Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks
Chromatin assembly mutants accumulate recombinogenic DNA damage and are sensitive to genotoxic agents. Here we have analyzed why impairment of the H3K56 acetylation-dependent CAF1 and Rtt106 chromatin assembly pathways, which have redundant roles in H3/H4 deposition during DNA replication, leads to...
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| creator | Clemente-Ruiz, Marta González-Prieto, Román Prado, Félix |
| description | Chromatin assembly mutants accumulate recombinogenic DNA damage and are sensitive to genotoxic agents. Here we have analyzed why impairment of the H3K56 acetylation-dependent CAF1 and Rtt106 chromatin assembly pathways, which have redundant roles in H3/H4 deposition during DNA replication, leads to genetic instability. We show that the absence of H3K56 acetylation or the simultaneous knock out of CAF1 and Rtt106 increases homologous recombination by affecting the integrity of advancing replication forks, while they have a minor effect on stalled replication fork stability in response to the replication inhibitor hydroxyurea. This defect in replication fork integrity is not due to defective checkpoints. In contrast, H3K56 acetylation protects against replicative DNA damaging agents by DNA repair/tolerance mechanisms that do not require CAF1/Rtt106 and are likely subsequent to the process of replication-coupled nucleosome deposition. We propose that the tight connection between DNA synthesis and histone deposition during DNA replication mediated by H3K56ac/CAF1/Rtt106 provides a mechanism for the stabilization of advancing replication forks and the maintenance of genome integrity, while H3K56 acetylation has an additional, CAF1/Rtt106-independent function in the response to replicative DNA damage. |
| doi_str_mv | 10.1371/journal.pgen.1002376 |
| format | Article |
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Here we have analyzed why impairment of the H3K56 acetylation-dependent CAF1 and Rtt106 chromatin assembly pathways, which have redundant roles in H3/H4 deposition during DNA replication, leads to genetic instability. We show that the absence of H3K56 acetylation or the simultaneous knock out of CAF1 and Rtt106 increases homologous recombination by affecting the integrity of advancing replication forks, while they have a minor effect on stalled replication fork stability in response to the replication inhibitor hydroxyurea. This defect in replication fork integrity is not due to defective checkpoints. In contrast, H3K56 acetylation protects against replicative DNA damaging agents by DNA repair/tolerance mechanisms that do not require CAF1/Rtt106 and are likely subsequent to the process of replication-coupled nucleosome deposition. We propose that the tight connection between DNA synthesis and histone deposition during DNA replication mediated by H3K56ac/CAF1/Rtt106 provides a mechanism for the stabilization of advancing replication forks and the maintenance of genome integrity, while H3K56 acetylation has an additional, CAF1/Rtt106-independent function in the response to replicative DNA damage.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1002376</identifier><identifier>PMID: 22102830</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acetylation ; Biology ; Cellular signal transduction ; Chromatin ; Chromatin Assembly and Disassembly - genetics ; Chromosome abnormalities ; Deoxyribonucleic acid ; DNA ; DNA - biosynthesis ; DNA damage ; DNA Damage - genetics ; DNA repair ; DNA Repair - genetics ; DNA replication ; DNA Replication - genetics ; Genetic aspects ; Histone Acetyltransferases - genetics ; Histone Acetyltransferases - metabolism ; Histones - genetics ; Histones - metabolism ; Homologous Recombination - genetics ; Lysine - metabolism ; Molecular Chaperones - genetics ; Molecular Chaperones - metabolism ; Mutation ; Nucleosomes - genetics ; Nucleosomes - metabolism ; Physiological aspects ; Proteins ; Ribonucleases - genetics ; Ribonucleases - metabolism ; Risk factors ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - metabolism ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Signal Transduction</subject><ispartof>PLoS genetics, 2011-11, Vol.7 (11), p.e1002376-e1002376</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>Clemente-Ruiz et al. 2011</rights><rights>2011 Clemente-Ruiz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Clemente-Ruiz M, González-Prieto R, Prado F (2011) Histone H3K56 Acetylation, CAF1, and Rtt106 Coordinate Nucleosome Assembly and Stability of Advancing Replication Forks. 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Here we have analyzed why impairment of the H3K56 acetylation-dependent CAF1 and Rtt106 chromatin assembly pathways, which have redundant roles in H3/H4 deposition during DNA replication, leads to genetic instability. We show that the absence of H3K56 acetylation or the simultaneous knock out of CAF1 and Rtt106 increases homologous recombination by affecting the integrity of advancing replication forks, while they have a minor effect on stalled replication fork stability in response to the replication inhibitor hydroxyurea. This defect in replication fork integrity is not due to defective checkpoints. In contrast, H3K56 acetylation protects against replicative DNA damaging agents by DNA repair/tolerance mechanisms that do not require CAF1/Rtt106 and are likely subsequent to the process of replication-coupled nucleosome deposition. We propose that the tight connection between DNA synthesis and histone deposition during DNA replication mediated by H3K56ac/CAF1/Rtt106 provides a mechanism for the stabilization of advancing replication forks and the maintenance of genome integrity, while H3K56 acetylation has an additional, CAF1/Rtt106-independent function in the response to replicative DNA damage.</description><subject>Acetylation</subject><subject>Biology</subject><subject>Cellular signal transduction</subject><subject>Chromatin</subject><subject>Chromatin Assembly and Disassembly - genetics</subject><subject>Chromosome abnormalities</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA - biosynthesis</subject><subject>DNA damage</subject><subject>DNA Damage - genetics</subject><subject>DNA repair</subject><subject>DNA Repair - genetics</subject><subject>DNA replication</subject><subject>DNA Replication - genetics</subject><subject>Genetic aspects</subject><subject>Histone Acetyltransferases - genetics</subject><subject>Histone Acetyltransferases - metabolism</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>Homologous Recombination - genetics</subject><subject>Lysine - metabolism</subject><subject>Molecular Chaperones - genetics</subject><subject>Molecular Chaperones - metabolism</subject><subject>Mutation</subject><subject>Nucleosomes - genetics</subject><subject>Nucleosomes - metabolism</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Ribonucleases - genetics</subject><subject>Ribonucleases - metabolism</subject><subject>Risk factors</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Signal Transduction</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11rFDEUhgdRbK3-A9EBQRG6azJJJjM3wlKsLRYL9eM2nMmcbFOzyTrJVPffm-1uSxe8UHKRcPK870lycoriOSVTyiR9dxXGwYObLufop5SQisn6QbFPhWATyQl_eG-9VzyJ8YoQJppWPi72qoqSqmFkv_h1YmMKHssT9knUJWhMKwfJBn9YHs2O6WEJvi8vUqKkLnUIQ289JCz9qB2GGBZYQoy46NzqhowJOutsWpXBlNBfg9fWz8sBl87qG9_ShOFHfFo8MuAiPtvOB8W34w9fj04mZ-cfT49mZxMta5YmXd33SJqq5qg5dB0aME0Htek72Yi6MUYAA9bIWlLS9b3m3FRNJQkIqAkiOyhebnyXLkS1fbOoKKNMcCGEzMTphugDXKnlYBcwrFQAq24CYZgrGJLN11XCtLpl2NQakMu2aUlddVwTyducE_vs9X6bbewW2Gv0aQC3Y7q74-2lmodrxap8ooZkgzdbgyH8HDEmtbBRo3PgMYxRtSRfmlHBM_lqQ84hn8x6E7KhXtNqVsn8QQSvaaamf6Hy6HFhda67sTm-I3i7I8hMwt9pDmOM6vTLxX-wn_-dPf--y76-x14iuHQZgxvXvyfugnwD6iHEOKC5e2lK1LpJbguu1k2itk2SZS_uV-lOdNsV7A9Umwx-</recordid><startdate>20111101</startdate><enddate>20111101</enddate><creator>Clemente-Ruiz, Marta</creator><creator>González-Prieto, Román</creator><creator>Prado, Félix</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20111101</creationdate><title>Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks</title><author>Clemente-Ruiz, Marta ; González-Prieto, Román ; Prado, Félix</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c763t-b6dde08264ec4abbefaf8ba6fdb78568ff5a3a3876710bddc44f28270a5a60ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Acetylation</topic><topic>Biology</topic><topic>Cellular signal transduction</topic><topic>Chromatin</topic><topic>Chromatin Assembly and Disassembly - genetics</topic><topic>Chromosome abnormalities</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA - biosynthesis</topic><topic>DNA damage</topic><topic>DNA Damage - genetics</topic><topic>DNA repair</topic><topic>DNA Repair - genetics</topic><topic>DNA replication</topic><topic>DNA Replication - genetics</topic><topic>Genetic aspects</topic><topic>Histone Acetyltransferases - genetics</topic><topic>Histone Acetyltransferases - metabolism</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>Homologous Recombination - genetics</topic><topic>Lysine - metabolism</topic><topic>Molecular Chaperones - genetics</topic><topic>Molecular Chaperones - metabolism</topic><topic>Mutation</topic><topic>Nucleosomes - genetics</topic><topic>Nucleosomes - metabolism</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Ribonucleases - genetics</topic><topic>Ribonucleases - metabolism</topic><topic>Risk factors</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Saccharomyces cerevisiae - metabolism</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Signal Transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Clemente-Ruiz, Marta</creatorcontrib><creatorcontrib>González-Prieto, Román</creatorcontrib><creatorcontrib>Prado, Félix</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints in Context (Gale)</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Clemente-Ruiz, Marta</au><au>González-Prieto, Román</au><au>Prado, Félix</au><au>Haber, James E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2011-11-01</date><risdate>2011</risdate><volume>7</volume><issue>11</issue><spage>e1002376</spage><epage>e1002376</epage><pages>e1002376-e1002376</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Chromatin assembly mutants accumulate recombinogenic DNA damage and are sensitive to genotoxic agents. Here we have analyzed why impairment of the H3K56 acetylation-dependent CAF1 and Rtt106 chromatin assembly pathways, which have redundant roles in H3/H4 deposition during DNA replication, leads to genetic instability. We show that the absence of H3K56 acetylation or the simultaneous knock out of CAF1 and Rtt106 increases homologous recombination by affecting the integrity of advancing replication forks, while they have a minor effect on stalled replication fork stability in response to the replication inhibitor hydroxyurea. This defect in replication fork integrity is not due to defective checkpoints. In contrast, H3K56 acetylation protects against replicative DNA damaging agents by DNA repair/tolerance mechanisms that do not require CAF1/Rtt106 and are likely subsequent to the process of replication-coupled nucleosome deposition. We propose that the tight connection between DNA synthesis and histone deposition during DNA replication mediated by H3K56ac/CAF1/Rtt106 provides a mechanism for the stabilization of advancing replication forks and the maintenance of genome integrity, while H3K56 acetylation has an additional, CAF1/Rtt106-independent function in the response to replicative DNA damage.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22102830</pmid><doi>10.1371/journal.pgen.1002376</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Acetylation Biology Cellular signal transduction Chromatin Chromatin Assembly and Disassembly - genetics Chromosome abnormalities Deoxyribonucleic acid DNA DNA - biosynthesis DNA damage DNA Damage - genetics DNA repair DNA Repair - genetics DNA replication DNA Replication - genetics Genetic aspects Histone Acetyltransferases - genetics Histone Acetyltransferases - metabolism Histones - genetics Histones - metabolism Homologous Recombination - genetics Lysine - metabolism Molecular Chaperones - genetics Molecular Chaperones - metabolism Mutation Nucleosomes - genetics Nucleosomes - metabolism Physiological aspects Proteins Ribonucleases - genetics Ribonucleases - metabolism Risk factors Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Signal Transduction |
| title | Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks |
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