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J. Biol. Chem., Vol. 281, Issue 14, 9287-9296, April 7, 2006

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Modifications of H3 and H4 during Chromatin Replication, Nucleosome Assembly, and Histone Exchange^*

Laura J. Benson, Yongli Gu, Tatyana Yakovleva¹, Kevin Tong, Courtney Barrows, Christine L. Strack, Richard G. Cook, Craig A. Mizzen^¶, and Anthony T. Annunziato²

From the Department of Biology, Boston College, Chestnut Hill, Massachusetts 02467, the ^¶Department of Cell and Developmental Biology, University of Illinois, Urbana, Illinois 61801, and the Department of Immunology, Baylor College of Medicine, Houston, Texas 77030

Histone posttranslational modifications that accompany DNA replication, nucleosome assembly, and H2A/H2B exchange were examined in human tissue culture cells. Through microsequencing analysis and chromatin immunoprecipitation, it was found that a subset of newly synthesized H3.2/H3.3 is modified by acetylation and methylation at sites that correlate with transcriptional competence. Immunoprecipitation experiments suggest that cytosolic predeposition complexes purified from cells expressing FLAG-H4 contain H3/H4 dimers, not tetramers. Studies of the deposition of newly synthesized H2A/H2B onto replicating and nonreplicating chromatin demonstrated that H2A/H2B exchange takes place in chromatin regions that contain acetylated H4; however, there is no single pattern of H4 acetylation that accompanies exchange. H2A/H2B exchange is also largely independent of the deposition of replacement histone variant, H3.3. Finally, immunoprecipitation of nucleosomes replicated in the absence of de novo nucleosome assembly showed that histone modifications do not prevent the transfer of parental histones to newly replicated DNA and thus have the potential to serve as means of epigenetic inheritance. Our experiments provide an in-depth analysis of the "histone code" associated with chromatin replication and dynamic histone exchange in human cells.

Received for publication, December 5, 2005 , and in revised form, February 6, 2006.

^* This work was supported by NIGMS, National Institutes of Health, Grants GM35837 (to A. T. A.) and GM53122 (to C. D. Allis). 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. S1-S3.

¹ Present address: Dept. of Biochemistry, University of Cambridge, CB2 1GA Cambridge, UK.

² To whom correspondence should be addressed: Dept. of Biology, Boston College, 140 Commonwealth Ave., Chestnut Hill, MA 02467. Tel.: 617-552-3812; Fax: 617-552-2011; E-mail: anthony.annunziato{at}bc.edu.

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