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J. Biol. Chem., Vol. 282, Issue 4, 2450-2455, January 26, 2007

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Proteome-wide Analysis in Saccharomyces cerevisiae Identifies Several PHD Fingers as Novel Direct and Selective Binding Modules of Histone H3 Methylated at Either Lysine 4 or Lysine 36^*

Xiaobing Shi¹, Ioulia Kachirskaia¹, Kay L. Walter, Jen-Hao A. Kuo, Aimee Lake, Foteini Davrazou^¶, Steve M. Chan^||, David G. E. Martin^**, Ian M. Fingerman, Scott D. Briggs, LeAnn Howe^**, Paul J. Utz^||, Tatiana G. Kutateladze^¶, Alexey A. Lugovskoy², Mark T. Bedford, and Or Gozani³

From the Department of Biological Sciences, Stanford University, Stanford, California 94305, the University of Texas M.D. Anderson Cancer Center, Smithville, Texas 78957, the ^¶Department of Pharmacology, University Colorado Health Sciences Center, Aurora, Colorado 80045, the ^||Department of Medicine, Division of Immunology and Rheumatology, Stanford University School of Medicine, Stanford, California 94305, the ^**Department of Biochemistry and Molecular Biology, The University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada, the Department of Biochemistry, Purdue University, West Lafayette, Indiana 47907, and the Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts 02115

The PHD finger motif is a signature chromatin-associated motif that is found throughout eukaryotic proteomes. Here we have determined the histone methyl-lysine binding activity of the PHD fingers present within the Saccharomyces cerevisiae proteome. We provide evidence on the genomic scale that PHD fingers constitute a general class of effector modules for histone H3 trimethylated at lysine 4 (H3K4me3) and histone H3 trimethylated at lysine 36 (H3K36me3). Structural modeling of PHD fingers demonstrates a conserved mechanism for recognizing the trimethyl moiety and provides insight into the molecular basis of affinity for the different methyl-histone ligands. Together, our study suggests that a common function for PHD fingers is to transduce methyl-lysine events and sheds light on how a single histone modification can be linked to multiple biological outcomes.

Received for publication, November 6, 2006 , and in revised form, November 29, 2006.

^* This work was supported by grants from the National Institutes of Health (to S. D. B., P. J. U., and T. G. K.), the Canadian Institutes of Health and Michael Smith Foundation (to L. H.), the Baxter Foundation and Dana Foundation (to P. J. U.), the Welch Foundation (to M. T. B.), and the Kimmel Foundation (to O. G.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1 and 2.

¹ These authors contributed equally to this work.

² Present address: Molecular Discovery, Biogen Idec Inc., Cambridge, MA 02142.

³ Recipient of a Burroughs Wellcome Career Development Award in Biomedical Sciences. To whom correspondence should be addressed. Tel.: 650-799-0306; Fax: 650-725-8309; E-mail: ogozani{at}stanford.edu.

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