Hst3p, a histone deacetylase, promotes maintenance of Saccharomyces cerevisiae chromosome III lacking efficient replication origins

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• 作者：Carmela Irene ; James F. Theis ; David Gresham…
• 关键词：SNP analysis ; Genome stability ; DNA replication ; Histone H3 K56 acetylation ; Sirtuin
• 刊名：Molecular Genetics and Genomics
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：291
• 期：1
• 页码：271-283
• 全文大小：5,141 KB
• 参考文献：Bechhoefer J, Rhind N (2012) Replication timing and its emergence from stochastic processes. Trends Genet 28:374–381. doi:10.​1016/​j.​tig.​2012.​03.​011 PubMed PubMedCentral CrossRef
  Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA (2002) Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J Biol Chem 277:45099–45107PubMed CrossRef
  Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L, Boeke JD (1995) The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev 9:2888–2902PubMed CrossRef
  Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115–132PubMed CrossRef
  Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, Verreault A (2006) The sirtuins Hst3p and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr Biol 16:1280–1289PubMed CrossRef
  Celic I, Verreault A, Boeke JD (2008) Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179:1769–1784PubMed PubMedCentral CrossRef
  Collins SR et al (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446:806–810PubMed CrossRef
  Das C, Lucia MS, Hansen KC, Tyler JK (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459:113–117. doi:10.​1038/​nature07861 PubMed PubMedCentral CrossRef
  Delgoshaie N et al (2014) Regulation of the histone deacetylase Hst3 by cyclin-dependent kinases and the ubiquitin ligase SCFCdc4. J Biol Chem 289:13186–13196. doi:10.​1074/​jbc.​M113.​523530 PubMed PubMedCentral CrossRef
  Dershowitz A, Newlon CS (1993) The effect on chromosome stability of deleting replication origins. Mol Cell Biol 13:391–398PubMed PubMedCentral CrossRef
  Dershowitz A, Snyder M, Sbia M, Skurnick JH, Ong LY, Newlon CS (2007) Linear derivatives of Saccharomyces cerevisiae chromosome III can be maintained in the absence of autonomously replicating sequence elements. Mol Cell Biol 27:4652–4663PubMed PubMedCentral CrossRef
  Driscoll R, Hudson A, Jackson SP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315:649–652PubMed PubMedCentral CrossRef
  Dulev S, de Renty C, Mehta R, Minkov I, Schwob E, Strunnikov A (2009) Essential global role of CDC14 in DNA synthesis revealed by chromosome underreplication unrecognized by checkpoints in cdc14 mutants. Proc Natl Acad Sci USA 106:14466–14471. doi:10.​1073/​pnas.​0900190106 PubMed PubMedCentral CrossRef
  Edenberg ER, Vashisht AA, Topacio BR, Wohlschlegel JA, Toczyski DP (2014) Hst3 is turned over by a replication stress-responsive SCF(Cdc4) phospho-degron. Proc Natl Acad Sci USA 111:5962–5967. doi:10.​1073/​pnas.​1315325111 PubMed PubMedCentral CrossRef
  Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, Labib K (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8:358–366PubMed CrossRef
  Gambus A et al (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J 28:2992–3004. doi:10.​1038/​emboj.​2009.​226 PubMed PubMedCentral CrossRef
  Gresham D, Ruderfer DM, Pratt SC, Schacherer J, Dunham MJ, Botstein D, Kruglyak L (2006) Genome-wide detection of polymorphisms at nucleotide resolution with a single DNA microarray. Science 311:1932–1936PubMed CrossRef
  Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315:653–655PubMed CrossRef
  Han J, Zhang H, Zhang H, Wang Z, Zhou H, Zhang Z (2013) A Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly. Cell 155:817–829. doi:10.​1016/​j.​cell.​2013.​10.​014 PubMed PubMedCentral CrossRef
  Hyland EM, Cosgrove MS, Molina H, Wang D, Pandey A, Cottee RJ, Boeke JD (2005) Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol 25:10060–10070. doi:10.​1128/​MCB.​25.​22.​10060-10070.​2005 PubMed PubMedCentral CrossRef
  Ivessa AS, Lenzmeier BA, Bessler JB, Goudsouzian LK, Schnakenberg SL, Zakian VA (2003) The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell 12:1525–1536PubMed CrossRef
  Ji H, Moore DP, Blomberg MA, Braiterman LT, Voytas DF, Natsoulis G, Boeke JD (1993) Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell 73:1007–1018PubMed CrossRef
  Kadyrova LY et al (2013) A reversible histone H3 acetylation cooperates with mismatch repair and replicative polymerases in maintaining genome stability. PLoS Genet 9:e1003899. doi:10.​1371/​journal.​pgen.​1003899 PubMed PubMedCentral CrossRef
  Kaplan T et al (2008) Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4:e1000270. doi:10.​1371/​journal.​pgen.​1000270 PubMed PubMedCentral CrossRef
  Labib K, De Piccoli G (2011) Surviving chromosome replication: the many roles of the S-phase checkpoint pathway. Philos Trans R Soc Lond B Biol Sci 366:3554–3561. doi:10.​1098/​rstb.​2011.​0071 PubMed PubMedCentral CrossRef
  Lengronne A, McIntyre J, Katou Y, Kanoh Y, Hopfner KP, Shirahige K, Uhlmann F (2006) Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol Cell 23:787–799PubMed CrossRef
  Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244–255. doi:10.​1016/​j.​celll.​2008.​06.​018 PubMed PubMedCentral CrossRef
  Maas NL, Miller KM, DeFazio LG, Toczyski DP (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23:109–119PubMed CrossRef
  Masumoto H, Hawke D, Kobayashi R, Verreault A (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436:294–298PubMed CrossRef
  Megee PC, Morgan BA, Mittman BA, Smith MM (1990) Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science 247:841–845PubMed CrossRef
  Newman TJ, Mamun MA, Nieduszynski CA, Blow JJ (2013) Replisome stall events have shaped the distribution of replication origins in the genomes of yeasts. Nucleic Acids Res 41:9705–9718. doi:10.​1093/​nar/​gkt728 PubMed PubMedCentral CrossRef
  Ozdemir A, Spicuglia S, Lasonder E, Vermeulen M, Campsteijn C, Stunnenberg HG, Logie C (2005) Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J Biol Chem 280:25949–25952. doi:10.​1074/​jbc.​C500181200 PubMed CrossRef
  Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD (2006) A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124:1069–1081PubMed CrossRef
  Pasero P, Bensimon A, Schwob E (2002) Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev 16:2479–2484PubMed PubMedCentral CrossRef
  Paulovich AG, Hartwell LH (1995) A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82:841–847PubMed CrossRef
  Raths SK, Naider F, Becker JM (1988) Peptide analogues compete with the binding of alpha-factor to its receptor in Saccharomyces cerevisiae. J Biol Chem 263:17333–17341PubMed
  Santocanale C, Sharma K, Diffley JF (1999) Activation of dormant origins of DNA replication in budding yeast. Genes development 13:2360–2364PubMed PubMedCentral CrossRef
  Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75–100. doi:10.​1146/​annurev.​biochem.​76.​052705.​162114 PubMed CrossRef
  Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27PubMed PubMedCentral
  Simoneau A et al (2015) Interplay between histone H3 lysine 56 deacetylation and chromatin modifiers in response to DNA damage. Genetics 200:185–205. doi:10.​1534/​genetics.​115.​175919 PubMed CrossRef
  Spencer F, Gerring SL, Connelly C, Hieter P (1990) Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124:237–249PubMed PubMedCentral
  Tanaka H et al (2009) Ctf4 coordinates the progression of helicase and DNA polymerase alpha. Genes Cells 14:807–820. doi:10.​1111/​j.​1365-2443.​2009.​01310.​x PubMed CrossRef
  Thaminy S, Newcomb B, Kim J, Gatbonton T, Foss E, Simon J, Bedalov A (2007) Hst3 is regulated by Mec1-dependent proteolysis and controls the S phase checkpoint and sister chromatid cohesion by deacetylating histone H3 at lysine 56. J Biol Chem 282:37805–37814PubMed CrossRef
  Theis JF, Newlon CS (2001) Two compound replication origins in Saccharomyces cerevisiae contain redundant origin recognition complex binding sites. Mol Cell Biol 21:2790–2801. doi:10.​1128/​MCB.​21.​8.​2790-2801.​2001 PubMed PubMedCentral CrossRef
  Theis JF et al (2007) Identification of mutations that decrease the stability of a fragment of Saccharomyces cerevisiae chromosome III lacking efficient replicators. Genetics 177:1445–1458PubMed PubMedCentral CrossRef
  Theis JF et al (2010) The DNA damage response pathway contributes to the stability of chromosome III derivatives lacking efficient replicators. PLoS Genet 6:e1001227. doi:10.​1371/​journal.​pgen.​1001227 PubMed PubMedCentral CrossRef
  Tjeertes JV, Miller KM, Jackson SP (2009) Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J 28:1878–1889. doi:10.​1038/​emboj2009119 PubMed PubMedCentral CrossRef
  Tsubota T et al (2007) Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 25:703–712. doi:10.​1016/​j.​molcel.​2007.​02.​006 PubMed PubMedCentral CrossRef
  Tuduri S, Tourriere H, Pasero P (2010) Defining replication origin efficiency using DNA fiber assays. Chromosome Res 18:91–102. doi:10.​1007/​s10577-009-9098-y PubMed CrossRef
  Wurtele H et al (2012) Histone H3 lysine 56 acetylation and the response to DNA replication fork damage. Mol Cell Biol 32:154–172. doi:10.​1128/​MCB.​05415-11 PubMed PubMedCentral CrossRef
  Xie W et al (2009) Histone H3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell 33:417–427. doi:10.​1016/​j.​molcel.​2009.​02.​04 PubMed PubMedCentral CrossRef
  Ye J et al (2005) Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. Mol Cell 18:123–130. doi:10.​1016/​j.​molcel.​2005.​02.​031 PubMed PubMedCentral CrossRef
  Yuan J, Pu M, Zhang Z, Lou Z (2009) Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 8:1747–1753. doi:10.​4161/​cc.​8.​11.​8620 PubMed PubMedCentral CrossRef
  Zaidi IW et al (2008) Rtt101 and Mms1 in budding yeast form a CUL4(DDB1)-like ubiquitin ligase that promotes replication through damaged DNA. EMBO Rep 9:1034–1040. doi:10.​1038/​embor2008155 PubMed PubMedCentral CrossRef
  
• 作者单位：Carmela Irene (1)
  James F. Theis (1)
  David Gresham (2)
  Patricia Soteropoulos (1)
  Carol S. Newlon (1)
  
  1. Department of Microbiology, Biochemistry and Molecular Genetics, Rutgers New Jersey Medical School, ICPH, 225 Warren St., Newark, NJ, 07101-1701, USA
  2. Department of Biology, Center for Genomics and System Biology, New York University, 100 Washington Square East, New York, NY, 10003, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Biochemistry
  Microbial Genetics and Genomics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1617-4623

文摘

Long gaps between active replication origins probably occur frequently during chromosome replication, but little is known about how cells cope with them. To address this issue, we deleted replication origins from S. cerevisiae chromosome III to create chromosomes with long interorigin gaps and identified mutations that destabilize them [originless fragment maintenance (Ofm) mutations]. ofm6-1 is an allele of HST3, a sirtuin that deacetylates histone H3K56Ac. Hst3p and Hst4p are closely related, but hst4Δ does not cause an Ofm phenotype. Expressing HST4 under the control of the HST3 promoter suppressed the Ofm phenotype of hst3Δ, indicating Hst4p, when expressed at the appropriate levels and/or at the correct time, can fully substitute for Hst3p in maintenance of ORIΔ chromosomes. H3K56Ac is the Hst3p substrate critical for chromosome maintenance. H3K56Ac-containing nucleosomes are preferentially assembled into chromatin behind replication forks. Deletion of the H3K56 acetylase and downstream chromatin assembly factors suppressed the Ofm phenotype of hst3, indicating that persistence of H3K56Ac-containing chromatin is deleterious for the maintenance of ORIΔ chromosomes, and experiments with synchronous cultures showed that it is replication of H3K56Ac-containing chromatin that causes chromosome loss. This work shows that while normal chromosomes can tolerate hyperacetylation of H3K56Ac, deacetylation of histone H3K56Ac by Hst3p is required for stable maintenance of a chromosome with a long interorigin gap. The Ofm phenotype is the first report of a chromosome instability phenotype of an hst3 single mutant. Keywords SNP analysis Genome stability DNA replication Histone H3 K56 acetylation Sirtuin