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 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.


Vyšlo v časopise: Histone H3K56 Acetylation, CAF1, and Rtt106 Coordinate Nucleosome Assembly and Stability of Advancing Replication Forks. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002376
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1002376

Souhrn

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.


Zdroje

1. HalazonetisTDGorgoulisVGBartekJ 2008 An oncogene-induced DNA damage model for cancer development. Science 319 1352 1355

2. CicciaAElledgeSJ 2010 The DNA damage response: making it safe to play with knives. Mol Cell 40 179 204

3. PutnamCDJaehnigEJKolodnerRD 2009 Perspectives on the DNA damage and replication checkpoint responses in Saccharomyces cerevisiae. DNA Repair (Amst) 8 974 982

4. HeyerWDEhmsenKTLiuJ 2010 Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44 113 139

5. ProbstAVDunleavyEAlmouzniG 2009 Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 10 192 206

6. MoggsJGGrandiPQuivyJPJonssonZOHubscherU 2000 A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20 1206 1218

7. ShibaharaKStillmanB 1999 Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96 575 585

8. FrancoAALamWMBurgersPMKaufmanPD 2005 Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev 19 1365 1375

9. GambusAJonesRCSanchez-DiazAKanemakiMvan DeursenF 2006 GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8 358 366

10. GrothACorpetACookAJRocheDBartekJ 2007 Regulation of replication fork progression through histone supply and demand. Science 318 1928 1931

11. TanBCChienCTHiroseSLeeSC 2006 Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J 25 3975 3985

12. GunjanAPaikJVerreaultA 2006 The emergence of regulated histone proteolysis. Curr Opin Genet Dev 16 112 118

13. NelsonDMYeXHallCSantosHMaT 2002 Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity. Mol Cell Biol 22 7459 7472

14. OsleyMA 1991 The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60 827 861

15. AiXParthunMR 2004 The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol Cell 14 195 205

16. BurgessRJZhouHHanJZhangZ 2010 A role for Gcn5 in replication-coupled nucleosome assembly. Mol Cell 37 469 480

17. LiQZhouHWurteleHDaviesBHorazdovskyB 2008 Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134 244 255

18. MaXJWuJAltheimBASchultzMCGrunsteinM 1998 Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc Natl Acad Sci U S A 95 6693 6698

19. YeJAiXEugeniEEZhangLCarpenterLR 2005 Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. Mol Cell 18 123 130

20. KleffSAndrulisEDAndersonCWSternglanzR 1995 Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 270 24674 24677

21. SobelRECookRGPerryCAAnnunziatoATAllisCD 1995 Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A 92 1237 1241

22. FillinghamJRechtJSilvaACSuterBEmiliA 2008 Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 28 4342 4353

23. DriscollRHudsonAJacksonSP 2007 Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315 649 652

24. HanJZhouHHorazdovskyBZhangKXuRM 2007 Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315 653 655

25. MasumotoHHawkeDKobayashiRVerreaultA 2005 A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436 294 298

26. TsubotaTBerndsenCEErkmannJASmithCLYangL 2007 Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 25 703 712

27. TylerJKAdamsCRChenSRKobayashiRKamakakaRT 1999 The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402 555 560

28. HuangSZhouHKatzmannDHochstrasserMAtanasovaE 2005 Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc Natl Acad Sci U S A 102 13410 13415

29. KrawitzDCKamaTKaufmanPD 2002 Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol Cell Biol 22 614 625

30. TylerJKCollinsKAPrasad-SinhaJAmiottEBulgerM 2001 Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol 21 6574 6584

31. EndoMIshikawaYOsakabeKNakayamaSKayaH 2006 Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO J 25 5579 5590

32. YeXFrancoAASantosHNelsonDMKaufmanPD 2003 Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol Cell 11 341 351

33. MyungKPennaneachVKatsESKolodnerRD 2003 Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc Natl Acad Sci U S A 100 6640 6645

34. PradoFCortes-LedesmaFAguileraA 2004 The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep 5 497 502

35. PradoFAguileraA 2005 Partial depletion of histone H4 increases homologous recombination-mediated genetic instability. Mol Cell Biol 25 1526 1536

36. ZhaoXMcKillop-SmithSMullerB 2004 The human histone gene expression regulator HBP/SLBP is required for histone and DNA synthesis, cell cycle progression and cell proliferation in mitotic cells. J Cell Sci 117 6043 6051

37. ChoyJSKronSJ 2002 NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol Cell Biol 22 8215 8225

38. QinSParthunMR 2002 Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol 22 8353 8365

39. ChenCCCarsonJJFeserJTamburiniBZabaronickS 2008 Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134 231 243

40. KimJAHaberJE 2009 Chromatin assembly factors Asf1 and CAF-1 have overlapping roles in deactivating the DNA damage checkpoint when DNA repair is complete. Proc Natl Acad Sci U S A 106 1151 1156

41. LingerJTylerJK 2005 The yeast histone chaperone chromatin assembly factor 1 protects against double-strand DNA-damaging agents. Genetics 171 1513 1522

42. Clemente-RuizMPradoF 2009 Chromatin assembly controls replication fork stability. EMBO Rep 10 790 796

43. RechtJTsubotaTTannyJCDiazRLBergerJM 2006 Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci U S A 103 6988 6993

44. KaplanTLiuCLErkmannJAHolikJGrunsteinM 2008 Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4 e1000270 doi:10.1371/journal.pgen.1000270

45. RufiangeAJacquesPEBhatWRobertFNouraniA 2007 Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27 393 405

46. SharpJAFoutsETKrawitzDCKaufmanPD 2001 Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr Biol 11 463 473

47. GreenEMAntczakAJBaileyAOFrancoAAWuKJ 2005 Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 15 2044 2049

48. HuFAlcasabasAAElledgeSJ 2001 Asf1 links Rad53 to control of chromatin assembly. Genes Dev 15 1061 1066

49. RameyCJHowarSAdkinsMLingerJSpicerJ 2004 Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol Cell Biol 24 10313 10327

50. HanJZhouHLiZXuRMZhangZ 2007 Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 282 28587 28596

51. PradoFCortes-LedesmaFHuertasPAguileraA 2003 Mitotic recombination in Saccharomyces cerevisiae. Curr Genet 42 185 198

52. LopesMCotta-RamusinoCPellicioliALiberiGPlevaniP 2001 The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412 557 561

53. CollinsSRMillerKMMaasNLRoguevAFillinghamJ 2007 Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 806 810

54. KatsESAlbuquerqueCPZhouHKolodnerRD 2006 Checkpoint functions are required for normal S-phase progression in Saccharomyces cerevisiae RCAF- and CAF-I-defective mutants. Proc Natl Acad Sci U S A 103 3710 3715

55. DuroEVaisicaJABrownGWRouseJ 2008 Budding yeast Mms22 and Mms1 regulate homologous recombination induced by replisome blockage. DNA Repair (Amst) 7 811 818

56. LukeBVersiniGJaquenoudMZaidiIWKurzT 2006 The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr Biol 16 786 792

57. ZaidiIWRabutGPovedaAScheelHMalmstromJ 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

58. AguileraAChavezSMalagonF 2000 Mitotic recombination in yeast: elements controlling its incidence. Yeast 16 731 754

59. Cotta-RamusinoCFachinettiDLuccaCDoksaniYLopesM 2005 Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol Cell 17 153 159

60. FrogetBBlaisonneauJLambertSBaldacciG 2008 Cleavage of stalled forks by fission yeast Mus81/Eme1 in absence of DNA replication checkpoint. Mol Biol Cell 19 445 456

61. MeisterPTaddeiAVernisLPoidevinMGasserSM 2005 Temporal separation of replication and recombination requires the intra-S checkpoint. J Cell Biol 168 537 544

62. SogoJMLopesMFoianiM 2002 Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297 599 602

63. PaquesFHaberJE 1999 Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63 349 404

64. HouseleyJTollerveyD 2011 Repeat expansion in the budding yeast ribosomal DNA can occur independently of the canonical homologous recombination machinery. Nucleic Acids Res

65. EmiliASchieltzDMYatesJR3rdHartwellLH 2001 Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol Cell 7 13 20

66. DaveyCASargentDFLugerKMaederAWRichmondTJ 2002 Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319 1097 1113

67. WilliamsSKTruongDTylerJK 2008 Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A 105 9000 9005

68. XuFZhangQZhangKXieWGrunsteinM 2007 Sir2 deacetylates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. Mol Cell 27 890 900

69. AdkinsMWTylerJK 2004 The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J Biol Chem 279 52069 52074

70. YangJHFreudenreichCH 2010 The Rtt109 histone acetyltransferase facilitates error-free replication to prevent CAG/CTG repeat contractions. DNA Repair (Amst) 9 414 420

71. MimitouEPSymingtonLS 2008 Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455 770 774

72. RouseJ 2009 Control of genome stability by SLX protein complexes. Biochem Soc Trans 37 495 510

73. CelicIVerreaultABoekeJD 2008 Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179 1769 1784

74. ErkmannJAKaufmanPD 2009 A negatively charged residue in place of histone H3K56 supports chromatin assembly factor association but not genotoxic stress resistance. DNA Repair (Amst) 8 1371 1379

75. RobertsTMZaidiIWVaisicaJAPeterMBrownGW 2008 Regulation of Rtt107 recruitment to stalled DNA replication forks by the cullin Rtt101 and the Rtt109 acetyltransferase. Mol Biol Cell 19 171 180

76. CorpetADe KoningLToedlingJSavignoniABergerF 2011 Asf1b, the necessary Asf1 isoform for proliferation, is predictive of outcome in breast cancer. EMBO J 30 480 493

77. PradoFAguileraA 1995 Role of reciprocal exchange, one-ended invasion crossover and single-strand annealing on inverted and direct repeat recombination in yeast: different requirements for the RAD1, RAD10, and RAD52 genes. Genetics 139 109 123

78. AmbergDCBurkeDJStrathernJN 2005 Methods in yeast genetics Cold Spring Harbor Laboratory

79. BrewerBJFangmanWL 1987 The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51 463 471

80. TerceroJALongheseMPDiffleyJF 2003 A central role for DNA replication forks in checkpoint activation and response. Mol Cell 11 1323 1336

81. PellicioliALuccaCLiberiGMariniFLopesM 1999 Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J 18 6561 6572

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