UV-induced RPA phosphorylation is increased in the absence of DNA polymerase η and requires DNA-PK

DNA Repair

Volumn 5, Issue 4, 2006, Pages 491-504

  Cruet Hennequart, Séverine ^a   Coyne, Seamus ^a   Glynn, Macdara T ^a   Oakley, Gregory G ^b,c   Carty, Michael P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

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

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

DNA PK; Pol ; RPA; UV damage; XPV

Indexed keywords

CHECKPOINT KINASE 1; DNA POLYMERASE; DOUBLE STRANDED DNA; NIBRIN; POL PROTEIN; PROTEIN KINASE; REPLICATION PROTEIN A; TETRACYCLINE;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING;

CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; DNA; DNA DAMAGE; DNA-ACTIVATED PROTEIN KINASE; DNA-DIRECTED DNA POLYMERASE; DOSE-RESPONSE RELATIONSHIP, RADIATION; FIBROBLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTONES; HUMANS; KINETICS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; REPLICATION PROTEIN A; TETRACYCLINE; ULTRAVIOLET RAYS;

EID: 33645366437     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.01.008     Document Type: Article

References (70)

1. B.B. Zhou, and S.J. Elledge The DNA damage response: putting checkpoints in perspective Nature 408 2000 433 439
2. N.F. Lowndes, and J.R. Murguia Sensing and responding to DNA damage Curr. Opin. Genet. Dev. 10 2000 17 25
3. E.C. Friedberg, L.D. McDaniel, and R.A. Schultz The role of endogenous and exogenous DNA damage and mutagenesis Curr. Opin. Genet. Dev. 14 2004 5 10
4. Y. Shiloh, and A.R. Lehmann Maintaining integrity Nat. Cell. Biol. 6 2004 923 928
5. D. Durocher, and S.P. Jackson DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr. Opin. Cell. Biol. 13 2001 225 231
6. Y. Shiloh ATM and ATR: networking cellular responses to DNA damage Curr. Opin. Genet. Dev. 11 2001 71 77
7. C.J. Bakkenist, and M.B. Kastan Initiating cellular stress responses Cell 118 2004 9 17
8. C.L. Limoli, E. Giedzinski, W.F. Morgan, and J.E. Cleaver Polymerase eta deficiency in the xeroderma pigmentosum variant uncovers an overlap between the S phase checkpoint and double-strand break repair Proc. Natl. Acad. Sci. U.S.A. 97 2000 7939 7946
9. J.E. Cleaver Defective repair replication of DNA in xeroderma pigmentosum Nature 218 1968 652 656
10. A.R. Lehmann, S. Kirk-Bell, C.F. Arlett, M.C. Paterson, P.H.M. Lohman, E.A. de Weerd-Kastelein, and D. Bootsma Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation Proc. Natl. Acad. Sci. U.S.A. 72 1975 219 223
11. V.M. Maher, L.M. Ouelette, R.D. Curren, and J.J. McCormick Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal human cells Nature 261 1976 593 594
12. J.E. Cleaver, and K.H. Kraemer C.A. Scriver A.L. Beaudet W.S. Sly D. Valle Metabolic Basis of Inherited Disease seventh ed. 1995 McGraw-Hill New York 4393 4419
13. J.E. Cleaver Common pathways for ultraviolet skin carcinogenesis in the repair and replication defective groups of xeroderma pigmentosum J. Dermatol. Sci. 23 2000 1 11
14. C. Masutani, R. Kusumoto, A. Yamada, N. Dohmae, M. Yokoi, M. Yuasa, M. Araki, S. Iwai, K. Takio, and F. Hanaoka The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta Nature 399 1999 700 704
15. R.E. Johnson, C.M. Kondratick, S. Prakash, and L. Prakash hRAD30 mutations in the variant form of xeroderma pigmentosum Science 285 1999 263 265
16. W.G. McGregor, D. Wei, V.M. Maher, and J.J. McCormick Abnormal, error-prone bypass of photoproducts by xeroderma pigmentosum variant cell extracts results in extreme strand bias for the kinds of mutations induced by UV light Mol. Cell. Biol. 19 1999 147 154
17. M. Thakur, M. Wernick, C. Collins, C.L. Limoli, E. Crowley, and J.E. Cleaver DNA polymerase eta undergoes alternative splicing, protects against UV sensitivity and apoptosis, and suppresses Mre11-dependent recombination Genes Chrom. Cancer 32 2001 222 235
18. J. Yao, K. Dixon, and M.P. Carty A single (6-4) photoproduct inhibits plasmid DNA replication in xeroderma pigmentosum variant cell extracts Environ. Mol. Mutagen. 38 2001 19 29
19. C.L. Limoli, E. Giedzinski, W.M. Bonner, and J.E. Cleaver UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, gamma-H2AX formation, and Mre11 relocalization Proc. Natl. Acad. Sci. U.S.A. 99 2002 233 238
20. J. Falck, J. Coates, and S.P. Jackson Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage Nature 434 2005 605 611
21. J.G. Robison, J. Elliott, K. Dixon, and G.G. Oakley Replication protein A and the Mre11.Rad50.Nbs1 complex co-localize and interact at sites of stalled replication forks J. Biol. Chem. 279 2004 34802 34810
22. E.J. Brown, and D. Baltimore Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance Genes Dev. 17 2003 615 628
23. D.A. Dart, K.E. Adams, I. Akerman, and N.D. Lakin Recruitment of the cell cycle checkpoint kinase ATR to chromatin during S-phase J. Biol. Chem. 279 2004 16433 16440
24. L. Zou, and S.J. Elledge DNA damage through ATRIP recognition of RPA-ssDNA complexes Science 300 2003 1542 1548
25. J.-S. Park, S.-J. Park, X. Peng, M. Wang, M.-A. Yu, and S.-H. Lee Involvment of DNA-dependent protein kinase in UV-induced replication arrest J. Biol. Chem. 274 1999 32520 32527
26. Y. Wang, X.Y. Zhou, H. Wang, M.S. Huq, and G. Iliakis Roles of replication protein A and DNA-dependent protein kinase in the regulation of DNA replication following DNA damage J. Biol. Chem. 274 1999 22060 22064
27. H. Wang, J. Guan, H. Wang, A.R. Perrault, Y. Wang, and G. Iliakis Replication protein A2 phosphorylation after DNA damage by the coordinated action of ataxia telangiectasia-mutated and DNA-dependent protein kinase Cancer Res. 61 2001 8554 8563
28. S.K. Binz, A.M. Sheehan, and M.S. Wold Replication protein A phosphorylation and the cellular response to DNA damage DNA Repair (Amst.) 3 2004 1015 1024
29. R. Fotedar, and J.M. Roberts Cell cycle regulated phosphorylation of RPA-32 occurs within the replication initiation complex EMBO J. 11 1992 2177 2187
30. H. Niu, H. Erdjument-Bromage, Z.Q. Pan, S.H. Lee, P. Tempst, and J. Hurwitz Mapping of amino acid residues in the p34 subunit of human single-stranded DNA-binding protein phosphorylated by DNA-dependent protein kinase and Cdc2 kinase in vitro J. Biol. Chem. 272 1997 12634 12641
31. G.G. Oakley, S.M. Patrick, J. Yao, M.P. Carty, J.J. Turchi, and K. Dixon RPA phosphorylation in mitosis alters DNA binding and protein-protein interactions Biochemistry 42 2003 3255 3264
32. V.F. Liu, and D.T. Weaver The ionizing radiation-induced replication protein A phosphorylation response differs between ataxia telangiectasia and normal human cells Mol. Cell. Biol. 13 1993 7222 7231
33. M.P. Carty, M. Zernik-Kobak, S. McGrath, and K. Dixon UV light-induced DNA synthesis arrest in HeLa cells is associated with changes in phosphorylation of human single-stranded DNA-binding protein EMBO J. 13 1994 2114 2123
34. M. Zernik-Kobak, K. Vasunia, M. Connelly, C.W. Anderson, and K. Dixon Sites of UV-induced phosphorylation of the p34 subunit of replication protein A from HeLa cells J. Biol. Chem. 272 1997 23896 23904
35. Y. Chen, and Y. Sanchez Chk1 in the DNA damage response: conserved roles from yeasts to mammals DNA Repair (Amst.) 3 2004 1025 1032
36. Y. Shiloh Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart Annu. Rev. Genet. 31 1997 635 662
37. R. Varon, C. Vissinga, M. Platzer, K.M. Cerosaletti, K.H. Chrzanowska, K. Saar, G. Beckmann, E. Seemanova, P.R. Cooper, N.J. Nowak, M. Stumm, C.M. Weemaes, R.A. Gatti, R.K. Wilson, M. Digweed, A. Rosenthal, K. Sperling, P. Concannon, and A. Reis Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome Cell 93 1998 467 476
38. J.P. Carney, R.S. Maser, H. Olivares, E.M. Davis, M. Le Beau, J.R. 3rd Yates, L. Hays, W.F. Morgan, and J.H. Petrini The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response Cell 93 1998 477 486
39. C. Featherstone, and S.P. Jackson DNA repair: the Nijmegen breakage syndrome protein Curr. Biol. 8 1998 R622 R625
40. J.H. Petrini The mammalian Mre11-Rad50-nbs1 protein complex: integration of functions in the cellular DNA-damage response Am. J. Hum. Genet. 64 1999 1264 1269
41. D.S. Lim, S.T. Kim, B. Xu, R.S. Maser, J. Lin, J.H. Petrini, and M.B. Kastan ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway Nature 404 2000 613 617
42. M. Gatei, D. Young, K.M. Cerosaletti, A. Desai-Mehta, K. Spring, S. Kozlov, M.F. Lavin, R.A. Gatti, P. Concannon, and K. Khanna ATM-dependent phosphorylation of nibrin in response to radiation exposure Nat. Genet. 25 2000 115 119
43. M.F. Lavin The Mre11 complex and ATM: a two-way functional interaction in recognising and signaling DNA double strand breaks DNA Repair (Amst.) 3 2004 1515 1520
44. S.J. Veuger, N.J. Curtin, G.C. Smith, and B.W. Durkacz Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair Oncogene 23 2004 7322 7329
45. S.J. Veuger, N.J. Curtin, C.J. Richardson, G.C. Smith, and B.W. Durkacz Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1 Cancer Res. 63 2003 6008 6015
46. J.J.J. Leahy, B.T. Golding, R.J. Griffin, I.R. Hardcastle, C. Richardson, L. Rigoreau, and G.C.M. Smith Identification of a highly potent and selective DNA-dependent protein kinase (DNA-PK) inhibitor (NU7441) by screening of chromenone libraries Bioinorg. Med. Chem. Lett. 14 2004 6083 6087
47. A. Yamada, C. Masutani, S. Iwai, and F. Hanaoka Complementation of defective translesion synthesis and UV light sensitivity in xeroderma pigmentosum variant cells by human and mouse DNA polymerase eta Nucleic Acids Res. 28 2000 2473 2480
48. C.F. Arlett, S.A. Harcourt, and B.C. Broughton The influence of caffeine on cell survival in excision-proficient and excision-deficient xeroderma pigmentosum and normal human cell strains following ultraviolet-light irradiation Mutat. Res. 33 1975 341 346
49. J.C. Boyer, W.K. Kaufmann, B.P. Brylawski, and M. Cordeiro-Stone Defective postreplication repair in xeroderma pigmentosum variant fibroblasts Cancer Res. 50 1990 2593 2598
50. J.E. Cleaver Stopping DNA replication in its tracks Science 285 1999 212 213
51. S.K. Bullock, W.K. Kaufmann, and M. Cordeiro-Stone Enhanced S phase delay and inhibition of replication of an undamaged shuttle vector in UVC-irradiated xeroderma pigmentosum variant Carcinogenesis 22 2001 233 241
52. J.E. Cleaver, V. Afzal, L. Feeney, M. McDowell, W. Sadinski, J.P. Volpe, D.B. Busch, D.M. Coleman, D.W. Ziffer, Y. Yu, H. Nagasawa, and J.B. Little Increased ultraviolet sensitivity and chromosomal instability related to P53 function in the xeroderma pigmentosum variant Cancer Res. 59 1999 1102 1108
53. A. Stary, P. Kannouche, A.R. Lehmann, and A. Sarasin Role of DNA polymerase eta in the UV mutation spectrum in human cells J. Biol. Chem. 278 2003 18767 18775
54. A. Kuzminov Single-strand interruptions in replicating chromosomes cause double-strand breaks Proc. Natl. Acad. Sci. U.S.A. 98 2001 8241
55. A. Celeste, O. Fernandez-Capetillo, M.J. Kruhlak, D.R. Pilch, D.W. Staudt, A. Lee, R.F. Bonner, W.M. Bonner, and A. Nussenzweig Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks Nat. Cell. Biol. 5 2003 675 679
56. O.K. Mirzoeva, and J.H. Petrini DNA replication-dependent nuclear dynamics of the Mre11 complex Mol. Cancer Res. 1 2003 207 218
57. I.M. Ward, and J. Chen Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress J. Biol. Chem. 276 2001 47759 47762
58. G.G. Oakley, L.I. Loberg, J. Yao, M.A. Risinger, R.L. Yunker, M. Zernik-Kobak, K.K. Khanna, M.F. Lavin, M.P. Carty, and K. Dixon UV-induced hyperphosphorylation of replication protein a depends on DNA replication and expression of ATM protein Mol. Biol. Cell. 12 2001 1199 1213
59. V.M. Vassin, M.S. Wold, and J.A. Borowiec Replication protein A (RPA) phosphorylation prevents RPA association with replication centers Mol. Cell. Biol. 24 2004 1930 1943
60. J.N. Sarkaria, R.S. Tibbetts, E.C. Busby, A.P. Kennedy, D.E. Hill, and R.T. Abraham Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin Cancer Res. 58 1998 4375 4382
61. I. Hickson, Y. Zhao, C.J. Richardson, S.J. Green, N.M. Martin, A.I. Orr, P.M. Reaper, S.P. Jackson, N.J. Curtin, and G.C. Smith Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM Cancer Res. 64 2004 9152 9159
62. Q. Liu, S. Guntuku, X.S. Cui, S. Matsuoka, D. Cortez, K. Tamai, G. Luo, S. Carattini-Rivera, F. DeMayo, A. Bradley, L.A. Donehower, and S.J. Elledge Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint Genes Dev. 14 2000 1448 1459
63. Y.W. Zhang, D.M. Otterness, G.G. Chiang, W. Xie, Y.C. Liu, F. Mercurio, and R.T. Abraham Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway Mol. Cell. 19 2005 607 618
64. E.P. Rogakou, D.R. Pilch, A.H. Orr, V.S. Ivanova, and W.M. Bonner DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139 J. Biol. Chem. 273 1998 5858 5868
65. E.I. Golub, R.C. Gupta, T. Haaf, M.S. Wold, and C.M. Radding Interaction of human rad51 recombination protein with single-stranded DNA binding protein, RPA Nucleic Acids Res. 26 1998 5388 5393
66. G. Rodrigo, S. Roumagnac, M.S. Wold, B. Salles, and P. Calsou DNA replication but not nucleotide excision repair is required for UVC-induced replication protein A phosphorylation in mammalian cells Mol. Cell. Biol. 20 2000 2696 2705
67. C. Lucca, F. Vanoli, C. Cotta-Ramusino, A. Pellicioli, G. Liberi, J. Haber, and M. Foiani Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing Oncogene 23 2004 1206 1213
68. M. Cordeiro-Stone, R.I. Schumacher, and R. Meneghini Structure of the replication fork in ultraviolet light-irradiated human cells Biophys. J. 27 1979 287 300
69. M. Cordeiro-Stone, L.S. Zaritskaya, L.K. Price, and W.K. Kaufmann Replication fork bypass of a pyrimidine dimer blocking leading strand DNA synthesis J. Biol. Chem. 272 1997 13945 13954
70. R.-G. Shao, C.-X. Cao, H. Zhang, K.W. Kohn, M.S. Wold, and Y. Pommier Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA:DNA-PK complexes EMBO J. 18 1999 1397 1406