Hyper-Acetylation of Histone H3K56 Limits Break-Induced Replication by Inhibiting Extensive Repair Synthesis

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Chromatin poses a barrier to the recombination process. Chromatin modification is therefore a prerequisite factor for the efficient execution of the recombination event. Chromatin remodeling and several unique histone modifications at or near DNA double strand breaks (DSBs) facilitate early recombination processes, but little is known how chromatin state impinges on post-invasion steps of recombination, such as repair synthesis through homologous template, particularly recombination subtypes such as break-induced replication (BIR) involving extensive repair synthesis. Here, we investigated the effect of deletions in chromatin modification and remodeling genes on BIR and discovered that hyper-acetylation of H3K56 selectively impairs BIR and gene conversion associated with long DNA gap synthesis. We also found that hyper-acetylation of H3K56 interferes with the recovery from replication stress in checkpoint deficient cells and induces translocation-type gross chromosomal rearrangements (GCRs). The results provide a basic understanding of how histone modification facilitates efficient fork progression in recombination, controls the types of the repair products and sustains chromosome integrity upon induction of genotoxic stress.

Vyšlo v časopise: Hyper-Acetylation of Histone H3K56 Limits Break-Induced Replication by Inhibiting Extensive Repair Synthesis. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004990
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004990

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Zdroje

1. Pâques F, Haber JE (1999) Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews 63: 349–404. 10357855

2. McEachern MJ, Haber JE (2006) Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem 75: 111–135. 16756487

3. Llorente B, Smith CE, Symington LS (2008) Break-induced replication: what is it and what is it for? Cell Cycle 7: 859–864. 18414031

4. Lydeard JR, Lipkin-Moore Z, Sheu, Stillman B, Burgers PM, et al. (2010) Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes & Development 24: 1133–1144. doi: 10.1155/2015/201379 25632406

5. Lydeard JR, Jain S, Yamaguchi M, Haber JE (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820–823. 17671506

6. Deem A, Keszthelyi A, Blackgrove T, Vayl A, Coffey B, et al. (2011) Break-induced replication is highly inaccurate. PLoS Biol 9: e1000594. doi: 10.1371/journal.pbio.1000594 21347245

7. Smith CE, Llorente B, Symington LS (2007) Template switching during break-induced replication. Nature 447: 102–105. 17410126

8. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y, et al. (2013) Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature 502: 389–392. doi: 10.1038/nature12584 24025772

9. Donnianni RA, Symington LS (2013) Break-induced replication occurs by conservative DNA synthesis. Proc Natl Acad Sci U S A 110: 13475–13480. doi: 10.1073/pnas.1309800110 23898170

10. Wilson MA, Kwon Y, Xu Y, Chung WH, Chi P, et al. (2013) Pif1 helicase and Poldelta promote recombination-coupled DNA synthesis via bubble migration. Nature 502: 393–396. doi: 10.1038/nature12585 24025768

11. Groth A, Rocha W, Verreault A, Almouzni G (2007) Chromatin challenges during DNA replication and repair. Cell 128: 721–733. 17320509

12. 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: 294–298. 16015338

13. Xu F, Zhang K, Grunstein M (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121: 375–385. 15882620

14. 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 19270680

15. Xie W, Song C, Young NL, Sperling AS, Xu F, 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.2009.02.004 19250903

16. 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: 109–119. 16818235

17. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, et al. (2006) The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr Biol 16: 1280–1289. 16815704

18. Watanabe S, Resch M, Lilyestrom W, Clark N, Hansen JC, et al. (2010) Structural characterization of H3K56Q nucleosomes and nucleosomal arrays. Biochim Biophys Acta 1799: 480–486. doi: 10.1016/j.bbagrm.2010.01.009 20100606

19. Neumann H, Hancock SM, Buning R, Routh A, Chapman L, et al. (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol Cell 36: 153–163. doi: 10.1016/j.molcel.2009.07.027 19818718

20. Driscoll R, Hudson A, Jackson SP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649–652. 17272722

21. Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, et al. (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315: 653–655. 17272723

22. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, et al. (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. 16627621

23. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, et al. (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134: 244–255. doi: 10.1016/j.cell.2008.06.018 18662540

24. Kaplan T, Liu CL, Erkmann JA, Holik J, Grunstein M, et al. (2008) Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4: e1000270. doi: 10.1371/journal.pgen.1000270 19023413

25. Williams SK, Truong D, Tyler JK (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. doi: 10.1073/pnas.0800057105 18577595

26. Yu Y, Song C, Zhang Q, DiMaggio PA, Garcia BA, et al. (2012) Histone H3 lysine 56 methylation regulates DNA replication through its interaction with PCNA. Mol Cell 46: 7–17. doi: 10.1016/j.molcel.2012.01.019 22387026

27. Wurtele H, Kaiser GS, Bacal J, St-Hilaire E, Lee EH, 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 22025679

28. Celic I, Verreault A, Boeke JD (2008) Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179: 1769–1784. doi: 10.1534/genetics.108.088914 18579506

29. Thaminy S, Newcomb B, Kim J, Gatbonton T, Foss E, et al. (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: 37805–37814. 17977840

30. Munoz-Galvan S, Jimeno S, Rothstein R, Aguilera A (2013) Histone H3K56 acetylation, Rad52, and non-DNA repair factors control double-strand break repair choice with the sister chromatid. PLoS Genet 9: e1003237. doi: 10.1371/journal.pgen.1003237 23357952

31. Ide S, Saka K, Kobayashi T (2013) Rtt109 prevents hyper-amplification of ribosomal RNA genes through histone modification in budding yeast. PLoS Genet 9: e1003410. doi: 10.1371/journal.pgen.1003410 23593017

32. Kadyrova LY, Mertz TM, Zhang Y, Northam MR, Sheng Z, 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 24204308

33. Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L, et al. (1995) The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev 9: 2888–2902. 7498786

34. Yang B, Miller A, Kirchmaier AL (2008) HST3/HST4-dependent deacetylation of lysine 56 of histone H3 in silent chromatin. Mol Biol Cell 19: 4993–5005. doi: 10.1091/mbc.E08-05-0524 18799617

35. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, et al. (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231–243. doi: 10.1016/j.cell.2008.06.035 18662539

36. Kim JA, Haber JE (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. doi: 10.1073/pnas.0812578106 19164567

37. Feser J, Truong D, Das C, Carson JJ, Kieft J, et al. (2010) Elevated histone expression promotes life span extension. Mol Cell 39: 724–735. doi: 10.1016/j.molcel.2010.08.015 20832724

38. Deem A, Barker K, VanHulle K, Downing B, Vayl A, et al. (2008) Defective Break-Induced Replication Leads to Half-Crossovers in Saccharomyces cerevisiae. Genetics 179: 1845–1860. doi: 10.1534/genetics.108.087940 18689895

39. Marrero VA, Symington LS (2010) Extensive DNA end processing by exo1 and sgs1 inhibits break-induced replication. PLoS Genet 6: e1001007. doi: 10.1371/journal.pgen.1001007 20628570

40. Lydeard JR, Lipkin-Moore Z, Jain S, Eapen VV, Haber JE (2010) Sgs1 and exo1 redundantly inhibit break-induced replication and de novo telomere addition at broken chromosome ends. PLoS Genet 6: e1000973. doi: 10.1371/journal.pgen.1000973 20523895

41. Adkins NL, Niu H, Sung P, Peterson CL (2013) Nucleosome dynamics regulates DNA processing. Nat Struct Mol Biol 20: 836–842. doi: 10.1038/nsmb.2585 23728291

42. van Attikum H, Fritsch O, Gasser SM (2007) Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26: 4113–4125. 17762868

43. Chen X, Cui D, Papusha A, Zhang X, Chu CD, et al. (2012) The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489: 576–580. doi: 10.1038/nature11355 22960743

44. Wysocki R, Javaheri A, Allard S, Sha F, Cote J, et al. (2005) Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol Cell Biol 25: 8430–8443. 16166626

45. Lazzaro F, Sapountzi V, Granata M, Pellicioli A, Vaze M, et al. (2008) Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. Embo j 27: 1502–1512. doi: 10.1038/emboj.2008.81 18418382

46. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, et al. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557–561. 11484058

47. Osborn AJ, Elledge SJ (2003) Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev 17: 1755–1767. 12865299

48. Alcasabas AA, Osborn AJ, Bachant J, Hu F, Werler PJ, et al. (2001) Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol 3: 958–965. 11715016

49. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, et al. (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078–1083. 12944972

50. Tourriere H, Versini G, Cordon-Preciado V, Alabert C, Pasero P (2005) Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell 19: 699–706. 16137625

51. Alabert C, Bianco JN, Pasero P (2009) Differential regulation of homologous recombination at DNA breaks and replication forks by the Mrc1 branch of the S-phase checkpoint. EMBO J 28: 1131–1141. doi: 10.1038/emboj.2009.75 19322196

52. Han J, Zhou H, Li Z, Xu RM, Zhang Z (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. 17690098

53. Myung K, Datta A, Kolodner RD (2001) Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104: 397–408. 11239397

54. Myung K, Pennaneach V, Kats ES, Kolodner RD (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. 12750463

55. Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806–810. 17314980

56. Watanabe S, Radman-Livaja M, Rando OJ, Peterson CL (2013) A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Science 340: 195–199. doi: 10.1126/science.1229758 23580526

57. Jain S, Sugawara N, Lydeard J, Vaze M, Tanguy Le Gac N, et al. (2009) A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev 23: 291–303. doi: 10.1101/gad.1751209 19204116

58. Chung WH, Zhu Z, Papusha A, Malkova A, Ira G (2010) Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet 6: e1000948. doi: 10.1371/journal.pgen.1000948 20485519

59. Pai CC, Deegan RS, Subramanian L, Gal C, Sarkar S, et al. (2014) A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun 5: 4091. doi: 10.1038/ncomms5091 24909977

60. Scully R, Xie A (2013) Double strand break repair functions of histone H2AX. Mutat Res 750: 5–14. doi: 10.1016/j.mrfmmm.2013.07.007 23916969

61. Hicks WM, Kim M, Haber JE (2010) Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329: 82–85. doi: 10.1126/science.1191125 20595613

62. Lo YC, Paffett KS, Amit O, Clikeman JA, Sterk R, et al. (2006) Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol Cell Biol 26: 4086–4094. 16705162

63. Villarreal DD, Lee K, Deem A, Shim EY, Malkova A, et al. (2012) Microhomology directs diverse DNA break repair pathways and chromosomal translocations. PLoS Genet 8: e1003026. doi: 10.1371/journal.pgen.1003026 23144625

64. Lee SE, Moore JK, Holmes A, Umezu K, Kolodner RD, et al. (1998) Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94: 399–409. 9708741

65. Prakash R, Satory D, Dray E, Papusha A, Scheller J, et al. (2009) Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23: 67–79. doi: 10.1101/gad.1737809 19136626

66. Vaze MB, Pellicioli A, Lee SE, Ira G, Liberi G, et al. (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol Cell 10: 373–385. 12191482

67. Sanchez-Diaz A, Kanemaki M, Marchesi V, Labib K (2004) Rapid depletion of budding yeast proteins by fusion to a heat-inducible degron. Sci STKE 2004: PL8. 15010550

68. Li F, Dong J, Pan X, Oum JH, Boeke JD, et al. (2008) Microarray-based genetic screen defines SAW1, a gene required for Rad1/Rad10-dependent processing of recombination intermediates. Mol Cell 30: 325–335. doi: 10.1016/j.molcel.2008.02.028 18471978

69. Shim EY, Ma J-L, Oum J-H, Yanez Y, Lee SE (2005) The Yeast Chromatin Remodeler RSC Complex Facilitates End Joining Repair of DNA Double-Strand Breaks. Molecular and Cellular Biology 25: 3934–3944. 15870268

70. Motegi A, Myung K (2007) Measuring the rate of gross chromosomal rearrangements in Saccharomyces cerevisiae: A practical approach to study genomic rearrangements observed in cancer. Methods 41: 168–176. 17189859