Ubiquitin family modifications and template switching

FEBS Letters

Volumn 585, Issue 18, 2011, Pages 2810-2817

  Branzei, Dana ^a  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Homologous recombination; Post replication repair; Replication fork; Strand annealing; Template switching

Indexed keywords

CYCLINE; DDR KINASE; DOUBLE STRANDED DNA; PHOSPHOTRANSFERASE; RAD18 PROTEIN; SINGLE STRANDED DNA; SUMO PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

DNA DAMAGE; DNA METABOLISM; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; DNA SYNTHESIS; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; GENE SWITCHING; GENETIC REGULATION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN FAMILY; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; SUMOYLATION; UBIQUITINATION;

ANIMALS; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMANS; MODELS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINATION, GENETIC; UBIQUITIN;

EID: 80052768689     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.04.053     Document Type: Review

References (136)

1. S.P. Jackson, and J. Bartek The DNA-damage response in human biology and disease Nature 461 2009 1071 1078
2. P.J. Hastings, G. Ira, and J.R. Lupski A microhomology-mediated break-induced replication model for the origin of human copy number variation PLoS Genet. 5 2009 e1000327
3. J. San Filippo, P. Sung, and H. Klein Mechanism of eukaryotic homologous recombination Annu. Rev. Biochem. 77 2008 229 257
4. M.R. Lieber The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway Annu. Rev. Biochem. 79 2010 181 211
5. H. Zhang, and C.W. Lawrence The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination Proc. Natl. Acad. Sci. USA 102 2005 15954 15959 (Pubitemid 41552849)
6. R.E. Johnson, S.T. Henderson, T.D. Petes, S. Prakash, M. Bankmann, and L. Prakash Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome Mol. Cell. Biol. 12 1992 3807 3818
7. S.T. Henderson, and T.D. Petes Instability of simple sequence DNA in Saccharomyces cerevisiae Mol. Cell. Biol. 12 1992 2749 2757
8. Y. Bai, and L.S. Symington A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae Genes Dev. 10 1996 2025 2037 (Pubitemid 26346111)
9. J. Smith, and R. Rothstein A mutation in the gene encoding the Saccharomyces cerevisiae single-stranded DNA-binding protein Rfa1 stimulates a RAD52-independent pathway for direct-repeat recombination Mol. Cell. Biol. 15 1995 1632 1641
10. A.J. Rattray, and L.S. Symington Use of a chromosomal inverted repeat to demonstrate that the RAD51 and RAD52 genes of Saccharomyces cerevisiae have different roles in mitotic recombination Genetics 138 1994 587 595 (Pubitemid 24337787)
11. N.P. Higgins, K. Kato, and B. Strauss A model for replication repair in mammalian cells J. Mol. Biol. 101 1976 417 425
12. H.D. Ulrich, and H. Walden Ubiquitin signalling in DNA replication and repair Nat. Rev. Mol. Cell Biol. 11 2010 479 489
13. S.E. Polo, and S.P. Jackson Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications Genes Dev. 25 2011 409 433
14. T.T. Huang, and A.D. D'Andrea Regulation of DNA repair by ubiquitylation Nat. Rev. Mol. Cell Biol. 7 2006 323 334
15. D. Branzei, and M. Foiani Maintaining genome stability at the replication fork Nat. Rev. Mol. Cell Biol. 11 2010 208 219
16. M.E. Moynahan, and M. Jasin Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis Nat. Rev. Mol. Cell Biol. 11 2010 196 207
17. W.D. Heyer, K.T. Ehmsen, and J. Liu Regulation of homologous recombination in eukaryotes Annu. Rev. Genet. 44 2010 113 139
18. L.S. Symington Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair Microbiol. Mol. Biol. Rev. 66 2002 630 670 (table of contents) (Pubitemid 35425112)
19. L.E. Kang, and L.S. Symington Aberrant double-strand break repair in rad51 mutants of Saccharomyces cerevisiae Mol. Cell. Biol. 20 2000 9162 9172 (Pubitemid 32246105)
20. E.L. Ivanov, N. Sugawara, J. Fishman-Lobell, and J.E. Haber Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae Genetics 142 1996 693 704
21. A.P. Davis, and L.S. Symington The yeast recombinational repair protein Rad59 interacts with Rad52 and stimulates single-strand annealing Genetics 159 2001 515 525 (Pubitemid 33035096)
22. N.R. Pannunzio, G.M. Manthey, and A.M. Bailis RAD59 is required for efficient repair of simultaneous double-strand breaks resulting in translocations in Saccharomyces cerevisiae DNA Repair (Amst.) 7 2008 788 800
23. N. Sugawara, G. Ira, and J.E. Haber DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair Mol. Cell. Biol. 20 2000 5300 5309 (Pubitemid 30431583)
24. W. Xiao, B.L. Chow, S. Broomfield, and M. Hanna The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways Genetics 155 2000 1633 1641 (Pubitemid 30626384)
25. A. Slack, P.C. Thornton, D.B. Magner, S.M. Rosenberg, and P.J. Hastings On the mechanism of gene amplification induced under stress in Escherichia coli PLoS Genet. 2 2006 e48
26. J.A. Lee, C.M. Carvalho, and J.R. Lupski A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders Cell 131 2007 1235 1247 (Pubitemid 350297419)
27. D. Branzei, and M. Foiani Template switching: from replication fork repair to genome rearrangements Cell 131 2007 1228 1230 (Pubitemid 350297427)
28. C. Payen, R. Koszul, B. Dujon, and G. Fischer Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms PLoS Genet. 4 2008 e1000175
29. C.M. Carvalho Complex rearrangements in patients with duplications of MECP2 can occur by fork stalling and template switching Hum. Mol. Genet. 18 2009 2188 2203
30. F. Zhang, M. Khajavi, A.M. Connolly, C.F. Towne, S.D. Batish, and J.R. Lupski The DNA replication FoSTeS/MMBIR mechanism can generate genomic, genic and exonic complex rearrangements in humans Nat. Genet. 41 2009 849 853
31. C.E. Smith, B. Llorente, and L.S. Symington Template switching during break-induced replication Nature 447 2007 102 105 (Pubitemid 46685835)
32. B. Llorente, C.E. Smith, and L.S. Symington Break-induced replication: what is it and what is it for? Cell Cycle 7 2008 859 864 (Pubitemid 351573777)
33. C. Mott, and L.S. Symington RAD51-independent inverted-repeat recombination by a strand-annealing mechanism DNA Repair (Amst.) 10 2011 408 415
34. K. Mizuno, S. Lambert, G. Baldacci, J.M. Murray, and A.M. Carr Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism Genes Dev. 23 2009 2876 2886
35. A.L. Paek, S. Kaochar, H. Jones, A. Elezaby, L. Shanks, and T. Weinert Fusion of nearby inverted repeats by a replication-based mechanism leads to formation of dicentric and acentric chromosomes that cause genome instability in budding yeast Genes Dev. 23 2009 2861 2875
36. P.J. Hastings, J.R. Lupski, S.M. Rosenberg, and G. Ira Mechanisms of change in gene copy number Nat. Rev. Genet. 10 2009 551 564
37. D. Branzei, and M. Foiani Leaping forks at inverted repeats Genes Dev. 24 2010 5 9
38. V. Gangavarapu, L. Haracska, I. Unk, R.E. Johnson, S. Prakash, and L. Prakash Mms2-Ubc13-dependent and -independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae Mol. Cell. Biol. 26 2006 7783 7790 (Pubitemid 44547723)
39. V. Gangavarapu, S. Prakash, and L. Prakash Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae Mol. Cell. Biol. 27 2007 7758 7764 (Pubitemid 350033679)
40. G.I. Karras, and S. Jentsch The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase Cell 141 2010 255 267
41. E.C. Minca, and D. Kowalski Multiple Rad5 activities mediate sister chromatid recombination to bypass DNA damage at stalled replication forks Mol. Cell 38 2010 649 661
42. D. Branzei, F. Vanoli, and M. Foiani SUMOylation regulates Rad18-mediated template switch Nature 456 2008 915 920
43. T. Kogoma Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription Microbiol. Mol. Biol. Rev. 61 1997 212 238 (Pubitemid 27283801)
44. L.G. Ball, K. Zhang, J.A. Cobb, C. Boone, and W. Xiao The yeast Shu complex couples error-free post-replication repair to homologous recombination Mol. Microbiol. 73 2009 89 102
45. C. Lawrence The RAD6 DNA repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it? BioEssays 16 1994 253 258 (Pubitemid 2073507)
46. L. Prakash Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations Mol. Gen. Genet. 184 1981 471 478 (Pubitemid 12129873)
47. D. Branzei, M. Seki, and T. Enomoto Rad18/Rad5/Mms2-mediated polyubiquitination of PCNA is implicated in replication completion during replication stress Genes Cells 9 2004 1031 1042 (Pubitemid 39467976)
48. D. Szuts, L.J. Simpson, S. Kabani, M. Yamazoe, and J.E. Sale Role for RAD18 in homologous recombination in DT40 cells Mol. Cell. Biol. 26 2006 8032 8041 (Pubitemid 44631002)
49. J. Huang, M.S. Huen, H. Kim, C.C. Leung, J.N. Glover, X. Yu, and J. Chen RAD18 transmits DNA damage signalling to elicit homologous recombination repair Nat. Cell Biol. 11 2009 592 603
50. A. Saberi RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination-mediated repair Mol. Cell. Biol. 27 2007 2562 2571 (Pubitemid 46581347)
51. S. Moertl, G.I. Karras, T. Wismuller, F. Ahne, and F. Eckardt-Schupp Regulation of double-stranded DNA gap repair by the RAD6 pathway DNA Repair (Amst.) 7 2008 1893 1906
52. F. Ahne, B. Jha, and F. Eckardt-Schupp The RAD5 gene product is involved in the avoidance of non-homologous end-joining of DNA double strand breaks in the yeast Saccharomyces cerevisiae Nucleic Acids Res. 25 1997 743 749 (Pubitemid 27299827)
53. B. Jha, F. Ahne, and F. Eckardt-Schupp The use of a double-marker shuttle vector to study DNA double-strand break repair in wild-type and radiation-sensitive mutants of the yeast Saccharomyces cerevisiae Curr. Genet. 23 1993 402 407 (Pubitemid 23197019)
54. S. Chen, A.A. Davies, D. Sagan, and H.D. Ulrich The RING finger ATPase Rad5p of Saccharomyces cerevisiae contributes to DNA double-strand break repair in a ubiquitin-independent manner Nucleic Acids Res. 33 2005 5878 5886 (Pubitemid 41742607)
55. M. Cordeiro-Stone, A.M. Makhov, L.S. Zaritskaya, and J.D. Griffith Analysis of DNA replication forks encountering a pyrimidine dimer in the template to the leading strand J. Mol. Biol. 289 1999 1207 1218 (Pubitemid 29296700)
56. V. Pages, and R.P. Fuchs Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo Science 300 2003 1300 1303 (Pubitemid 36618243)
57. D. Branzei, and M. Foiani The DNA damage response during DNA replication Curr. Opin. Cell Biol. 17 2005 568 575 (Pubitemid 41541967)
58. S. Prakash, R.E. Johnson, and L. Prakash Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function Annu. Rev. Biochem. 74 2005 317 353 (Pubitemid 40995510)
59. S.S. Lange, K. Takata, and R.D. Wood DNA polymerases and cancer Nat. Rev. Cancer 11 2011 96 110
60. Y. Daigaku, A.A. Davies, and H.D. Ulrich Ubiquitin-dependent DNA damage bypass is separable from genome replication Nature 465 2010 951 955
61. R.C. Heller, and K.J. Marians Replication fork reactivation downstream of a blocked nascent leading strand Nature 439 2006 557 562 (Pubitemid 43185374)
62. S. Lambert Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange Mol. Cell 39 2010 346 359
63. M. Clemente-Ruiz, and F. Prado Chromatin assembly controls replication fork stability EMBO Rep. 10 2009 790 796
64. G. Liberi 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 (Pubitemid 40189297)
65. G. Lettier, Q. Feng, A.A. de Mayolo, N. Erdeniz, R.J. Reid, M. Lisby, U.H. Mortensen, and R. Rothstein The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae PLoS Genet. 2 2006 e194
66. M. Nakahara Genetic evidence for single-strand lesions initiating Nbs1-dependent homologous recombination in diversification of Ig V in chicken B lymphocytes PLoS Genet. 5 2009 e1000356
67. F. Vanoli, M. Fumasoni, B. Szakal, L. Maloisel, and D. Branzei Replication and recombination factors contributing to recombination-dependent bypass of DNA lesions by template switch PLoS Genet. 6 2010 e1001205
68. S. Tateishi, Y. Sakuraba, S. Masuyama, H. Inoue, and M. Yamaizumi Dysfunction of human Rad18 results in defective postreplication repair and hypersensitivity to multiple mutagens Proc. Natl. Acad. Sci. USA 97 2000 7927 7932 (Pubitemid 30460750)
69. W. Xiao, S.L. Lin, S. Broomfield, B.L. Chow, and Y.F. Wei The products of the yeast MMS2 and two human homologs (hMMS2 and CROC-1) define a structurally and functionally conserved Ubc-like protein family Nucleic Acids Res. 26 1998 3908 3914 (Pubitemid 28401339)
70. G.Y. Zhao A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination Mol. Cell 25 2007 663 675 (Pubitemid 46341920)
71. C.A. Torres-Ramos, S. Prakash, and L. Prakash Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae Mol. Cell. Biol. 22 2002 2419 2426 (Pubitemid 34224644)
72. I. Unk Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen Proc. Natl. Acad. Sci. USA 103 2006 18107 18112 (Pubitemid 44871620)
73. A. Motegi, R. Sood, H. Moinova, S.D. Markowitz, P.P. Liu, and K. Myung Human SHPRH suppresses genomic instability through proliferating cell nuclear antigen polyubiquitination J. Cell Biol. 175 2006 703 708 (Pubitemid 44878502)
74. E.C. Friedberg Suffering in silence: the tolerance of DNA damage Nat. Rev. Mol. Cell Biol. 6 2005 943 953 (Pubitemid 41778713)
75. C. Hoege, B. Pfander, G.L. Moldovan, G. Pyrowolakis, and S. Jentsch RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO Nature 419 2002 135 141 (Pubitemid 35025438)
76. R.E. Johnson, S. Prakash, and L. Prakash Yeast DNA repair protein RAD5 that promotes instability of simple repetitive sequences is a DNA-dependent ATPase J. Biol. Chem. 269 1994 28259 28262 (Pubitemid 24354565)
77. A. Blastyak, L. Pinter, I. Unk, L. Prakash, S. Prakash, and L. Haracska Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression Mol. Cell 28 2007 167 175 (Pubitemid 47542303)
78. T. Weinert, S. Kaochar, H. Jones, A. Paek, and A.J. Clark The replication fork's five degrees of freedom, their failure and genome rearrangements Curr. Opin. Cell Biol. 21 2009 778 784
79. S.J. Goldfless, A.S. Morag, K.A. Belisle, V.A. Sutera Jr.; and S.T. Lovett DNA repeat rearrangements mediated by DnaK-dependent replication fork repair Mol. Cell 21 2006 595 604 (Pubitemid 43290727)
80. A. Chavez, V. Agrawal, and F.B. Johnson Homologous recombination- dependent rescue of deficiency in the structural maintenance of chromosomes (Smc) 5/6 complex J. Biol. Chem. 286 2011 5119 5125
81. H.W. Mankouri, T.M. Ashton, and I.D. Hickson Holliday junction-containing DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage Proc. Natl. Acad. Sci. USA 108 2011 4944 4949
82. E.C. Minca, and D. Kowalski Replication fork stalling by bulky DNA damage: localization at active origins and checkpoint modulation Nucleic Acids Res. 39 2011 2610 2623
83. S. Jentsch, J.P. McGrath, and A. Varshavsky The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme Nature 329 1987 131 134 (Pubitemid 17125247)
84. R.M. Hofmann, and C.M. Pickart Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair Cell 96 1999 645 653 (Pubitemid 29122807)
85. H.D. Ulrich, and S. Jentsch Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair EMBO J. 19 2000 3388 3397 (Pubitemid 30428216)
86. P. Stelter, and H.D. Ulrich Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation Nature 425 2003 188 191 (Pubitemid 37150898)
87. P.L. Kannouche, J. Wing, and A.R. Lehmann Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage Mol. Cell 14 2004 491 500 (Pubitemid 38648802)
88. L. Haracska, C.A. Torres-Ramos, R.E. Johnson, S. Prakash, and L. Prakash Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae Mol. Cell. Biol. 24 2004 4267 4274 (Pubitemid 41070998)
89. K. Choi, B. Szakal, Y.H. Chen, D. Branzei, and X. Zhao The Smc5/6 complex and Esc2 influence multiple replication-associated recombination processes in Saccharomyces cerevisiae Mol. Biol. Cell 21 2010 2306 2314
90. N. Cherng Expansions, contractions, and fragility of the spinocerebellar ataxia type 10 pentanucleotide repeat in yeast Proc. Natl. Acad. Sci. USA 108 2011 2843 2848
91. A.A. Shishkin Large-scale expansions of Friedreich's ataxia GAA repeats in yeast Mol. Cell 35 2009 82 92
92. D.L. Daee, T. Mertz, and R.S. Lahue Postreplication repair inhibits CAG.CTG repeat expansions in Saccharomyces cerevisiae Mol. Cell. Biol. 27 2007 102 110 (Pubitemid 46013236)
93. R.L. Erlich, R.C. Fry, T.J. Begley, D.L. Daee, R.S. Lahue, and L.D. Samson Anc1, a protein associated with multiple transcription complexes, is involved in postreplication repair pathway in S. cerevisiae PLoS One 3 2008 e3717
94. J.R. Lydeard, Z. Lipkin-Moore, Y.J. Sheu, B. Stillman, P.M. Burgers, and J.E. Haber Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly Genes Dev. 24 2010 1133 1144
95. B. Pfander, G.L. Moldovan, M. Sacher, C. Hoege, and S. Jentsch SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase Nature 436 2005 428 433 (Pubitemid 41059056)
96. E. Papouli, S. Chen, A.A. Davies, D. Huttner, L. Krejci, P. Sung, and H.D. Ulrich Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p Mol. Cell 19 2005 123 133 (Pubitemid 40884663)
97. O. Parnas, A. Zipin-Roitman, B. Pfander, B. Liefshitz, Y. Mazor, S. Ben-Aroya, S. Jentsch, and M. Kupiec Elg1, an alternative subunit of the RFC clamp loader, preferentially interacts with SUMOylated PCNA EMBO J. 29 2010 2611 2622
98. K.B. Falbo Involvement of a chromatin remodeling complex in damage tolerance during DNA replication Nat. Struct. Mol. Biol. 16 2009 1167 1172
99. T. Inagawa, T. Yamada-Inagawa, T. Eydmann, I.S. Mian, T.S. Wang, and J.Z. Dalgaard Schizosaccharomyces pombe Rtf2 mediates site-specific replication termination by inhibiting replication restart Proc. Natl. Acad. Sci. USA 106 2009 7927 7932
100. J.Z. Dalgaard, and A.J. Klar A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mat1 in S. pombe Genes Dev. 15 2001 2060 2068 (Pubitemid 32762050)
101. J.C. Game, and S.B. Chernikova The role of RAD6 in recombinational repair, checkpoints and meiosis via histone modification DNA Repair (Amst.) 8 2009 470 482
102. J.C. Game, M.S. Williamson, T. Spicakova, and J.M. Brown The RAD6/BRE1 histone modification pathway in Saccharomyces confers radiation resistance through a RAD51-dependent process that is independent of RAD18 Genetics 173 2006 1951 1968 (Pubitemid 44285675)
103. K. Robzyk, J. Recht, and M.A. Osley Rad6-dependent ubiquitination of histone H2B in yeast Science 287 2000 501 504
104. W.W. Hwang, S. Venkatasubrahmanyam, A.G. Ianculescu, A. Tong, C. Boone, and H.D. Madhani A conserved RING finger protein required for histone H2B monoubiquitination and cell size control Mol. Cell 11 2003 261 266 (Pubitemid 36126606)
105. A. Wood Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter Mol. Cell 11 2003 267 274 (Pubitemid 36126607)
106. M.D. Shahbazian, K. Zhang, and M. Grunstein Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1 Mol. Cell 19 2005 271 277 (Pubitemid 41019673)
107. H.W. Mankouri, H.P. Ngo, and I.D. Hickson Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3 Mol. Biol. Cell 18 2007 4062 4073 (Pubitemid 47519496)
108. C.D. Putnam, T.K. Hayes, and R.D. Kolodner Post-replication repair suppresses duplication-mediated genome instability PLoS Genet. 6 2010 e1000933
109. A.A. Davies, D. Huttner, Y. Daigaku, S. Chen, and H.D. Ulrich Activation of ubiquitin-dependent DNA damage bypass is mediated by replication protein a Mol. Cell 29 2008 625 636 (Pubitemid 351374681)
110. A. Motegi, K. Kuntz, A. Majeed, S. Smith, and K. Myung Regulation of gross chromosomal rearrangements by ubiquitin and SUMO ligases in Saccharomyces cerevisiae Mol. Cell. Biol. 26 2006 1424 1433 (Pubitemid 43202567)
111. J.R. Lydeard, S. Jain, M. Yamaguchi, and J.E. Haber Break-induced replication and telomerase-independent telomere maintenance require Pol32 Nature 448 2007 820 823 (Pubitemid 47266343)
112. D. Branzei, M. Seki, F. Onoda, and T. Enomoto The product of Saccharomyces cerevisiae WHIP/MGS1, a gene related to replication factor C genes, interacts functionally with DNA polymerase delta Mol. Gen. Genom. 268 2002 371 386 (Pubitemid 35352136)
113. T. Hishida, T. Ohno, H. Iwasaki, and H. Shinagawa Saccharomyces cerevisiae MGS1 is essential in strains deficient in the RAD6-dependent DNA damage tolerance pathway EMBO J. 21 2002 2019 2029 (Pubitemid 34437199)
114. L. Giot, R. Chanet, M. Simon, C. Facca, and G. Faye Involvement of the yeast DNA polymerase delta in DNA repair in vivo Genetics 146 1997 1239 1251 (Pubitemid 27337672)
115. C.E. Smith, A.F. Lam, and L.S. Symington Aberrant double-strand break repair resulting in half crossovers in mutants defective for Rad51 or the DNA polymerase delta complex Mol. Cell. Biol. 29 2009 1432 1441
116. H.W. Mankouri, and I.D. Hickson Top3 processes recombination intermediates and modulates checkpoint activity after DNA damage Mol. Biol. Cell 17 2006 4473 4483 (Pubitemid 44522064)
117. J.R. Mullen, V. Kaliraman, S.S. Ibrahim, and S.J. Brill Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae Genetics 157 2001 103 118
118. F. Onoda, M. Seki, A. Miyajima, and T. Enomoto Involvement of SGS1 in DNA damage-induced heteroallelic recombination that requires RAD52 in Saccharomyces cerevisiae Mol. Gen. Genet. 264 2001 702 708
119. D. Branzei Ubc9- and Mms21-mediated Sumoylation counteracts recombinogenic events at damaged replication forks Cell 127 2006 509 522 (Pubitemid 44647424)
120. M.T. Lee, A.A. Bakir, K.N. Nguyen, and J. Bachant The SUMO isopeptidase Ulp2p is required to prevent recombination-induced chromosome segregation lethality following DNA replication stress PLoS Genet. 7 2011 e1001355
121. J. Sollier, R. Driscoll, F. Castellucci, M. Foiani, S.P. Jackson, and D. Branzei The Saccharomyces cerevisiae Esc2 and Smc5-6 proteins promote sister chromatid junction-mediated intra-S repair Mol. Biol. Cell 20 2009 1671 1682
122. H.W. Mankouri, H.P. Ngo, and I.D. Hickson Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae Mol. Biol. Cell 20 2009 1683 1694
123. T.M. Ashton, H.W. Mankouri, A. Heidenblut, P.J. McHugh, and I.D. Hickson Pathways for Holliday Junction processing during homologous recombination in Saccharomyces cerevisiae Mol. Cell. Biol. 31 2011 1921 1933
124. S. Eladad, T.Z. Ye, P. Hu, M. Leversha, S. Beresten, M.J. Matunis, and N.A. Ellis Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification Hum. Mol. Genet. 14 2005 1351 1365 (Pubitemid 40744493)
125. C.Y. Lu, C.H. Tsai, S.J. Brill, and S.C. Teng Sumoylation of the BLM ortholog, Sgs1, promotes telomere-telomere recombination in budding yeast Nucleic Acids Res. 38 2010 488 498
126. D. Branzei, and M. Foiani Regulation of DNA repair throughout the cell cycle Nat. Rev. Mol. Cell Biol. 9 2008 297 308 (Pubitemid 351430844)
127. K. Herzberg Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks Mol. Cell. Biol. 26 2006 8396 8409 (Pubitemid 44748573)
128. S. Kaochar, L. Shanks, and T. Weinert Checkpoint genes and Exo1 regulate nearby inverted repeat fusions that form dicentric chromosomes in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 107 2010 21605 21610
129. I. Morin, H.P. Ngo, A. Greenall, M.K. Zubko, N. Morrice, and D. Lydall Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response EMBO J. 27 2008 2400 2410
130. M. Segurado, and J.F. Diffley Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks Genes Dev. 22 2008 1816 1827 (Pubitemid 351915506)
131. M. Kai, K. Furuya, F. Paderi, A.M. Carr, and T.S. Wang Rad3-dependent phosphorylation of the checkpoint clamp regulates repair-pathway choice Nat. Cell Biol. 9 2007 691 697 (Pubitemid 47214732)
132. S. Matsuoka ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 316 2007 1160 1166 (Pubitemid 46877472)
133. A. Nikiforov, M. Svetlova, L. Solovjeva, L. Sasina, J. Siino, I. Nazarov, M. Bradbury, and N. Tomilin DNA damage-induced accumulation of Rad18 protein at stalled replication forks in mammalian cells involves upstream protein phosphorylation Biochem. Biophys. Res. Commun. 323 2004 831 837 (Pubitemid 39243394)
134. T.A. Day Phosphorylated Rad 18 directs DNA Polymerase eta to sites of stalled replication J. Cell Biol. 191 2010 953 966
135. H. Dou, C. Huang, M. Singh, P.B. Carpenter, and E.T. Yeh Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex Mol. Cell 39 2010 333 345
136. W. Gu, F. Zhang, and J.R. Lupski Mechanisms for human genomic rearrangements Pathogenetics 1 2008 4