2). The human homolog of yeast Sir2, SIRT1, was found to interact directly with CTIP2 and was recruited to the promoter template in a CTIP2-dependent manner. Moreover, SIRT1 enhanced the deacetylation of template-associated histones H3/H4 in CTIP2-transfected cells, and stimulated CTIP2-dependent transcriptional repression. Finally, endogenous SIRT1 and CTIP2 co-purified from Jurkat cell nuclear extracts in the context of a large (1–2 mDa) complex. These findings implicate SIRT1 as a histone H3/H4 deacetylase in mammalian cells and in transcriptional repression mediated by CTIP2.

Received for publication, July 11, 2003 , and in revised form, August 5, 2003.

^* This work was supported in part by National Institutes of Health Grant GM60852 (to M. L.) and NIEHS Center National Institutes of Health Grant ES00210 to the Oregon State University Environmental Health Sciences Center. 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.

^¶ Supported by a graduate fellowship from the Royal Thai Government.

^|||| To whom correspondence should be addressed: Laboratory of Molecular Pharmacology, Dept. of Pharmaceutical Sciences, College of Pharmacy, Oregon State University, Corvallis, OR 97331. Tel.: 541-737-5809; Fax: 541-737-3999; E-mail: Mark.Leid{at}oregonstate.edu.

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