Histone H3 lysine 56 acetylation and the response to DNA replication fork damage

Molecular and Cellular Biology

Volumn 32, Issue 1, 2012, Pages 154-172

  Wurtele, Hugo ^a   Kaiser, Gitte Schalck ^d   Bacal, Julien ^c   St Hilaire, Edlie ^a   Lee, Eun Hye ^a   Tsao, Sarah ^a   Dorn, Jonas ^a   Maddox, Paul ^a,b   Lisby, Michael ^d   Pasero, Philippe ^c   Verreault, Alain ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c INSTITUTE OF HUMAN GENETICS   (France)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; HISTONE H3; HISTONE H3 LYSINE 56; HYDROXYUREA; MESYLIC ACID METHYL ESTER; RAD52 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL SURVIVAL; CHROMATIN; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HISTONE ACETYLATION; HOMOLOGOUS RECOMBINATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ACETYLATION; ANTINEOPLASTIC AGENTS; CAMPTOTHECIN; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; HISTONES; HYDROXYUREA; LYSINE; METHYL METHANESULFONATE; MUTAGENS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84856793630     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05415-11     Document Type: Article

References (100)

1. 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.
2. Alvaro D, Lisby M, Rothstein R. 2007. Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet. 3:e228.
3. Alvino GM, et al. 2007. Replication in hydroxyurea: it's a matter of time. Mol. Cell. Biol. 27:6396-6406.
4. Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K. 2010. The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell 37:834-842.
5. Barlow JH, Rothstein R. 2009. Rad52 recruitment is DNA replication independent and regulated by Cdc28 and the Mec1 kinase. EMBO J. 28:1121-1130.
6. Ben-Aroya S, et al. 2010. Proteasome nuclear activity affects chromosome stability by controlling the turnover of Mms22, a protein important for DNA repair. PLoS Genet. 6:e1000852.
7. Bernstein KA, et al. 2009. Sgs1 function in the repair of DNA replication intermediates is separable from its role in homologous recombinational repair. EMBO J. 28:915-925.
8. Branzei D, et al. 2006. Ubc9- and Mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127: 509-522.
9. Branzei D, Vanoli F, Foiani M. 2008. SUMOylation regulates Rad18- mediated template switch. Nature 456:915-920.
10. Budzowska M, Kanaar R. 2009. Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem. Biophys. 53: 17-31.
11. Burgess RJ, Zhou H, Han J, Zhang Z. 2010. A role for Gcn5 in replication-coupled nucleosome assembly. Mol. Cell 37:469-480.
12. Celic I, et al. 2006. The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr. Biol. 16: 1280-1289.
13. Chen CC, 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.
14. Chen CC, Tyler J. 2008. Chromatin reassembly signals the end of DNA repair. Cell Cycle 7:3792-3797.
15. Collins SR, et al. 2007. Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446:806-810.
16. Conde F, San-Segundo PA. 2008. Role of Dot1 in the response to alkylatingDNAdamage in Saccharomyces cerevisiae: regulation ofDNAdamage tolerance by the error-prone polymerases Polζ/Rev1. Genetics 179: 1197-1210.
17. Das C, Lucia MS, Hansen KC, Tyler JK. 2009. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459:113-117.
18. Downs JA, Lowndes NF, Jackson SP. 2000. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001-1004.
19. Driscoll R, Hudson A, Jackson SP. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649-652.
20. Drogaris P, Wurtele H, Masumoto H, Verreault A, Thibault P. 2008. Comprehensive profiling of histone modifications using a label-free approach and its applications in determining structure-function relationships. Anal. Chem. 80:6698-6707.
21. Duro E, Vaisica JA, Brown GW, Rouse J. 2008. Budding yeast Mms22 and Mms1 regulate homologous recombination induced by replisome blockage. DNA Repair (Amst.) 7:811-818.
22. Endo K, Tago Y, Daigaku Y, Yamamoto K. 2007. Error-free RAD52 pathway and error-prone REV3 pathway determines spontaneous mutagenesis in Saccharomyces cerevisiae. Genes Genet. Syst. 82:35-42.
23. Franco AA, Lam WM, Burgers PM, Kaufman PD. 2005. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19:1365-1375.
24. Green CM, Lehmann AR. 2005. Translesion synthesis and error-prone polymerases. Adv. Exp. Med. Biol. 570:199-223.
25. Groth A, Rocha W, Verreault A, Almouzni G. 2007. Chromatin challenges during DNA replication and repair. Cell 128:721-733.
26. Haldar D, Kamakaka RT. 2008. Schizosaccharomyces pombe Hst4 functions inDNAdamage response by regulating histone H3 K56 acetylation. Eukaryot. Cell 7:800-813.
27. Han J, et al. 2007. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315:653-655.
28. 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.
29. Herskowitz I, Jensen RE. 1991. Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol. 194:132-146.
30. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
31. Hyland EM, et al. 2005. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol. Cell. Biol. 25:10060-10070.
32. Ivessa AS, Zakian VA. 2002. To fire or not to fire: origin activation in Saccharomyces cerevisiae ribosomal DNA. Genes Dev. 16:2459-2464.
33. Jackson V, Shires A, Tanphaichitr N, Chalkley R. 1976. Modifications to histones immediately after synthesis. J. Mol. Biol. 104:471-483.
34. Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293: 1074-1080.
35. 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.
36. Kim UJ, Han M, Kayne P, Grunstein M. 1988. Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J. 7:2211-2219.
37. Krawitz DC, Kama T, Kaufman PD. 2002. Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol. Cell. Biol. 22:614-625.
38. Kushnirov VV. 2000. Rapid and reliable protein extraction from yeast. Yeast 16:857-860.
39. Lehmann AR, et al. 2007. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst.) 6:891-899.
40. Lewis LK, Karthikeyan G, Cassiano J, Resnick MA. 2005. Reduction of nucleosome assembly during new DNA synthesis impairs both major pathways of double-strand break repair. Nucleic Acids Res. 33: 4928-4939.
41. Li Q, et al. 2008. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244-255.
42. Liberi G, et al. 2006. Methods to study replication fork collapse in budding yeast. Methods Enzymol. 409:442-462.
43. Liberi G, et al. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19:339-350.
44. Lisby M, Barlow JH, Burgess RC, Rothstein R. 2004. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118:699-713.
45. Lisby M, Rothstein R, Mortensen UH. 2001. Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. U. S. A. 98:8276-8282.
46. Lopes da Rosa J, Boyartchuk VL, Zhu LJ, Kaufman PD. 2010. Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 107:1594-1599.
47. Luke B, et al. 2006. The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr. Biol. 16: 786-792.
48. Lundin C, et al. 2005. Methyl methanesulfonate (MMS) produces heatlabile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res. 33:3799-3811.
49. MA W, Resnick MA, Gordenin DA. 2008. Apn1 and Apn2 endonucleases prevent accumulation of repair-associated DNA breaks in budding yeast as revealed by direct chromosomal analysis. Nucleic Acids Res. 36:1836-1846.
50. 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.
51. Mankouri HW, Ashton TM, Hickson ID. 2011. Holliday junctioncontaining DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage. Proc. Natl. Acad. Sci. U. S. A. 108:4944-4949.
52. Maringele L, Lydall D. 2006. Pulsed-field gel electrophoresis of budding yeast chromosomes. Methods Mol. Biol. 313:65-73.
53. 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.
54. Memisoglu A, Samson L. 2000. Base excision repair in yeast and mammals. Mutat. Res. 451:39-51.
55. Merker RJ, Klein HL. 2002. hpr1Δ affects ribosomal DNA recombination and cell life span in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 421-429.
56. Miller KM, et al. 2010. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol. 17:1144-1151.
57. Monti P, et al. 2008. Rev1 and Polζ influence toxicity and mutagenicity of Me-lex, a sequence selective N3-adenine methylating agent. DNA Repair (Amst.) 7:431-438.
58. Neumann H, 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.
59. Nikolova T, Ensminger M, Lobrich M, Kaina B. 2010. Homologous recombination protects mammalian cells from replication-associated DNA double-strand breaks arising in response to methyl methanesulfonate. DNA Repair (Amst.) 9:1050-1063.
60. Nitiss JL, Wang JC. 1996. Mechanisms of cell killing by drugs that trap covalent complexes betweenDNAtopoisomerases and DNA. Mol. Pharmacol. 50:1095-1102.
61. Ozdemir A, et al. 2005. Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J. Biol. Chem. 280: 25949-25952.
62. 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. 16:2479-2484.
63. Pellicioli A, et al. 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.
64. Pommier Y. 2009. DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem. Rev. 109:2894-2902.
65. Pommier Y. 2006. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6:789-802.
66. Pommier Y, et al. 2003. Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat. Res. 532:173-203.
67. Recht J, 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.
68. Redon C, et al. 2003. Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep. 4:678-684.
69. Roberts TM, Zaidi IW, Vaisica JA, Peter M, Brown GW. 2008. Regulation of rtt107 recruitment to stalledDNAreplication forks by the cullin rtt101 and the rtt109 acetyltransferase. Mol. Biol. Cell 19:171-180.
70. Rocha W, Verreault A. 2008. Clothing up DNA for all seasons: histone chaperones and nucleosome assembly pathways. FEBS Lett. 582: 1938-1949.
71. Rouse J. 2004. Esc4p, a new target of Mec1p (ATR), promotes resumption of DNA synthesis after DNA damage. EMBO J. 23:1188-1197.
72. Ruiz-Carrillo A, Wangh LJ, Allfrey VG. 1975. Processing of newly synthesized histone molecules. Science 190:117-128.
73. Santocanale C, Diffley JF. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395: 615-618.
74. Sedgwick B. 2004. Repairing DNA methylation damage. Nat. Rev. Mol. Cell Biol. 5:148-157.
75. Shibahara K, Stillman B. 1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96: 575-585.
76. Shimko JC, North JA, Bruns AN, Poirier MG, Ottesen JJ. 2011. Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J. Mol. Biol. 408: 187-204.
77. Sobel RE, Cook RG, Allis CD. 1994. Non-random acetylation of histone H4 by a cytoplasmic histone acetyltransferase as determined by novel methodology. J. Biol. Chem. 269:18576-18582.
78. Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD. 1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. U. S. A. 92:1237-1241.
79. Sweeney FD, et al. 2005. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15:1364-1375.
80. Symington LS. 2002. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66:630-670.
81. Tang Y, et al. 2011. Structure of the Rtt109-AcCoA/Vps75 complex and implications for chaperone-mediated histone acetylation. Structure 19: 221-231.
82. Tercero JA, Diffley JF. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412:553-557.
83. Thaminy S, 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.
84. Tjeertes JV, Miller KM, Jackson SP. 2009. Screen for DNA-damageresponsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J. 28:1878-1889.
85. Torres-Rosell J, et al. 2007. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9:923-931.
86. Tsubota T, et al. 2007. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell 25:703-712.
87. Vanoli F, Fumasoni M, Szakal B, Maloisel L, Branzei D. 2010. Replication and recombination factors contributing to recombinationdependent bypass of DNA lesions by template switch. PLoS Genet. 6:e1001205.
88. Vempati RK, et al. 2010. p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals. J. Biol. Chem. 285: 28553-28564.
89. Viggiani CJ, Aparicio OM. 2006. New vectors for simplified construction of BrdU-incorporating strains of Saccharomyces cerevisiae. Yeast 23: 1045-1051.
90. Wurtele H, et al. 2010. Modulation of histone H3 lysine 56 acetylation as an antifungal therapeutic strategy. Nat. Med. 16:774-780.
91. Wurtele H, Verreault A. 2006. Histone post-translational modifications and the response to DNA double-strand breaks. Curr. Opin. Cell Biol. 18:137-144.
92. Xhemalce B, et al. 2007. Regulation of histone H3 lysine 56 acetylation in Schizosaccharomyces pombe. J. Biol. Chem. 282:15040-15047.
93. Xiao W, Chow BL, Rathgeber L. 1996. The repair of DNA methylation damage in Saccharomyces cerevisiae. Curr. Genet. 30:461-468.
94. 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.
95. Yarbro JW. 1992. Mechanism of action of hydroxyurea. Semin. Oncol. 19(3 Suppl. 9):1-10.
96. Ye J, et al. 2005. Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. Mol. Cell 18:123-130.
97. 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.
98. 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.
99. Zhang W, Qin Z, Zhang X, Xiao W. 2011. Roles of sequential ubiquitination of PCNA in DNA-damage tolerance. FEBS Lett. 585:2786-2794.
100. Zhang Z, Shibahara K, Stillman B. 2000. PCNA connects DNA replication to epigenetic inheritance in yeast. Nature 408:221-225.