Dealing with DNA damage: Relationships between checkpoint and repair pathways

Mutation Research - Reviews in Mutation Research

Volumn 704, Issue 1-3, 2010, Pages 2-11

  Warmerdam, Daniël O ^a   Kanaar, Roland ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Cell cycle checkpoints; DNA damage signaling; DNA repair; Genome stability

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CYCLINE; PHOSPHATIDYLINOSITOL 3 KINASE;

APOPTOSIS; CARBOXY TERMINAL SEQUENCE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA TRANSCRIPTION; EXCISION REPAIR; GENE ACTIVATION; GENE MUTATION; HOMOLOGOUS RECOMBINATION; HUMAN; MITOSIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; STRESS; SUMOYLATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

CELL CYCLE; DNA DAMAGE; DNA REPAIR; HUMANS; MODELS, BIOLOGICAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TIME;

EID: 77951974344     PISSN: 13835742     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrrev.2009.12.001     Document Type: Review

References (167)

1. Sherr C.J. D-type cyclins. Trends Biochem. Sci. 20 (1995) 187-190
2. Beijersbergen R.L., and Bernards R. Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins. Biochim. Biophys. Acta 1287 (1996) 103-120
3. Koff A., Giordano A., Desai D., Yamashita K., Harper J.W., Elledge S., Nishimoto T., Morgan D.O., Franza B.R., and Roberts J.M. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257 (1992) 1689-1694
4. van den Heuvel S., and Harlow E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262 (1993) 2050-2054
5. Obaya A.J., and Sedivy J.M. Regulation of cyclin-Cdk activity in mammalian cells. Cell. Mol. Life Sci. 59 (2002) 126-142
6. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 411 (2001) 366-374
7. Kanaar R., Wyman C., and Rothstein R. Quality control of DNA break metabolism: in the 'end', it's a good thing. EMBO J. 27 (2008) 581-588
8. Zhou B.B., and Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 408 (2000) 433-439
9. Zierhut C., and Diffley J.F. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27 (2008) 1875-1885
10. Falck J., Mailand N., Syljuasen R.G., Bartek J., and Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410 (2001) 842-847
11. Dronkert M.L., and Kanaar R. Repair of DNA interstrand cross-links. Mutat. Res. 486 (2001) 217-247
12. Wyman C., Warmerdam D.O., and Kanaar R. From DNA end chemistry to cell-cycle response: the importance of structure, even when it's broken. Mol. Cell 30 (2008) 5-6
13. Lovejoy C.A., and Cortez D. Common mechanisms of PIKK regulation. DNA Repair (Amst.) (2009)
14. Cimprich K.A., and Cortez D. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9 (2008) 616-627
15. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
16. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31 (2006) 402-410
17. Wyman C., and Kanaar R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40 (2006) 363-383
18. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
19. Lee J.H., and Paull T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304 (2004) 93-96
20. Lee J.H., and Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308 (2005) 551-554
21. Kozlov S.V., Graham M.E., Peng C., Chen P., Robinson P.J., and Lavin M.F. Involvement of novel autophosphorylation sites in ATM activation. EMBO J. 25 (2006) 3504-3514
22. Shreeram S., Demidov O.N., Hee W.K., Yamaguchi H., Onishi N., Kek C., Timofeev O.N., Dudgeon C., Fornace A.J., Anderson C.W., Minami Y., Appella E., and Bulavin D.V. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol. Cell 23 (2006) 757-764
23. Berkovich E., Monnat Jr. R.J., and Kastan M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9 (2007) 683-690
24. Pellegrini M., Celeste A., Difilippantonio S., Guo R., Wang W., Feigenbaum L., and Nussenzweig A. Autophosphorylation at serine 1987 is dispensable for murine Atm activation in vivo. Nature 443 (2006) 222-225
25. Dupre A., Boyer-Chatenet L., and Gautier J. Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat. Struct. Mol. Biol. 13 (2006) 451-457
26. Celeste A., Difilippantonio S., Difilippantonio M.J., Fernandez-Capetillo O., Pilch D.R., Sedelnikova O.A., Eckhaus M., Ried T., Bonner W.M., and Nussenzweig A. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114 (2003) 371-383
27. Bassing C.H., Suh H., Ferguson D.O., Chua K.F., Manis J., Eckersdorff M., Gleason M., Bronson R., Lee C., Alt F.W., and Histone. H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114 (2003) 359-370
28. Uziel T., Lerenthal Y., Moyal L., Andegeko Y., Mittelman L., and Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22 (2003) 5612-5621
29. Carson C.T., Schwartz R.A., Stracker T.H., Lilley C.E., Lee D.V., and Weitzman M.D. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22 (2003) 6610-6620
30. Moreno-Herrero F., de Jager M., Dekker N.H., Kanaar R., Wyman C., and Dekker C. Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 437 (2005) 440-443
31. de Jager M., van Noort J., van Gent D.C., Dekker C., Kanaar R., and Wyman C. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8 (2001) 1129-1135
32. Kanaar R., and Wyman C. DNA repair by the MRN complex: break it to make it. Cell 135 (2008) 14-16
33. Falck J., Coates J., and Jackson S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434 (2005) 605-611
34. Kitagawa R., Bakkenist C.J., McKinnon P.J., and Kastan M.B. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18 (2004) 1423-1438
35. Lee J.H., and Paull T.T. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26 (2007) 7741-7748
36. Soutoglou E., and Misteli T. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320 (2008) 1507-1510
37. Bonilla C.Y., Melo J.A., and Toczyski D.P. Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell 30 (2008) 267-276
38. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald III E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., and Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316 (2007) 1160-1166
39. Lim D.S., Kim S.T., Xu B., Maser R.S., Lin J., Petrini J.H., and Kastan M.B. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404 (2000) 613-617
40. Gatei M., Young D., Cerosaletti K.M., Desai-Mehta A., Spring K., Kozlov S., Lavin M.F., Gatti R.A., Concannon P., and Khanna K. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet. 25 (2000) 115-119
41. Stewart G.S., Last J.I., Stankovic T., Haites N., Kidd A.M., Byrd P.J., and Taylor A.M. Residual ataxia telangiectasia mutated protein function in cells from ataxia telangiectasia patients, with 5762ins137 and 7271T-->G mutations, showing a less severe phenotype. J. Biol. Chem. 276 (2001) 30133-30141
42. Kim S.T., Xu B., and Kastan M.B. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 16 (2002) 560-570
43. Lee J.H., Xu B., Lee C.H., Ahn J.Y., Song M.S., Lee H., Canman C.E., Lee J.S., Kastan M.B., and Lim D.S. Distinct functions of Nijmegen breakage syndrome in ataxia telangiectasia mutated-dependent responses to DNA damage. Mol. Cancer Res. 1 (2003) 674-681
44. Riballo E., Kuhne M., Rief N., Doherty A., Smith G.C., Recio M.J., Reis C., Dahm K., Fricke A., Krempler A., Parker A.R., Jackson S.P., Gennery A., Jeggo P.A., and Lobrich M. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16 (2004) 715-724
45. Gontijo A.M., Green C.M., and Almouzni G. Repairing DNA damage in chromatin. Biochimie 85 (2003) 1133-1147
46. Misteli T., and Soutoglou E. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat. Rev. Mol. Cell Biol. 10 (2009) 243-254
47. Zou L., Cortez D., and Elledge S.J. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16 (2002) 198-208
48. Kondo T., Wakayama T., Naiki T., Matsumoto K., and Sugimoto K. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294 (2001) 867-870
49. Melo J.A., Cohen J., and Toczyski D.P. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15 (2001) 2809-2821
50. Ellison V., and Stillman B. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5' recessed DNA. PLoS Biol. 1 (2003) E33
51. Zou L., Liu D., and Elledge S.J. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13827-13832
52. Majka J., Binz S.K., Wold M.S., and Burgers P.M. Replication protein A directs loading of the DNA damage checkpoint clamp to 5′-DNA junctions. J. Biol. Chem. 281 (2006) 27855-27861
53. Dore A.S., Kilkenny M.L., Rzechorzek N.J., and Pearl L.H. Crystal structure of the rad9-rad1-hus1 DNA damage checkpoint complex-implications for clamp loading and regulation. Mol. Cell 34 (2009) 735-745
54. Essers J., Theil A.F., Baldeyron C., van Cappellen W.A., Houtsmuller A.B., Kanaar R., and Vermeulen W. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25 (2005) 9350-9359
55. Leonhardt H., Rahn H.P., Weinzierl P., Sporbert A., Cremer T., Zink D., and Cardoso M.C. Dynamics of DNA replication factories in living cells. J. Cell Biol. 149 (2000) 271-280
56. Somanathan S., Suchyna T.M., Siegel A.J., and Berezney R. Targeting of PCNA to sites of DNA replication in the mammalian cell nucleus. J. Cell Biochem. 81 (2001) 56-67
57. Medhurst A.L., Warmerdam D.O., Akerman I., Verwayen E.H., Kanaar R., Smits V.A., and Lakin N.D. ATR and Rad17 collaborate in modulating Rad9 localisation at sites of DNA damage. J. Cell Sci. 121 (2008) 3933-3940
58. Majka J., Niedziela-Majka A., and Burgers P.M. The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint. Mol. Cell 24 (2006) 891-901
59. Lee J., Kumagai A., and Dunphy W.G. The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. J. Biol. Chem. 282 (2007) 28036-28044
60. Delacroix S., Wagner J.M., Kobayashi M., Yamamoto K., and Karnitz L.M. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev. 21 (2007) 1472-1477
61. Bao S., Tibbetts R.S., Brumbaugh K.M., Fang Y., Richardson D.A., Ali A., Chen S.M., Abraham R.T., and Wang X.F. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 411 (2001) 969-974
62. Wang X., Zou L., Lu T., Bao S., Hurov K.E., Hittelman W.N., Elledge S.J., and Li L. Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol. Cell 23 (2006) 331-341
63. Yoo H.Y., Kumagai A., Shevchenko A., Shevchenko A., and Dunphy W.G. Ataxia-telangiectasia mutated (ATM)-dependent activation of ATR occurs through phosphorylation of TopBP1 by ATM. J. Biol. Chem. 282 (2007) 17501-17506
64. Mamely I., van Vugt M.A., Smits V.A., Semple J.I., Lemmens B., Perrakis A., Medema R.H., and Freire R. Polo-like kinase-1 controls proteasome-dependent degradation of Claspin during checkpoint recovery. Curr. Biol. 16 (2006) 1950-1955
65. Essers J., Vermeulen W., and Houtsmuller A.B. DNA damage repair: anytime, anywhere?. Curr. Opin. Cell Biol. 18 (2006) 240-246
66. Lukas J., Lukas C., and Bartek J. Mammalian cell cycle checkpoints: signalling pathways and their organization in space and time. DNA Repair (Amst.) 3 (2004) 997-1007
67. Smits V.A. Spreading the signal: dissociation of Chk1 from chromatin. Cell Cycle 5 (2006) 1039-1043
68. Smits V.A., Reaper P.M., and Jackson S.P. Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Curr. Biol. 16 (2006) 150-159
69. Lukas C., Falck J., Bartkova J., Bartek J., and Lukas J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5 (2003) 255-260
70. Kramer A., Mailand N., Lukas C., Syljuasen R.G., Wilkinson C.J., Nigg E.A., Bartek J., and Lukas J. Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat. Cell Biol. 6 (2004) 884-891
71. 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
72. 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
73. Kannouche P.L., Wing J., and Lehmann A.R. 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
74. Lehmann A.R. Translesion synthesis in mammalian cells. Exp. Cell Res. 312 (2006) 2673-2676
75. Fu Y., Zhu Y., Zhang K., Yeung M., Durocher D., and Xiao W. Rad6-Rad18 mediates a eukaryotic SOS response by ubiquitinating the 9-1-1 checkpoint clamp. Cell 133 (2008) 601-611
76. Jansen J.G., Fousteri M.I., and de Wind N. Send in the clamps: control of DNA translesion synthesis in eukaryotes. Mol. Cell 28 (2007) 522-529
77. Sabbioneda S., Minesinger B.K., Giannattasio M., Plevani P., Muzi-Falconi M., and Jinks-Robertson S. The 9-1-1 checkpoint clamp physically interacts with polzeta and is partially required for spontaneous polzeta-dependent mutagenesis in Saccharomyces cerevisiae. J. Biol. Chem. 280 (2005) 38657-38665
78. Kai M., Furuya K., Paderi F., Carr A.M., and Wang T.S. Rad3-dependent phosphorylation of the checkpoint clamp regulates repair-pathway choice. Nat. Cell Biol. 9 (2007) 691-697
79. Stewart G.S., Panier S., Townsend K., Al-Hakim A.K., Kolas N.K., Miller E.S., Nakada S., Ylanko J., Olivarius S., Mendez M., Oldreive C., Wildenhain J., Tagliaferro A., Pelletier L., Taubenheim N., Durandy A., Byrd P.J., Stankovic T., Taylor A.M., and Durocher D. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136 (2009) 420-434
80. Bergink S., Salomons F.A., Hoogstraten D., Groothuis T.A., de Waard H., Wu J., Yuan L., Citterio E., Houtsmuller A.B., Neefjes J., Hoeijmakers J.H., Vermeulen W., and Dantuma N.P. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20 (2006) 1343-1352
81. Mailand N., Bekker-Jensen S., Faustrup H., Melander F., Bartek J., Lukas C., and Lukas J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131 (2007) 887-900
82. Huen M.S., Grant R., Manke I., Minn K., Yu X., Yaffe M.B., and Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131 (2007) 901-914
83. Kolas N.K., Chapman J.R., Nakada S., Ylanko J., Chahwan R., Sweeney F.D., Panier S., Mendez M., Wildenhain J., Thomson T.M., Pelletier L., Jackson S.P., and Durocher D. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318 (2007) 1637-1640
84. Muller S., Hoege C., Pyrowolakis G., and Jentsch S. SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2 (2001) 202-210
85. Bergink S., and Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458 (2009) 461-467
86. Ulrich H.D. Preface. Ubiquitin, SUMO and the maintenance of genome stability. DNA Repair (Amst.) 8 (2009) 429
87. Hu J., McCall C.M., Ohta T., and Xiong Y. Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat. Cell Biol. 6 (2004) 1003-1009
88. Yang X., Menon S., Lykke-Andersen K., Tsuge T., Di X., Wang X., Rodriguez-Suarez R.J., Zhang H., and Wei N. The COP9 signalosome inhibits p27(kip1) degradation and impedes G1-S phase progression via deneddylation of SCF Cul1. Curr. Biol. 12 (2002) 667-672
89. Lieber M.R., Ma Y., Pannicke U., and Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4 (2003) 712-720
90. Wilson T.E., Grawunder U., and Lieber M.R. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388 (1997) 495-498
91. Lees-Miller S.P., and Meek K. Repair of DNA double strand breaks by non-homologous end joining. Biochimie 85 (2003) 1161-1173
92. Ahnesorg P., Smith P., and Jackson S.P. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124 (2006) 301-313
93. Ma Y., Pannicke U., Schwarz K., and Lieber M.R. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108 (2002) 781-794
94. Ma Y., Schwarz K., and Lieber M.R. The Artemis: DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. DNA Repair (Amst.) 4 (2005) 845-851
95. Goodarzi A.A., Yu Y., Riballo E., Douglas P., Walker S.A., Ye R., Harer C., Marchetti C., Morrice N., Jeggo P.A., and Lees-Miller S.P. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J. 25 (2006) 3880-3889
96. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., and Jackson S.P. Human CtIP promotes DNA end resection. Nature 450 (2007) 509-514
97. Paull T.T., and Gellert M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 (1998) 969-979
98. Eppink B., Wyman C., and Kanaar R. Multiple interlinked mechanisms to circumvent DNA replication roadblocks. Exp. Cell Res. 312 (2006) 2660-2665
99. Agarwal S., Tafel A.A., and Kanaar R. DNA double-strand break repair and chromosome translocations. DNA Repair (Amst.) 5 (2006) 1075-1081
100. Modesti M., Budzowska M., Baldeyron C., Demmers J.A., Ghirlando R., and Kanaar R. RAD51AP1 is a structure-specific DNA binding protein that stimulates joint molecule formation during RAD51-mediated homologous recombination. Mol. Cell 28 (2007) 468-481
101. Essers J., Hendriks R.W., Swagemakers S.M., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H., and Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89 (1997) 195-204
102. Friedberg E.C., Aguilera A., Gellert M., Hanawalt P.C., Hays J.B., Lehmann A.R., Lindahl T., Lowndes N., Sarasin A., and Wood R.D. DNA repair: from molecular mechanism to human disease. DNA Repair (Amst.) 5 (2006) 986-996
103. Hoogstraten D., Bergink S., Ng J.M., Verbiest V.H., Luijsterburg M.S., Geverts B., Raams A., Dinant C., Hoeijmakers J.H., Vermeulen W., and Houtsmuller A.B. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J. Cell Sci. 121 (2008) 2850-2859
104. Nishi R., Alekseev S., Dinant C., Hoogstraten D., Houtsmuller A.B., Hoeijmakers J.H., Vermeulen W., Hanaoka F., and Sugasawa K. UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells. DNA Repair (Amst.) 8 (2009) 767-776
105. Sugasawa K., Okuda Y., Saijo M., Nishi R., Matsuda N., Chu G., Mori T., Iwai S., Tanaka K., Tanaka K., and Hanaoka F. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121 (2005) 387-400
106. de Laat W.L., Jaspers N.G., and Hoeijmakers J.H. Molecular mechanism of nucleotide excision repair. Genes Dev. 13 (1999) 768-785
107. Giglia-Mari G., Coin F., Ranish J.A., Hoogstraten D., Theil A., Wijgers N., Jaspers N.G., Raams A., Argentini M., van der Spek P.J., Botta E., Stefanini M., Egly J.M., Aebersold R., Hoeijmakers J.H., and Vermeulen W. A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat. Genet. 36 (2004) 714-719
108. Huang J.C., Svoboda D.L., Reardon J.T., and Sancar A. Human nucleotide excision nuclease removes thymine dimers from DNA by incising the 22nd phosphodiester bond 5′ and the 6th phosphodiester bond 3′ to the photodimer. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 3664-3668
109. Moser J., Kool H., Giakzidis I., Caldecott K., Mullenders L.H., and Fousteri M.I. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol. Cell 27 (2007) 311-323
110. Dinant C., Luijsterburg M.S., Hofer T., von Bornstaedt G., Vermeulen W., Houtsmuller A.B., and van Driel R. Assembly of multiprotein complexes that control genome function. J. Cell Biol. 185 (2009) 21-26
111. Politi A., Mone M.J., Houtsmuller A.B., Hoogstraten D., Vermeulen W., Heinrich R., and van Driel R. Mathematical modeling of nucleotide excision repair reveals efficiency of sequential assembly strategies. Mol. Cell 19 (2005) 679-690
112. Mimitou E.P., and Symington L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455 (2008) 770-774
113. Gravel S., Chapman J.R., Magill C., and Jackson S.P. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22 (2008) 2767-2772
114. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., and Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134 (2008) 981-994
115. 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
116. Shiotani B., and Zou L. Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol. Cell 33 (2009) 547-558
117. El-Shemerly M., Hess D., Pyakurel A.K., Moselhy S., and Ferrari S. ATR-dependent pathways control hEXO1 stability in response to stalled forks. Nucleic Acids Res. 36 (2008) 511-519
118. El-Shemerly M., Janscak P., Hess D., Jiricny J., and Ferrari S. Degradation of human exonuclease 1b upon DNA synthesis inhibition. Cancer Res. 65 (2005) 3604-3609
119. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G., Beverloo H.B., Hoeijmakers J.H., and Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 24 (2004) 5776-5787
120. Hanada K., Budzowska M., Modesti M., Maas A., Wyman C., Essers J., and Kanaar R. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J. 25 (2006) 4921-4932
121. Hanada K., Budzowska M., Davies S.L., van Drunen E., Onizawa H., Beverloo H.B., Maas A., Essers J., Hickson I.D., and Kanaar R. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14 (2007) 1096-1104
122. Munoz I.M., Hain K., Declais A.C., Gardiner M., Toh G.W., Sanchez-Pulido L., Heuckmann J.M., Toth R., Macartney T., Eppink B., Kanaar R., Ponting C.P., Lilley D.M., and Rouse J. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 35 (2009) 116-127
123. Svendsen J.M., Smogorzewska A., Sowa M.E., O'Connell B.C., Gygi S.P., Elledge S.J., and Harper J.W. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138 (2009) 63-77
124. Klein H.L., and Symington L.S. Breaking up just got easier to do. Cell 138 (2009) 20-22
125. Andersen S.L., Bergstralh D.T., Kohl K.P., LaRocque J.R., Moore C.B., and Sekelsky J. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell 35 (2009) 128-135
126. Fekairi S., Scaglione S., Chahwan C., Taylor E.R., Tissier A., Coulon S., Dong M.Q., Ruse C., Yates III J.R., Russell P., Fuchs R.P., McGowan C.H., and Gaillard P.H. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138 (2009) 78-89
127. Ip S.C., Rass U., Blanco M.G., Flynn H.R., Skehel J.M., and West S.C. Identification of Holliday junction resolvases from humans and yeast. Nature 456 (2008) 357-361
128. Hinz J.M., Yamada N.A., Salazar E.P., Tebbs R.S., and Thompson L.H. Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Repair (Amst.) 4 (2005) 782-792
129. Huertas P., Cortes-Ledesma F., Sartori A.A., Aguilera A., and Jackson S.P. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455 (2008) 689-692
130. Huertas P., and Jackson S.P. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 284 (2009) 9558-9565
131. Barlow J.H., Lisby M., and Rothstein R. Differential regulation of the cellular response to DNA double-strand breaks in G1. Mol. Cell 30 (2008) 73-85
132. Lisby M., Barlow J.H., Burgess R.C., and Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118 (2004) 699-713
133. Wong A.K., Pero R., Ormonde P.A., Tavtigian S.V., and Bartel P.L. RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J. Biol. Chem. 272 (1997) 31941-31944
134. Chen P.L., Chen C.F., Chen Y., Xiao J., Sharp Z.D., and Lee W.H. The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 5287-5292
135. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4 (2003) 435-445
136. Esashi F., Christ N., Gannon J., Liu Y., Hunt T., Jasin M., and West S.C. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434 (2005) 598-604
137. Ferrari G., Rossi R., Arosio D., Vindigni A., Biamonti G., and Montecucco A. Cell cycle-dependent phosphorylation of human DNA ligase I at the cyclin-dependent kinase sites. J. Biol. Chem. 278 (2003) 37761-37767
138. Montecucco A., Rossi R., Levin D.S., Gary R., Park M.S., Motycka T.A., Ciarrocchi G., Villa A., Biamonti G., and Tomkinson A.E. DNA ligase I is recruited to sites of DNA replication by an interaction with proliferating cell nuclear antigen: identification of a common targeting mechanism for the assembly of replication factories. EMBO J. 17 (1998) 3786-3795
139. Cardoso M.C., Joseph C., Rahn H.P., Reusch R., Nadal-Ginard B., and Leonhardt H. Mapping and use of a sequence that targets DNA ligase I to sites of DNA replication in vivo. J. Cell Biol. 139 (1997) 579-587
140. Tomkinson A.E., and Levin D.S. Mammalian DNA ligases. Bioessays 19 (1997) 893-901
141. Martin I.V., and MacNeill S.A. ATP-dependent DNA ligases. Genome Biol. 3 (2002) (Review S3005)
142. Song W., Levin D.S., Varkey J., Post S., Bermudez V.P., Hurwitz J., and Tomkinson A.E. A conserved physical and functional interaction between the cell cycle checkpoint clamp loader and DNA ligase I of eukaryotes. J. Biol. Chem. 282 (2007) 22721-22730
143. Song W., Pascal J.M., Ellenberger T., and Tomkinson A.E. The DNA binding domain of human DNA ligase I interacts with both nicked DNA and the DNA sliding clamps, PCNA and hRad9-hRad1-hHus1. DNA Repair (Amst.) (2009)
144. Marini F., Nardo T., Giannattasio M., Minuzzo M., Stefanini M., Plevani P., Muzi M., and Falconi. DNA nucleotide excision repair-dependent signaling to checkpoint activation. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 17325-17330
145. Stiff T., Walker S.A., Cerosaletti K., Goodarzi A.A., Petermann E., Concannon P., O'Driscoll M., and Jeggo P.A. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J. 25 (2006) 5775-5782
146. Lazzaro F., Giannattasio M., Puddu F., Granata M., Pellicioli A., Plevani P., and Muzi-Falconi M. Checkpoint mechanisms at the intersection between DNA damage and repair. DNA Repair (Amst.) (2009)
147. Nakada D., Hirano Y., and Sugimoto K. Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway. Mol. Cell. Biol. 24 (2004) 10016-10025
148. 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
149. Marti T.M., Hefner E., Feeney L., Natale V., and Cleaver J.E. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 9891-9896
150. O'Driscoll M., Ruiz-Perez V.L., Woods C.G., Jeggo P.A., and Goodship J.A. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33 (2003) 497-501
151. Costanzo V., Shechter D., Lupardus P.J., Cimprich K.A., Gottesman M., and Gautier J. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell 11 (2003) 203-213
152. Warmerdam D.O., Freire R., Kanaar R., and Smits V.A. Cell cycle-dependent processing of DNA lesions controls localization of Rad9 to sites of genotoxic stress. Cell Cycle 8 (2009)
153. Roos-Mattjus P., Vroman B.T., Burtelow M.A., Rauen M., Eapen A.K., and Karnitz L.M. Genotoxin-induced Rad9-Hus1-Rad1 (9-1-1) chromatin association is an early checkpoint signaling event. J. Biol. Chem. 277 (2002) 43809-43812
154. Bomgarden R.D., Lupardus P.J., Soni D.V., Yee M.C., Ford J.M., and Cimprich K.A. Opposing effects of the UV lesion repair protein XPA and UV bypass polymerase eta on ATR checkpoint signaling. EMBO J. 25 (2006) 2605-2614
155. Shell S.M., Li Z., Shkriabai N., Kvaratskhelia M., Brosey C., Serrano M.A., Chazin W.J., Musich P.R., and Zou Y. Checkpoint kinase ATR promotes nucleotide excision repair of UV-induced DNA damage via physical interaction with XPA. J. Biol. Chem. (2009)
156. Deckbar D., Birraux J., Krempler A., Tchouandong L., Beucher A., Walker S., Stiff T., Jeggo P., and Lobrich M. Chromosome breakage after G2 checkpoint release. J. Cell Biol. 176 (2007) 749-755
157. Callegari A.J., and Kelly T.J. Shedding light on the DNA damage checkpoint. Cell Cycle 6 (2007) 660-666
158. Watrin E., and Peters J.M. The cohesin complex is required for the DNA damage-induced G2/M checkpoint in mammalian cells. EMBO J. (2009)
159. Yazdi P.T., Wang Y., Zhao S., Patel N., Lee E.Y., and Qin J. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev. 16 (2002) 571-582
160. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
161. Buscemi G., Perego P., Carenini N., Nakanishi M., Chessa L., Chen J., Khanna K., and Delia D. Activation of ATM and Chk2 kinases in relation to the amount of DNA strand breaks. Oncogene 23 (2004) 7691-7700
162. Dinant C., de Jager M., Essers J., van Cappellen W.A., Kanaar R., Houtsmuller A.B., and Vermeulen W. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 120 (2007) 2731-2740
163. Aten J.A., Stap J., Krawczyk P.M., van Oven C.H., Hoebe R.A., Essers J., and Kanaar R. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303 (2004) 92-95
164. Stap J., Krawczyk P.M., Van Oven C.H., Barendsen G.W., Essers J., Kanaar R., and Aten J.A. Induction of linear tracks of DNA double-strand breaks by alpha-particle irradiation of cells. Nat. Methods 5 (2008) 261-266
165. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., and Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173 (2006) 195-206
166. Mone M.J., Volker M., Nikaido O., Mullenders L.H., van Zeeland A.A., Verschure P.J., Manders E.M., and van Driel R. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2 (2001) 1013-1017
167. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., and Jackson S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 37-45