Posttranslational modifications of repair factors and histones in the cellular response to stalled replication forks

DNA Repair

Volumn 8, Issue 9, 2009, Pages 1089-1100

  Schleker, Thomas ^a   Nagai, Shigeki ^a   Gasser, Susan M ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Checkpoint; Chromatin remodeling; Histone modification; Repair; Replication

Indexed keywords

DNA; HISTONE;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING;

DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HISTONES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SACCHAROMYCES CEREVISIAE;

EID: 68249093137     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.04.010     Document Type: Article

References (147)

1. Dubrana K., van Attikum H., Hediger F., and Gasser S.M. The processing of double-strand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast. J. Cell Sci. 120 (2007) 4209-4220
2. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
3. Majka J., and Burgers P.M. The PCNA-RFC families of DNA clamps and clamp loaders. Prog. Nucleic Acid Res. Mol. Biol. 78 (2004) 227-260
4. Harrison J.C., and Haber J.E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40 (2006) 209-235
5. Aboussekhra A., Biggerstaff M., Shivji M.K., Vilpo J.A., Moncollin V., Podust V.N., Protic M., Hubscher U., Egly J.M., and Wood R.D. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80 (1995) 859-868
6. He Z., Henricksen L.A., Wold M.S., and Ingles C.J. RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature 374 (1995) 566-569
7. Sogo J.M., Lopes M., and Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297 (2002) 599-602
8. Shimada K., Pasero P., and Gasser S.M. ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phase. Genes Dev. 16 (2002) 3236-3252
9. Tourriere H., and Pasero P. Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst) (2007)
10. Moldovan G.L., Pfander B., and Jentsch S. PCNA, the maestro of the replication fork. Cell 129 (2007) 665-679
11. Parrilla-Castellar E.R., Arlander S.J., and Karnitz L. Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst) 3 (2004) 1009-1014
12. Celic I., Verreault A., and Boeke J.D. Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179 (2008) 1769-1784
13. Schwartz D.C., and Hochstrasser M. A superfamily of protein tags: ubiquitin, SUMO and related modifiers. Trends Biochem. Sci. 28 (2003) 321-328
14. Heun P. SUMOrganization of the nucleus. Curr. Opin. Cell Biol. 19 (2007) 350-355
15. Pfander B., Moldovan G.L., Sacher M., Hoege C., and Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436 (2005) 428-433
16. Papouli E., Chen S., Davies A.A., Huttner D., Krejci L., Sung P., and Ulrich H.D. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell. 19 (2005) 123-133
17. Zhao G.Y., Sonoda E., Barber L.J., Oka H., Murakawa Y., Yamada K., Ikura T., Wang X., Kobayashi M., Yamamoto K., Boulton S.J., and Takeda S. A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol. Cell. 25 (2007) 663-675
18. Krogan N.J., Lam M.H., Fillingham J., Keogh M.C., Gebbia M., Li J., Datta N., Cagney G., Buratowski S., Emili A., and Greenblatt J.F. Proteasome involvement in the repair of DNA double-strand breaks. Mol. Cell. 16 (2004) 1027-1034
19. Gudmundsdottir K., Lord C.J., and Ashworth A. The proteasome is involved in determining differential utilization of double-strand break repair pathways. Oncogene 26 (2007) 7601-7606
20. Murakawa Y., Sonoda E., Barber L.J., Zeng W., Yokomori K., Kimura H., Niimi A., Lehmann A., Zhao G.Y., Hochegger H., Boulton S.J., and Takeda S. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res. 67 (2007) 8536-8543
21. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
22. Lehmann A.R., Niimi A., Ogi T., Brown S., Sabbioneda S., Wing J.F., Kannouche P.L., and Green C.M. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst) 6 (2007) 891-899
23. Fleck O., and Schar P. Translesion DNA synthesis: little fingers teach tolerance. Curr. Biol. 14 (2004) R389-391
24. Branzei D., Vanoli F., and Foiani M. SUMOylation regulates Rad18-mediated template switch. Nature 456 (2008) 915-920
25. Ulrich H.D. Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell. Biol. 15 (2005) 525-532
26. Dudas A., and Chovanec M. DNA double-strand break repair by homologous recombination. Mutat. Res. 566 (2004) 131-167
27. Lambert S., Froget B., and Carr A.M. Arrested replication fork processing: Interplay between checkpoints and recombination. DNA Repair (Amst) (2007)
28. Wyman C., and Kanaar R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40 (2006) 363-383
29. Meister P., Taddei A., Vernis L., Poidevin M., Gasser S.M., and Baldacci G. Temporal separation of replication and recombination requires the intra-S checkpoint. J. Cell Biol. 168 (2005) 537-544
30. Barbour L., Ball L.G., Zhang K., and Xiao W. DNA damage checkpoints are involved in postreplication repair. Genetics 174 (2006) 1789-1800
31. Liberi G., Maffioletti G., Lucca C., Chiolo I., Baryshnikova A., Cotta-Ramusino C., Lopes M., Pellicioli A., Haber J.E., and Foiani M. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19 (2005) 339-350
32. Ira G., Malkova A., Liberi G., Foiani M., and Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003) 401-411
33. Barbour L., and Xiao W. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat. Res. 532 (2003) 137-155
34. Muller S., Hoege C., Pyrowolakis G., and Jentsch S. SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell. Biol. 2 (2001) 202-210
35. Moldovan G.L., Pfander B., and Jentsch S. PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell. 23 (2006) 723-732
36. Strom L., Lindroos H.B., Shirahige K., and Sjogren C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell. 16 (2004) 1003-1015
37. Unal E., Arbel-Eden A., Sattler U., Shroff R., Lichten M., Haber J.E., and Koshland D. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell. 16 (2004) 991-1002
38. Strom L., Karlsson C., Lindroos H.B., Wedahl S., Katou Y., Shirahige K., and Sjogren C. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317 (2007) 242-245
39. Unal E., Heidinger-Pauli J.M., and Koshland D. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317 (2007) 245-248
40. Chang D.J., Lupardus P.J., and Cimprich K.A. Monoubiquitination of proliferating cell nuclear antigen induced by stalled replication requires uncoupling of DNA polymerase and mini-chromosome maintenance helicase activities. J. Biol. Chem. 281 (2006) 32081-32088
41. Byun T.S., Pacek M., Yee M.C., Walter J.C., and Cimprich K.A. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19 (2005) 1040-1052
42. MacDougall C.A., Byun T.S., Van C., Yee M.C., and Cimprich K.A. The structural determinants of checkpoint activation. Genes Dev. 21 (2007) 898-903
43. Davies A.A., Huttner D., Daigaku Y., Chen S., and Ulrich H.D. Activation of ubiquitin-dependent DNA damage bypass is mediated by replication protein a. Mol. Cell. 29 (2008) 625-636
44. Yang X.H., Shiotani B., Classon M., and Zou L. Chk1 and Claspin potentiate PCNA ubiquitination. Genes Dev. 22 (2008) 1147-1152
45. Parker J.L., Bucceri A., Davies A.A., Heidrich K., Windecker H., and Ulrich H.D. SUMO modification of PCNA is controlled by DNA. EMBO J. 27 (2008) 2422-2431
46. De Piccoli G., Cortes-Ledesma F., Ira G., Torres-Rosell J., Uhle S., Farmer S., Hwang J.Y., Machin F., Ceschia A., McAleenan A., Cordon-Preciado V., Clemente-Blanco A., Vilella-Mitjana F., Ullal P., Jarmuz A., Leitao B., Bressan D., Dotiwala F., Papusha A., Zhao X., Myung K., Haber J.E., Aguilera A., and Aragon L. Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol. 8 (2006) 1032-1034
47. Lehmann A.R., Walicka M., Griffiths D.J., Murray J.M., Watts F.Z., McCready S., and Carr A.M. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol. Cell. Biol. 15 (1995) 7067-7080
48. Potts P.R., Porteus M.H., and Yu H. Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J. 25 (2006) 3377-3388
49. Torres-Rosell J., Machin F., Farmer S., Jarmuz A., Eydmann T., Dalgaard J.Z., and Aragon L. SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions. Nat. Cell Biol. 7 (2005) 412-419
50. McDonald W.H., Pavlova Y., Yates III J.R., and Boddy M.N. Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J. Biol. Chem. 278 (2003) 45460-45467
51. Andrews E.A., Palecek J., Sergeant J., Taylor E., Lehmann A.R., and Watts F.Z. Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 25 (2005) 185-196
52. Zhao X., and Blobel G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 4777-4782
53. Potts P.R., and Yu H. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 25 (2005) 7021-7032
54. Lindroos H.B., Strom L., Itoh T., Katou Y., Shirahige K., and Sjogren C. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways. Mol. Cell. 22 (2006) 755-767
55. Haering C.H., Farcas A.M., Arumugam P., Metson J., and Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature 454 (2008) 297-301
56. Branzei D., Sollier J., Liberi G., Zhao X., Maeda D., Seki M., Enomoto T., Ohta K., and Foiani M. Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127 (2006) 509-522
57. Ampatzidou E., Irmisch A., O'Connell M.J., and Murray J.M. Smc5/6 is required for repair at collapsed replication forks. Mol. Cell. Biol. 26 (2006) 9387-9401
58. Prudden J., Pebernard S., Raffa G., Slavin D.A., Perry J.J., Tainer J.A., McGowan C.H., and Boddy M.N. SUMO-targeted ubiquitin ligases in genome stability. EMBO J 26 (2007) 4089-4101
59. Sun H., Leverson J.D., and Hunter T. Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J 26 (2007) 4102-4112
60. Xie Y., Kerscher O., Kroetz M.B., McConchie H.F., Sung P., and Hochstrasser M. The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J. Biol. Chem. 282 (2007) 34176-34184
61. Uzunova K., Gottsche K., Miteva M., Weisshaar S.R., Glanemann C., Schnellhardt M., Niessen M., Scheel H., Hofmann K., Johnson E.S., Praefcke G.J., and Dohmen R.J. Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 282 (2007) 34167-34175
62. Ii T., Fung J., Mullen J.R., and Brill S.J. The yeast Slx5-Slx8 DNA integrity complex displays ubiquitin ligase activity. Cell Cycle 6 (2007) 2800-2809
63. Mullen J.R., and Brill S.J. Activation of the Slx5-Slx8 ubiquitin ligase by poly-small ubiquitin-like modifier conjugates. J. Biol. Chem. 283 (2008) 19912-19921
64. Tatham M.H., Geoffroy M.C., Shen L., Plechanovova A., Hattersley N., Jaffray E.G., Palvimo J.J., and Hay R.T. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10 (2008) 538-546
65. Lallemand-Breitenbach V., Jeanne M., Benhenda S., Nasr R., Lei M., Peres L., Zhou J., Zhu J., Raught B., and de H. The Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10 (2008) 547-555
66. Weisshaar S.R., Keusekotten K., Krause A., Horst C., Springer H.M., Gottsche K., Dohmen R.J., and Praefcke G.J. Arsenic trioxide stimulates SUMO-2/3 modification leading to RNF4-dependent proteolytic targeting of PML. FEBS Lett. 582 (2008) 3174-3178
67. Mullen J.R., Kaliraman V., Ibrahim S.S., and Brill S.J. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157 (2001) 103-118
68. Collins S.R., Kemmeren P., Zhao X.C., Greenblatt J.F., Spencer F., Holstege F.C., Weissman J.S., and Krogan N.J. Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol. Cell. Proteomics 6 (2007) 439-450
69. Wang Z., Jones G.M., and Prelich G. Genetic analysis connects SLX5 and SLX8 to the SUMO pathway in Saccharomyces cerevisiae. Genetics 172 (2006) 1499-1509
70. Pero R., Lembo F., Di Vizio D., Boccia A., Chieffi P., Fedele M., Pierantoni G.M., Rossi P., Iuliano R., Santoro M., Viglietto G., Bruni C.B., Fusco A., and Chiariotti L. RNF4 is a growth inhibitor expressed in germ cells but not in human testicular tumors. Am. J. Pathol. 159 (2001) 1225-1230
71. Hirvonen-Santti S.J., Rannikko A., Santti H., Savolainen S., Nyberg M., Janne O.A., and Palvimo J.J. Down-regulation of estrogen receptor beta and transcriptional coregulator SNURF/RNF4 in testicular germ cell cancer. Eur. Urol. 44 (2003) 742-747 discussion 747
72. Melnick A., and Licht J.D. Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 93 (1999) 3167-3215
73. Zhang C., Roberts T.M., Yang J., Desai R., and Brown G.W. Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair (Amst) 5 (2006) 336-346
74. Burgess R.C., Rahman S., Lisby M., Rothstein R., and Zhao X. The Slx5-Slx8 complex affects sumoylation of DNA repair proteins and negatively regulates recombination. Mol. Cell. Biol. 27 (2007) 6153-6162
75. Alvaro D., Lisby M., and Rothstein R. Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet. 3 (2007) e228
76. Nagai S., Dubrana K., Tsai-Pflugfelder M., Davidson M.B., Roberts T.M., Brown G.W., Varela E., Hediger F., Gasser S.M., and Krogan N.J. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322 (2008) 597-602
77. McEachern M.J., and Haber J.E. Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75 (2006) 111-135
78. Bystricky K., Laroche T., van Houwe G., Blaszczyk M., and Gasser S.M. Chromosome looping in yeast: telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization. J. Cell Biol. 168 (2005) 375-387
79. Tremethick D.J. Higher-order structures of chromatin: the elusive 30 nm fiber. Cell 128 (2007) 651-654
80. Henikoff S., and Ahmad K. Assembly of variant histones into chromatin. Annu. Rev. Cell Dev. Biol. 21 (2005) 133-153
81. Ye X., Franco A.A., Santos H., Nelson D.M., Kaufman P.D., and Adams P.D. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell. 11 (2003) 341-351
82. Spector M.S., Raff A., DeSilva H., Lee K., and Osley M.A. Hir1p and Hir2p function as transcriptional corepressors to regulate histone gene transcription in the Saccharomyces cerevisiae cell cycle. Mol. Cell. Biol. 17 (1997) 545-552
83. Li Q., Zhou H., Wurtele H., Davies B., Horazdovsky B., Verreault A., and Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134 (2008) 244-255
84. Xu F., Zhang Q., Zhang K., Xie W., and Grunstein M. Sir2 deacetylates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. Mol. Cell. 27 (2007) 890-900
85. Gunjan A., Paik J., and Verreault A. Regulation of histone synthesis and nucleosome assembly. Biochimie 87 (2005) 625-635
86. Kats E.S., Albuquerque C.P., Zhou H., and Kolodner R.D. 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 (2006) 3710-3715
87. Green E.M., Antczak A.J., Bailey A.O., Franco A.A., Wu K.J., Yates III J.R., and Kaufman P.D. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15 (2005) 2044-2049
88. Krawitz D.C., Kama T., and Kaufman P.D. Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol. Cell. Biol. 22 (2002) 614-625
89. Sharp J.A., Fouts E.T., Krawitz D.C., and Kaufman P.D. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11 (2001) 463-473
90. Sharp J.A., Rizki G., and Kaufman P.D. Regulation of histone deposition proteins Asf1/Hir1 by multiple DNA damage checkpoint kinases in Saccharomyces cerevisiae. Genetics 171 (2005) 885-899
91. Sutton A., Bucaria J., Osley M.A., and Sternglanz R. Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics 158 (2001) 587-596
92. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., and Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402 (1999) 555-560
93. Emili A., Schieltz D.M., Yates III J.R., and Hartwell L.H. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell. 7 (2001) 13-20
94. Hu F., Alcasabas A.A., and Elledge S.J. Asf1 links Rad53 to control of chromatin assembly. Genes Dev. 15 (2001) 1061-1066
95. Tamburini B.A., Carson J.J., Adkins M.W., and Tyler J.K. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot Cell 4 (2005) 1583-1590
96. Gunjan A., and Verreault A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115 (2003) 537-549
97. Ramey C.J., Howar S., Adkins M., Linger J., Spicer J., and Tyler J.K. Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol. Cell. Biol. 24 (2004) 10313-10327
98. Franco A.A., Lam W.M., Burgers P.M., and Kaufman P.D. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19 (2005) 1365-1375
99. Schulz L.L., and Tyler J.K. The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication. FASEB J. 20 (2006) 488-490
100. Sanematsu F., Takami Y., Barman H.K., Fukagawa T., Ono T., Shibahara K., and Nakayama T. Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J. Biol. Chem. 281 (2006) 13817-13827
101. Recht J., Tsubota T., Tanny J.C., Diaz R.L., Berger J.M., Zhang X., Garcia B.A., Shabanowitz J., Burlingame A.L., Hunt D.F., Kaufman P.D., and Allis C.D. 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 (2006) 6988-6993
102. Masumoto H., Hawke D., Kobayashi R., and Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436 (2005) 294-298
103. Ozdemir A., Spicuglia S., Lasonder E., Vermeulen M., Campsteijn C., Stunnenberg H.G., and Logie C. Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J. Biol. Chem. 280 (2005) 25949-25952
104. Xu F., Zhang K., and Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121 (2005) 375-385
105. Hyland E.M., Cosgrove M.S., Molina H., Wang D., Pandey A., Cottee R.J., and Boeke J.D. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol. Cell. Biol. 25 (2005) 10060-10070
106. Driscoll R., Hudson A., and Jackson S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315 (2007) 649-652
107. Maas N.L., Miller K.M., DeFazio L.G., and Toczyski D.P. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell. 23 (2006) 109-119
108. Celic I., Masumoto H., Griffith W.P., Meluh P., Cotter R.J., Boeke J.D., and Verreault A. The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr. Biol. 16 (2006) 1280-1289
109. Collins S.R., Miller K.M., Maas N.L., Roguev A., Fillingham J., Chu C.S., Schuldiner M., Gebbia M., Recht J., Shales M., Ding H., Xu H., Han J., Ingvarsdottir K., Cheng B., Andrews B., Boone C., Berger S.L., Hieter P., Zhang Z., Brown G.W., Ingles C.J., Emili A., Allis C.D., Toczyski D.P., Weissman J.S., Greenblatt J.F., and Krogan N.J. Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 (2007) 806-810
110. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., and Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315 (2007) 653-655
111. Tsubota T., Berndsen C.E., Erkmann J.A., Smith C.L., Yang L., Freitas M.A., Denu J.M., and Kaufman P.D. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell. 25 (2007) 703-712
112. Adkins M.W., Carson J.J., English C.M., Ramey C.J., and Tyler J.K. The histone chaperone anti-silencing function 1 stimulates the acetylation of newly synthesized histone H3 in S-phase. J. Biol. Chem. 282 (2007) 1334-1340
113. Agez M., Chen J., Guerois R., van Heijenoort C., Thuret J.Y., Mann C., and Ochsenbein F. Structure of the histone chaperone ASF1 bound to the histone H3 C-terminal helix and functional insights. Structure 15 (2007) 191-199
114. Han J., Zhou H., Li Z., Xu R.M., and Zhang Z. Acetylation of lysine 56 of histone H3 catalyzed by Rtt109 and regulated by Asf1 is required for replisome integrity. J. Biol. Chem. (2007)
115. Chen C.C., Carson J.J., Feser J., Tamburini B., Zabaronick S., Linger J., and Tyler J.K. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134 (2008) 231-243
116. Fillingham J., Keogh M.C., and Krogan N.J. GammaH2AX and its role in DNA double-strand break repair. Biochem. Cell. Biol. 84 (2006) 568-577
117. Foster E.R., and Downs J.A. Histone H2A phosphorylation in DNA double-strand break repair. FEBS J. 272 (2005) 3231-3240
118. Lowndes N.F., and Toh G.W. DNA repair: the importance of phosphorylating histone H2AX. Curr. Biol. 15 (2005) R99-R102
119. Redon C., Pilch D.R., Rogakou E.P., Orr A.H., Lowndes N.F., and Bonner W.M. Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep. 4 (2003) 678-684
120. Redon C., Pilch D.R., and Bonner W.M. Genetic analysis of Saccharomyces cerevisiae H2A serine 129 mutant suggests a functional relationship between H2A and the sister-chromatid cohesion partners Csm3-Tof1 for the repair of topoisomerase I-induced DNA damage. Genetics 172 (2006) 67-76
121. Takahashi A., and Ohnishi T. Does gammaH2AX foci formation depend on the presence of DNA double strand breaks?. Cancer Lett. 229 (2005) 171-179
122. Ward I.M., and Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276 (2001) 47759-47762
123. van Attikum H., and Gasser S.M. The histone code at DNA breaks: a guide to repair?. Nat. Rev. Mol. Cell. Biol. 6 (2005) 757-765
124. Cobb J.A., Schleker T., Rojas V., Bjergbaek L., Tercero J.A., and Gasser S.M. Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes Dev. 19 (2005) 3055-3069
125. Torres-Rosell J., De Piccoli G., Cordon-Preciado V., Farmer S., Jarmuz A., Machin F., Pasero P., Lisby M., Haber J.E., and Aragon L. Anaphase onset before complete DNA replication with intact checkpoint responses. Science 315 (2007) 1411-1415
126. Strom L., and Sjogren C. DNA damage-induced cohesion. Cell Cycle 4 (2005) 536-539
127. Kraus E., Leung W.Y., and Haber J.E. Break-induced replication: a review and an example in budding yeast. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 8255-8262
128. Choy J.S., and Kron S.J. NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol. Cell. Biol. 22 (2002) 8215-8225
129. Giannattasio M., Lazzaro F., Plevani P., and Muzi-Falconi M. The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. (2005)
130. Ng H.H., Xu R.M., Zhang Y., and Struhl K. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem. 277 (2002) 34655-34657
131. Wysocki R., Javaheri A., Allard S., Sha F., Cote J., and Kron S.J. Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25 (2005) 8430-8443
132. Huyen Y., Zgheib O., Ditullio Jr. R.A., Gorgoulis V.G., Zacharatos P., Petty T.J., Sheston E.A., Mellert H.S., Stavridi E.S., and Halazonetis T.D. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 (2004) 406-411
133. Grenon M., Costelloe T., Jimeno S., O'Shaughnessy A., Fitzgerald J., Zgheib O., Degerth L., and Lowndes N.F. Docking onto chromatin via the Saccharomyces cerevisiae Rad9 Tudor domain. Yeast 24 (2007) 105-119
134. Bostelman L.J., Keller A.M., Albrecht A.M., Arat A., and Thompson J.S. Methylation of histone H3 lysine-79 by Dot1p plays multiple roles in the response to UV damage in Saccharomyces cerevisiae. DNA Repair (Amst) 6 (2007) 383-395
135. Conde F., and San-Segundo P.A. Role of Dot1 in the response to alkylating DNA damage in Saccharomyces cerevisiae: regulation of DNA damage tolerance by the error-prone polymerases Polzeta/Rev1. Genetics 179 (2008) 1197-1210
136. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
137. Bao Y., and Shen X. INO80 subfamily of chromatin remodeling complexes. Mutat. Res. 618 (2007) 18-29
138. Morrison A.J., Highland J., Krogan N.J., Arbel-Eden A., Greenblatt J.F., Haber J.E., and Shen X. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119 (2004) 767-775
139. van Attikum H., Fritsch O., and Gasser S.M. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26 (2007) 4113-4125
140. Shen X., Mizuguchi G., Hamiche A., and Wu C. A chromatin remodelling complex involved in transcription and DNA processing. Nature 406 (2000) 541-544
141. van Attikum H., Fritsch O., Hohn B., and Gasser S.M. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119 (2004) 777-788
142. Shimada K., Oma Y., Schleker T., Kugou K., Ohta K., Harata M., and Gasser S.M. Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr. Biol. 18 (2008) 566-575
143. Morrison A.J., Kim J.A., Person M.D., Highland J., Xiao J., Wehr T.S., Hensley S., Bao Y., Shen J., Collins S.R., Weissman J.S., Delrow J., Krogan N.J., Haber J.E., and Shen X. Mec1/Tel1 phosphorylation of the INO80 chromatin remodeling complex influences DNA damage checkpoint responses. Cell 130 (2007) 499-511
144. Ogiwara H., Enomoto T., and Seki M. The INO80 chromatin remodeling complex functions in sister chromatid cohesion. Cell Cycle 6 (2007) 1090-1095
145. Pan X., Ye P., Yuan D.S., Wang X., Bader J.S., and Boeke J.D. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124 (2006) 1069-1081
146. Dhillon N., Oki M., Szyjka S.J., Aparicio O.M., and Kamakaka R.T. H2A.Z functions to regulate progression through the cell cycle. Mol. Cell. Biol. 26 (2006) 489-501
147. Zhang H., Roberts D.N., and Cairns B.R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123 (2005) 219-231