DNA damage responses and their many interactions with the replication fork

Carcinogenesis

Volumn 27, Issue 5, 2006, Pages 883-892

  Andreassen, Paul R ^a,b   Ho, Gary P H ^c   D'Andrea, Alan D ^c  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; DNA;

ATAXIA TELANGIECTASIA; BLOOM SYNDROME; CANCER; CANCER SUSCEPTIBILITY; CELL CYCLE S PHASE; CELL DIVISION; CHROMOSOMAL INSTABILITY; DNA DAMAGE; DNA REPAIR; DNA SYNTHESIS; FANCONI ANEMIA; GENE DUPLICATION; GENE REPLICATION; GENOME; HOMOLOGOUS RECOMBINATION; HUMAN; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SISTER CHROMATID;

ANIMALS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMANS; MODELS, BIOLOGICAL; MODELS, GENETIC; RECOMBINATION, GENETIC; S PHASE; SISTER CHROMATID EXCHANGE;

EID: 33646183367     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgi319     Document Type: Review

References (139)

1. Kastan,M.B. and Bartek,J. (2004) Cell-cycle checkpoints and cancer. Nature, 432, 316-323.
2. Bartek,J., Lukas,C. and Lukas,J. (2004) Checking on DNA damage in S phase. Nat. Rev. Mol. Cell Biol., 5, 792-804.
3. Hartwell,L.H. and Weinert,T.A. (1989) Checkpoints: Controls that ensure the order of cell cycle events. Science, 246, 629-634.
4. Barbour,L. and Xiao,W. (2003) Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: A yeast model. Murat. Res., 532, 137-155.
5. Thompson,L.H. and Schild,D. (2002) Recombinational DNA repair and human disease. Mutat. Res., 509, 49-78.
6. Orren,D.K., Petersen,L.N. and Bohr,V.A. (1995) A UV-responsive G2 checkpoint in rodent cells. Mol. Cell. Biol., 15, 3722-3730.
7. Sorenson,C.M. and Eastman,A. (1988) Influence of cis-diamminedichloroplatinum(II) on DNA synthesis and cell cycle progression in excision repair proficient and deficient Chinese hamster ovary cells. Cancer Res., 48, 6703-6707.
8. Kruyt,F.A., Dijkmans,L.M., Arwert,F. and Joenje,H. (1997) Involvement of the Fanconi's anemia protein FAC in a pathway that signals to the cyclin B/cdc2 kinase. Cancer Res., 57, 2244-2251.
9. He,Z., Henricksen,L.A., Wold,M.S. and Ingles,C.J. (1995) RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature, 374, 566-569.
10. 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. (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell, 80, 859-868.
11. Shivji,K.K., Kenny,M.K. and Wood,R.D. (1992) Proliferating cell nuclear antigen is required for DNA excision repair. Cell, 69, 367-374.
12. Prelich,G., Tan,C.K., Kostura,M., Mathews,M.B., So,A.G., Downey,K.M. and Stillman,B. (1987) Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature, 326, 517-520.
13. Bravo,R., Frank,R., Blundell,P.A. and Macdonald-Bravo,H. (1987) Cyclin/ PCNA is the auxiliary protein of DNA polymerase-delta. Nature, 326, 515-517
14. Longhese,M.P., Plevani,P. and Lucchini,G. (1994) Replication factor A is required in vivo for DNA replication, repair, and recombination. Mol. Cell. Biol., 14, 7884-7890.
15. Costanzo,V., Shechter,D., Lupardus,P.J., Cimprich,K.A., Gottesman,M. and Gautier,J. (2003) An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell, 11, 203-213.
16. Shechter,D., Costanzo,V. and Gautier,J. (2004) ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol., 6, 648-655.
17. Cortez,D., Glick,G. and Elledge,S.J. (2004) Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc. Natl Acad. Sci. USA, 101, 10078-10083.
18. Yoo,H.Y., Shevchenko,A., Shevchenko,A. and Dunphy,W.G. (2004) Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J. Biol. Chem., 279, 53353-53364.
19. Segurado,M., Gomez,M. and Antequera,F. (2002) Increased recombination intermediates and homologous integration hot spots at DNA replication origins. Mol. Cell, 10, 907-916.
20. Rothkamm,K., Kruger,I., Thompson,L.H. and Lobrich,M. (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol., 23, 5706-5715.
21. Akkari,Y.M., Bateman,R.L., Reifsteck,C.A., Olson,S.B, and Grompe,M. (2000) DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol. Cell. Biol., 20, 8283-8289.
22. Heffernan,T.P., Simpson,D.A., Frank,A.R., Heinloth,A.N., Paules,R.S., Cordeiro-Stone,M. and Kaufmann,W.K. (2002) An ATR- and Chk1- dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol. Cell. Biol., 22, 8552-8561.
23. Weiss,R.S., Leder,P. and Vaziri,C. (2003) Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Mol. Cell. Biol., 23, 791-803.
24. Falck,J., Mailand,N., Syljuasen,R.G., Bartek,J. and Lukas,J. (2001) The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature, 410, 842-847.
25. Falck,J., Petrini,J.H., Williams,B.R., Lukas,J. and Bartek,J. (2002) The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet., 30, 290-294.
26. Guo,Z., Kumagai,A., Wang,S.X. and Dunphy,W.G. (2000) Requirement for ATR in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev., 14, 2745-2756.
27. Liu,Q., Guntuku,S., Cui,X.S. et al. (2000) Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage check point. Genes Dev., 14, 1448-1459.
28. Sengupta,S., Robles,A.I., Linke,S.P. et al. (2004) Functional interaction between BLM helicase and 53BP1 in a Chk1-mediated pathway during S-phase arrest. J. Cell Biol., 166, 801-13.
29. Osborn,A.J., Elledge,S.J. and Zou,L. (2002) Checking on the fork: The DNA-replication stress-response pathway. Trends Cell Biol., 12, 509-516.
30. Tibbetts,R.S., Cortez,D., Brumbaugh,K.M., Scully,R., Livingston,D., Elledge,S.J. and Abraham,R.T. (2000) Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev., 14, 2989-3002.
31. Oakley,T.J. and Hickson,I.D. (2002) Defending genome integrity during S-phase: Putative roles for RecQ helicases and topoisomerase III. DNA Repair (Amst.), 1, 175-207.
32. Cox,M.M., Goodman,M.F., Kreuzer,K.N., Sherratt,D.J., Sandler,S.J. and Marians,K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41.
33. Helleday,T. (2003) Pathways for mitotic homologous recombination in mammalian cells. Mutat. Res., 532, 103-115.
34. Hochegger,H., Sonoda,E. and Takeda,S. (2004) Post-replication repair in DT40 cells: Translesion polymerases versus recombinases. Bioessays, 26, 151-158.
35. Kunkel,T.A., Pavlov,Y.I. and Bebenek,K. (2003) Functions of human DNA polymerases eta, kappa and iota suggested by their properties, including fidelity with undamaged DNA templates. DNA Repair (Amst.), 2, 135-149.
36. Sjogren,C. and Nasmyth,K. (2001) Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol., 11, 991-995.
37. Duker,N.J. (2002) Chromosome breakage syndromes and cancer. Am. J. Med Genet., 115, 125-129.
38. Nurse,P. (1994) Ordering S phase and M phase in the cell cycle. Cell, 79, 547-550.
39. Painter,R.B. and Young,B.R. (1980) Radiosensitivity in ataxia-telangiectasia: A new explanation. Proc. Natl Acad. Sci. USA, 77, 7315-7317.
40. Kaufmann,W.K. and Cleaver,J.E. (1981) Mechanisms of inhibition of DNA replication by ultraviolet light in normal human and xeroderma pigmentosum fibroblasts. J. Mol. Biol., 149, 171-187.
41. Tercero,J.A. and Diffley,J.F. (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature, 412, 553-557.
42. Takisawa,H., Mimura,S. and Kubota,Y. (2000) Eukaryotic DNA replication: from pre-replication complex to initiation complex. Curr. Opin. Cell Biol., 12, 690-696.
43. Walter,J.C. (2000) Evidence for sequential action of cdc7 and cdk2 protein kinases during initiation of DNA replication in Xenopus egg extracts. J. Biol. Chem, 275, 39773-39778.
44. Walter,J. and Newport,J. (2000) Initiation of eukaryotic DNA replication: Origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase alpha. Mol. Cell, 5, 617-627.
45. Savitsky,K., Bar-Shira,A., Gilad,S. et al. (1995) A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science, 268, 1749-1753.
46. Sorensen,C.S., Syljuasen,R.G., Falck,J., Schroeder,T., Ronnstrand,L., Khanna,K.K., Zhou,B.B., Bartek,J. and Lukas,J. (2003) Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell, 3, 247-258.
47. Mailand,N., Falck,J., Lukas,C., Syljuasen,R.G., Welcker,M., Bartek,J. and Lukas,J. (2000) Rapid destruction of human Cdc25A in response to DNA damage. Science, 288, 1425-1429.
48. Painter,R.B. (1985) Inhibition and recovery of DNA synthesis in human cells after exposure to ultraviolet light. Mutat. Res., 145, 63-69.
49. Bao,S., Lu,T., Wang,X., Zheng,H., Wang,L.E., Wei,Q., Hittelman,W.N. and Li,L. (2004) Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects. Oncogene, 23, 5586-5593.
50. Lim,D.S., Kim,S.T., Xu,B., Maser,R.S., Lin,J., Petrini,J.H. and Kastan,M.B. (2000) ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature, 404, 613-617.
51. Zhao,S., Weng,Y.C., Yuan,S.S. et al. (2000) Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature, 405, 473-477.
52. Xu,B., O'Donnell,A.H., Kim,S.T. and Kastan,M.B. (2002) Phosphorylation of serine 1387 in Brca1 is specifically required for the Atm-mediated S-phase checkpoint after ionizing irradiation. Cancer Res., 62, 4588-4591.
53. Wang,X., Andreassen,P.R. and D'Andrea,A.D. (2004) Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell Biol., 24, 5850-5862.
54. Taniguchi,T., Garcia-Higuera,I., Xu,B., Andreassen,P.R., Gregory,R.C., Kim,S.T., Lane,W.S., Kastan,M.B. and D'Andrea,A.D. (2002) Convergence of the fanconi anemia and ataxia telangiectasia signaling pathways. Cell, 109, 459-472.
55. Kim,S.T., Xu,B. and Kastan,M.B. (2002) Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev., 16, 560-570.
56. Yazdi,P.T., Wang,Y., Zhao,S., Patel,N., Lee,E.Y. and Qin,J. (2002) SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev., 16, 571-582.
57. Zhong,H., Bryson,A., Eckersdorff,M. and Ferguson,D.O. (2005) Rad5O depletion impacts upon ATR-dependent DNA damage responses. Hum Mol. Genet., 14, 2685-2693.
58. Kitagawa,R., Bakkenist,C.J., McKinnon,P.J. and Kastan,M.B. (2004) Phosphorylation of SMC1 is a critical downstream event in the ATM-NBSI-BRCA1 pathway. Genes Dev., 18, 1423-1438.
59. Chahwan,C., Nakamura,T.M., Sivakumar,S., Russell,P. and Rhind,N. (2003) The fission yeast Rad32 (Mrell)-Rad5O-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell Biol., 23, 6564-6573.
60. Morrison,C., Sonoda,E., Takao,N., Shinohara,A., Yamamoto,K. and Takeda,S. (2000) The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J., 19, 463-471.
61. Tauchi,H., Kobayashi,J., Morishima,K. et al. (2002) Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature, 420, 93-98.
62. Moynahan,M.E., Chiu,J.W., Koller,B.H. and Jasin,M. (1999) Brca1 controls homology-directed DNA repair. Mol. Cell, 4, 511-518.
63. Johansson,F., Lagerqvist,A., Erixon,K. and Jenssen,D. (2004) A method to monitor replication fork progression in mammalian cells: Nucleotide excision repair enhances and homologous recombination delays elongation along damaged DNA. Nucleic Acids Res., 32, e157.
64. Nakanishi,K., Taniguchi,T., Ranganathan,V., New,H.V., Moreau,L.A., Stotsky,M., Mathew,C.G., Kastan,M.B., Weaver,D.T. and D'Andrea,A.D. (2002) Interaction of FANCD2 and NBS1 in the DNA damage response. Nat. Cell Biol., 4, 913-920.
65. Garcia-Higuera,I., Taniguchi,T., Ganesan,S., Meyn,M.S., Timmers,C,, Hejna,J., Grompe,M. and D'Andrea,A.D. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell, 7, 249-262.
66. Sonoda,E., Sasaki,M.S., Buerstedde,J.M., Bezzubova,O., Shinohara,A., Ogawa,H., Takata,M., Yamaguchi-Iwai,Y. and Takeda,S. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J., 17, 598-608.
67. Fabre,F., Chan,A., Heyer,W.D. and Gangloff,S. (2002) Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl Acad. Sci. USA, 99, 16887-16892.
68. Cha,R.S. and Kleckner,N. (2002) ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science, 297, 602-606.
69. Abraham,J., Lemmers,B., Hande,M.P. et al. (2003) Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J., 22, 6137-6147.
70. Casper,A.M., Nghiem,P., Arlt,M.F. and Glover,T.W. (2002) ATR regulates fragile site stability. Cell, 111, 779-789.
71. Cobb,J.A., Bjergbaek,L., Shimada,K., Frei,C. and Gasser,S.M. (2003) DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J., 22, 4325-4336.
72. Kai,M. and Wang,T.S. (2003) Checkpoint responses to replication stalling: Inducing tolerance and preventing mutagenesis. Mutat. Res., 532, 59-73.
73. Lopes,M., Cotta-Ramusino,C., Pellicioli,A., Liberi,G., Plevani,P., Muzi-Falconi,M., Newlon,C.S. and Foiani,M. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature, 412, 557-561.
74. +, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J., 16, 2682-2692.
75. Lomonosov,M., Anand,S., Sangrithi,M., Davies,R. and Venkitaraman,A.R. (2003) Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev., 17, 3017-3022.
76. Moynahan,M.E., Pierce,A,J. and Jasin,M. (2001) BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell, 7, 263-272.
77. Kaliraman,V., Mullen,J.R., Fricke,W.M., Bastin-Shanower,S.A. and Brill,S.J. (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev., 15, 2730-2740.
78. Davies,S.L., North,P.S., Dart,A., Lakin,N.D. and Hickson,I.D. (2004) Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell Biol., 24, 1279-1291.
79. - phenotype by expression of a bacterial Holliday junction resolvase. EMBO J., 19, 2751-2762.
80. Karow,J,K., Constantinou,A., Li,J.L., West,S.C. and Hickson,I.D. (2000) The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl Acad. Sci. USA, 97, 6504-6508.
81. Sogo,J.M., Lopes,M. and Foiani,M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science, 297, 599-602.
82. Boddy,M.N., Gaillard,P.H., McDonald,W.H., Shanahan,P., Yates,J.R.,III and Russell,P. (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell, 107, 537-548.
83. Boddy,M.N., Lopez-Girona,A., Shanahan,P., Interthal,H., Heyer,W.D. and Russell,P. (2000) Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell Biol., 20, 8758-8766.
84. Sengupta,S., Linke,S.P., Pedeux,R. et al. (2003) BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J., 22, 1210-1222.
85. Gangloff,S., Soustelle,C. and Fabre,F. (2000) Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet., 25, 192-194.
86. Saintigny,Y., Delacote,F., Vares,G., Petitot,F., Lambert,S., Averbeck,D. and Lopez,B.S. (2001) Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J., 20, 3861-3870.
87. Lundin,C., Erixon,K., Arnaudeau,C., Schultz,N., Jenssen,D., Meuth,M. and Helleday,T. (2002) Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell Biol., 22, 5869-5878.
88. Lundin,C., Schultz,N., Arnaudeau,C., Mohindra,A., Hansen,L.T. and Helleday,T. (2003) RAD51 is involved in repair of damage associated with DNA replication in mammalian cells. J. Mol. Biol., 328, 521-535.
89. Yang,Y.G., Cortes,U., Patnaik,S., Jasin,M. and Wang,Z.Q. (2004) Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene, 23, 3872-3882.
90. Zou,L. and Elledge,S.J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548.
91. Flores-Rozas,H. and Kolodner,R.D. (2000) Links between replication, recombination and genome instability in eukaryotes. Trends Biochem. Sci., 25, 196-200.
92. Gasior,S.L., Olivares,H., Ear,U., Hari,D.M., Weichselbaum,R. and Bishop,D.K. (2001) Assembly of RecA-like recombinases: Distinct roles for mediator proteins in mitosis and meiosis. Proc. Natl Acad. Sci. USA, 98, 8411-8418.
93. Eggler,A.L., Inman,R.B. and Cox,M.M. (2002) The Rad51-dependent pairing of long DNA substrates is stabilized by replication protein A. J. Biol. Chem, 277, 39280-39288.
94. Ward,I.M. and Chen,J. (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem, 276, 47759-47762.
95. Prakash,S., Johnson,R.E. and Prakash,L. (2005) Eukaryotic translesion synthesis DNA polymerases: Specificity of structure and function. Annu. Rev. Biochem., 74, 317-353.
96. Lehmann,A.R. (1972) Postreplication repair of DNA in ultraviolet-irradiated mammalian cells. J. Mol. Biol., 66, 319-337.
97. Yamashita,Y.M., Okada,T., Matsusaka,T., Sonoda,E., Zhao,G.Y., Araki,K., Tateishi,S., Yamaizumi,M. and Takeda,S. (2002) RAD18 and RAD54 cooperatively contribute to maintenance of genomic stability in vertebrate cells. EMBO J., 21, 5558-5566.
98. Sonoda,E., Okada,T., Zhao,G.Y. et al. (2003) Multiple roles of Rev3, the catalytic subunit of pol zeta in maintaining genome stability in vertebrates. EMBO J., 22, 3188-3197.
99. Niedzwiedz,W., Mosedale,G., Johnson,M., Ong,C.Y., Pace,P. and Patel,K.J. (2004) The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell, 15, 607-620.
100. Okada,T., Sonoda,E., Yoshimura,M., Kawano,Y., Saya,H., Kohzaki,M. and Takeda,S. (2005) Multiple roles of vertebrate REV genes in DNA repair and recombination. Mol. Cell Biol., 25, 6103-6111.
101. Plosky,B.S. and Woodgate,R. (2004) Switching from high-fidelity replicases to low-fidelity lesion-bypass polymerases. Curr. Opin. Genet Dev., 14, 113-119.
102. Bauer,G.A. and Burgers,P.M. (1988) The yeast analog of mammalian cyclin/ proliferating-cell nuclear antigen interacts with mammalian DNA polymerase delta. Proc. Natl Acad Sci. USA, 85, 7506-7510.
103. Hoege,C., Pfander,B., Moldovan,G.L., Pyrowolakis,G. and Jentsch,S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature, 419, 135-141.
104. Kannouche,P.L., Wing,J. and Lehmann,A.R. (2004) Interaction of human DNA polymerase eta with morroubiquitinated PCNA: A possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell, 14, 491-500.
105. Stelter,P. and Ulrich,H.D. (2003) Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature, 425, 188-191.
106. Haracska,L., Johnson,R.E., Unk,I., Phillips,B.B., Hurwitz,J., Prakash,L. and Prakash,S. (2001) Targeting of human DNA polymerase iota to the replication machinery via interaction with PCNA. Proc. Natl Acad Sci. USA, 98, 14256-14261.
107. Haracska,L., Kondratick,C.M., Unk,I, Prakash,S. and Prakash,L. (2001) Interaction with PCNA is essential for yeast DNA polymerase eta function. Mol. Cell, 8, 407-415.
108. Haracska,L., Unk,I., Johnson,R.E., Phillips,B.B., Hurwitz,J., Prakash,L. and Prakash,S. (2002) Stimulation of DNA synthesis activity of human DNA polymerase kappa by PCNA. Mol. Cell Biol., 22, 784-791.
109. McCulloch,S.D., Kokoska R.J., Masutani C., Iwai,S., Hanaoka,F. and Kunkel,T.A. (2004) Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature, 428, 97-100.
110. Bresson,A. and Fuchs,R.P. (2002) Lesion bypass in yeast cells: Pol eta participates in a multi-DNA polymerase process. EMBO J., 21, 3881-3887.
111. McCulloch,S.D., Kokoska,R.J., Chilkova,O., Welch,C.M., Johansson,E., Burgers,P.M. and Kunkel,T.A. (2004) Enzymatic switching for efficient and accurate translesion DNA replication. Nucleic Acids Res., 32, 4665-4675.
112. Solomon,D.A., Cardoso,M.C. and Knudsen,E.S. (2004) Dynamic targeting of the replication machinery to sites of DNA damage. J. Cell Biol., 166, 455-463.
113. Masutani,C., Kusumoto,R., Yamada,A., Dohmae,N., Yokoi,M., Yuasa,M., Araki,M., Iwai,S., Takio,K. and Hanaoka,F. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature, 399, 700-704.
114. Hirano,T. (2002) The ABCs of SMC proteins: Two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev., 16, 399-414.
115. Uhlmann,F. (2004) The mechanism of sister chromatid cohesion. Exp. Cell Res., 296, 80-85.
116. Kim,J. and MacNeill,S.A. (2003) Genome stability: A new member of the RFC family. Curr. Biol., 13, R873-R875.
117. Toth,A., Ciosk,R., Uhlmann,F., Galova,M., Schleiffer,A. and Nasmyth,K. (1999) Yeast cohesin complex requires a conserved protein, Ecolp(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev., 13, 320-333.
118. Losada,A., Yokochi,T., Kobayashi,R. and Hirano,T. (2000) Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes. J. Cell Biol., 150, 405-416.
119. Sumara,I., Vorlaufer,E., Gieffers,C., Peters,B.H. and Peters,J.M. (2000) Characterization of vertebrate cohesin complexes and their regulation in prophase. J. Cell Biol., 151, 749-762.
120. Furuya,K., Takahashi,K. and Yanagida,M. (1998) Faithful anaphase is ensured by Mis4, a sister chromatid cohesion molecule required in S phase and not destroyed in G1 phase. Genes Dev., 12, 3408-3418.
121. Gillespie,P.J. and Hirano,T. (2004) Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr. Biol., 14, 1598-1603.
122. Takahashi,T.S., Yiu,P., Chou,M.F., Gygi,S. and Walter,J.C. (2004) Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat. Cell Biol., 6, 991-996.
123. Suter,B., Tong,A., Chang,M., Yu,L., Brown,G.W., Boone,C. and Rine,J. (2004) The origin recognition complex links replication, sister chromatid cohesion and transcriptional silencing in Saccharomyces cerevisiae. Genetics, 167, 579-591.
124. Skibbens,R.V., Corson,L.B., Koshland,D. and Hieter,P. (1999) Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev., 13, 307-319.
125. Edwards,S., Li,C.M., Levy,D.L., Brown,J., Snow,P.M. and Campbell,J.L. (2003) Saccharomyces cerevisiae DNA polymerase epsilon and polymerase sigma interact physically and functionally, suggesting a role for polymerase epsilon in sister chromatid cohesion. Mol. Cell Biol., 23, 2733-2748.
126. Hanna,J.S., Kroll,E.S., Lundblad,V. and Spencer,F.A. (2001) Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol. Cell Biol., 21, 3144-3158.
127. Mayer,M.L., Gygi,S.P., Aebersold,R. and Hieter,P. (2001) Identification of RFC(Ctf18p, Ctf8p, Dcc 1p): An alternative RFC complex required for sister chromatid cohesion in S.cerevisiae. Mol. Cell, 7, 959-970.
128. Kenna,M.A. and Skibbens,R.V. (2003) Mechanical link between cohesion establishment and DNA replication: Ctf7p/Eco1p, a cohesion establishment factor, associates with three different replication factor C complexes. Mol. Cell Biol., 23, 2999-3007.
129. Vega,H., Waisfisz,Q., Gordillo,M. et al. (2005) Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat. Genet., 37, 468-470.
130. Tanaka,K., Yonekawa,T., Kawasaki,Y., Kai,M., Furuya,K., Iwasaki,M., Murakami,H., Yanagida,M. and Okayama,H. (2000) Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol. Cell Biol., 20, 3459-3469.
131. Van den Berg,D.J. and Francke,U. (1993) Sensitivity of Roberts syndrome cells to gamma radiation, mitomycin C, and protein synthesis inhibitors. Somat. Cell Mol. Genet., 19, 377-392.
132. Warren,C.D., Eckley,D.M., Lee,M.S., Hanna,J.S., Hughes,A., Peyser,B., Jie,C., Irizarry,R. and Spencer,F.A. (2004) S-phase checkpoint genes safeguard high-fidelity sister chromatid cohesion. Mol. Biol. Cell, 15, 1724-1735.
133. Kim,J.S., Krasieva,T.B., LaMorte,V., Taylor,A.M. and Yokomori,K. (2002) Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem, 277, 45149-45153.
134. Birkenbihl,R.P. and Subramani,S. (1992) Cloning and characterization of rad21 an essential gene of Schizosaccharomyces pombe involved in DNA double-strand-break repair. Nucleic Acids Res., 20, 6605-6611.
135. Michaelis,C., Ciosk,R. and Nasmyth,K. (1997) Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell, 91, 35-45.
136. Hartsuiker,E., Vaessen,E., Carr,A.M. and Kohli,J. (2001) Fission yeast Rad5O stimulates sister chromatid recombination and links cohesion with repair. EMBO J., 20, 6660-6671.
137. Jessberger,R., Riwar,B., Baechtold,H. and Akhmedov,A.T. (1996) SMC proteins constitute two subunits of the mammalian recombination complex RC-1. EMBO J., 15, 4061-4068.
138. Strom,L., Lindroos,H.B., Shirahige,K. and Sjogren,C. (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell, 16, 1003-1015.
139. Nagao,K., Adachi,Y. and Yanagida,M. (2004) Separase-mediated cleavage of cohesin at interphase is required for DNA repair. Nature, 430, 1044-1048.