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Originally published In Press as doi:10.1074/jbc.M202256200 on April 26, 2002

J. Biol. Chem., Vol. 277, Issue 28, 25026-25031, July 12, 2002
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The Oncoprotein Set/TAF-1beta , an Inhibitor of Histone Acetyltransferase, Inhibits Active Demethylation of DNA, Integrating DNA Methylation and Transcriptional Silencing*

Nadia CervoniDagger , Nancy DetichDagger , Sang-beom Seo§, Debabrata Chakravarti§, and Moshe SzyfDagger

From the Dagger  Department of Pharmacology and Therapeutics, McGill University, Montreal, Quebec H3G 1Y6, Canada and the § Department of Pharmacology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104

Histone hypoacetylation and DNA hypermethylation are hallmarks of gene silencing. Although a role for DNA methylation in regulating histone acetylation has been established, it is not clear how and whether epigenetic histone markings influence DNA modifications in transcriptional silencing. We have previously shown that induction of histone acetylation by trichostatin A promotes demethylation of ectopically methylated DNA (Cervoni, N., and Szyf, M. (2001) J. Biol. Chem. 276, 40778-40787). The oncoprotein Set/TAF-Ibeta is a subunit of the recently identified inhibitor of acetyltransferases complex that inhibits histone acetylation by binding to and masking histone acetyltransferase targets (Seo, S. B., McNamara, P., Heo, S., Turner, A., Lane, W. S., and Chakravarti, D. (2001) Cell 104, 119-130). We show here that the overexpression of Set/TAF-Ibeta , whose expression is up-regulated in multiple tumor tissues, inhibits demethylation of ectopically methylated DNA resulting in gene silencing. Overexpression of a mutant Set/TAF-Ibeta that does not inhibit histone acetylation is defective in inhibiting DNA demethylation. Taken together, these results are consistent with a novel regulatory role for Set/TAF-Ibeta , integrating epigenetic states of histones and DNA in gene regulation and provide a new mechanism that can explain how hypermethylation of specific regions might come about by inhibition of demethylation in cancer cells.

* This work was supported by the National Cancer Institute of Canada. Work in D. C.'s laboratory was supported by National Institutes of Health Grant RO1 DK57079.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed at the above address: Dept. of Pharmacology and Therapeutics, McGill University, 3655 Drummond St., Montreal, Quebec H3G 1Y6, Canada. Tel.: 514-398-7107; Fax: 514-398-6690; E-mail: mszyf@pharma.mcgill.ca.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.


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