Acetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly

Qing Li; Hui Zhou; Hugo Wurtele; Brian Davies; Bruce Horazdovsky; Alain Verreault; Zhiguo Zhang

doi:10.1016/j.cell.2008.06.018

Acetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly

Qing Li, Hui Zhou, Hugo Wurtele, Brian Davies, Bruce Horazdovsky, Alain Verreault, Zhiguo Zhang

Biochemistry and Molecular Biology

Research output: Contribution to journal › Article › peer-review

308 Scopus citations

Abstract

Chromatin assembly factor 1 (CAF-1) and Rtt106 participate in the deposition of newly synthesized histones onto replicating DNA to form nucleosomes. This process is critical for the maintenance of genome stability and inheritance of functionally specialized chromatin structures in proliferating cells. However, the molecular functions of the acetylation of newly synthesized histones in this DNA replication-coupled nucleosome assembly pathway remain enigmatic. Here we show that histone H3 acetylated at lysine 56 (H3K56Ac) is incorporated onto replicating DNA and, by increasing the binding affinity of CAF-1 and Rtt106 for histone H3, H3K56Ac enhances the ability of these histone chaperones to assemble DNA into nucleosomes. Genetic analysis indicates that H3K56Ac acts in a nonredundant manner with the acetylation of the N-terminal residues of H3 and H4 in nucleosome assembly. These results reveal a mechanism by which H3K56Ac regulates replication-coupled nucleosome assembly mediated by CAF-1 and Rtt106.

Original language	English (US)
Pages (from-to)	244-255
Number of pages	12
Journal	Cell
Volume	134
Issue number	2
DOIs	https://doi.org/10.1016/j.cell.2008.06.018
State	Published - Jul 25 2008

Keywords

DNA

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2008.06.018

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title = "Acetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly",

abstract = "Chromatin assembly factor 1 (CAF-1) and Rtt106 participate in the deposition of newly synthesized histones onto replicating DNA to form nucleosomes. This process is critical for the maintenance of genome stability and inheritance of functionally specialized chromatin structures in proliferating cells. However, the molecular functions of the acetylation of newly synthesized histones in this DNA replication-coupled nucleosome assembly pathway remain enigmatic. Here we show that histone H3 acetylated at lysine 56 (H3K56Ac) is incorporated onto replicating DNA and, by increasing the binding affinity of CAF-1 and Rtt106 for histone H3, H3K56Ac enhances the ability of these histone chaperones to assemble DNA into nucleosomes. Genetic analysis indicates that H3K56Ac acts in a nonredundant manner with the acetylation of the N-terminal residues of H3 and H4 in nucleosome assembly. These results reveal a mechanism by which H3K56Ac regulates replication-coupled nucleosome assembly mediated by CAF-1 and Rtt106.",

keywords = "DNA",

author = "Qing Li and Hui Zhou and Hugo Wurtele and Brian Davies and Bruce Horazdovsky and Alain Verreault and Zhiguo Zhang",

note = "Funding Information: We thank Jan van Deursen, Junjie Chen, Daniel Billadeau, and Rebecca Burgess for their critical reading of the manuscript. We thank Drs. Paul Kaufman and Jessica Tyler for plasmids and the Jacques C{\^o}t{\'e}'s laboratory for chromatin purification protocol. We thank Dr. Bruce Stillman for T-antigen, yeast strains, helpful discussions, and advice. We thank Junhong Han for performing experiments described in Figure 5 E. This work is supported in part by grants from the CIHR to A.V. and by NIH grants to Z.Z. IRIC receives infrastructure support from FRSQ. ",

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AU - Li, Qing

AU - Zhou, Hui

AU - Wurtele, Hugo

AU - Davies, Brian

AU - Horazdovsky, Bruce

AU - Verreault, Alain

AU - Zhang, Zhiguo

N1 - Funding Information: We thank Jan van Deursen, Junjie Chen, Daniel Billadeau, and Rebecca Burgess for their critical reading of the manuscript. We thank Drs. Paul Kaufman and Jessica Tyler for plasmids and the Jacques Côté's laboratory for chromatin purification protocol. We thank Dr. Bruce Stillman for T-antigen, yeast strains, helpful discussions, and advice. We thank Junhong Han for performing experiments described in Figure 5 E. This work is supported in part by grants from the CIHR to A.V. and by NIH grants to Z.Z. IRIC receives infrastructure support from FRSQ.

PY - 2008/7/25

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N2 - Chromatin assembly factor 1 (CAF-1) and Rtt106 participate in the deposition of newly synthesized histones onto replicating DNA to form nucleosomes. This process is critical for the maintenance of genome stability and inheritance of functionally specialized chromatin structures in proliferating cells. However, the molecular functions of the acetylation of newly synthesized histones in this DNA replication-coupled nucleosome assembly pathway remain enigmatic. Here we show that histone H3 acetylated at lysine 56 (H3K56Ac) is incorporated onto replicating DNA and, by increasing the binding affinity of CAF-1 and Rtt106 for histone H3, H3K56Ac enhances the ability of these histone chaperones to assemble DNA into nucleosomes. Genetic analysis indicates that H3K56Ac acts in a nonredundant manner with the acetylation of the N-terminal residues of H3 and H4 in nucleosome assembly. These results reveal a mechanism by which H3K56Ac regulates replication-coupled nucleosome assembly mediated by CAF-1 and Rtt106.

AB - Chromatin assembly factor 1 (CAF-1) and Rtt106 participate in the deposition of newly synthesized histones onto replicating DNA to form nucleosomes. This process is critical for the maintenance of genome stability and inheritance of functionally specialized chromatin structures in proliferating cells. However, the molecular functions of the acetylation of newly synthesized histones in this DNA replication-coupled nucleosome assembly pathway remain enigmatic. Here we show that histone H3 acetylated at lysine 56 (H3K56Ac) is incorporated onto replicating DNA and, by increasing the binding affinity of CAF-1 and Rtt106 for histone H3, H3K56Ac enhances the ability of these histone chaperones to assemble DNA into nucleosomes. Genetic analysis indicates that H3K56Ac acts in a nonredundant manner with the acetylation of the N-terminal residues of H3 and H4 in nucleosome assembly. These results reveal a mechanism by which H3K56Ac regulates replication-coupled nucleosome assembly mediated by CAF-1 and Rtt106.

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Acetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly

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