Viral transport of DNA damage that mimics a stalled replication fork

Journal of Virology

Volumn 79, Issue 1, 2005, Pages 569-580

  Jurvansuu, Jaana ^a   Raj, Kenneth ^a   Stasiak, Andrzej ^b   Beard, Peter ^a,c  

^a National Center of Competence in Research in Molecular Oncology   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIA TELANGIECTASIA RELATED PROTEIN; ATM PROTEIN; BINDING PROTEIN; CHECKPOINT KINASE 1; DNA DIRECTED DNA POLYMERASE DELTA; NIBRIN; PROTEIN; PROTEIN HUS1; PROTEIN RAD1; PROTEIN RAD9; REPLICATION PROTEIN A; TOPOISOMERASE II BINDING PROTEIN 1; UNCLASSIFIED DRUG; VIRUS DNA;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS TYPE 2; ARTICLE; CELL CYCLE G2 PHASE; CELL VIABILITY; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA DEGRADATION; DNA REPLICATION; DNA STRUCTURE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ULTRAVIOLET IRRADIATION;

CARRIER PROTEINS; CELL LINE; DEPENDOVIRUS; DNA DAMAGE; DNA REPLICATION; DNA, VIRAL; G2 PHASE; HUMANS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASES; ULTRAVIOLET RAYS;

EID: 10644254331     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.1.569-580.2005     Document Type: Article

References (84)

1. Araki, H., S.-H. Leem, A. Phongdara, and A. Sugino. 1995. Dpb11, which interacts with DNA polymerase II(ε) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc. Natl. Acad. Sci. USA 92:11791-11795.
2. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
3. Bao, S., R. S. Tibbetts, K. M. Brumbaugh, Y. Fang, D. A. Richardson, A. Ali, S. M. Chen, R. T. Abraham, and X. F. Wang. 2001. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 411:969-974.
4. Bermudez, V. P., L. A. Lindsey-Boltz, A. J. Cesare, Y. Maniwa, J. D. Griffith, J. Hurwitz, and A. Sancar. 2003. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc. Natl. Acad. Sci. USA 100:1633-1638.
5. Berns, K. I., and R. M. Linden. 1995. The cryptic life style of adeno-associated virus. Bioessays 17:237-245.
6. Bischof, O., S. H. Kim, J. Irving, S. Beresten, N. A. Ellis, and J. Campisi. 2001. Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell Biol. 153:367-380.
7. Brosh, R. M., Jr., J. L. Li, M. K. Kenny, J. K. Karow, M. P. Cooper, R. P. Kureekattil, I. D. Hickson, and V. A. Bohr. 2000. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275:23500-23508.
8. Brown, E. J., and D. Baltimore. 2003. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17:615-628.
9. Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
10. Burtelow, M. A., P. M. Roos-Mattjus, M. Rauen, J. R. Babendure, and L. M. Karnitz. 2001. Reconstitution and molecular analysis of the hRad9-hHus1-hRad1 (9-1-1) DNA damage responsive checkpoint complex. J. Biol. Chem. 276:25903-25909.
11. Caldecott, K. W. 2003. Cell signaling. The BRCT domain: signaling with friends? Science 302:579-580.
12. Caspari, T., and A. M. Carr. 2002. Checkpoints: how to flag up double-strand breaks. Curr. Biol. 12:R105-R107.
13. Casper, A. M., P. Nghiem, M. F. Arlt, and T. W. Glover. 2002. ATR regulates fragile site stability. Cell 111:779-789.
14. Cha, R. S., and N. Kleckner. 2002. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297:602-606.
15. Chini, C. C., and J. Chen. 2003. Human claspin is required for replication checkpoint control. J. Biol. Chem. 278:30057-30062.
16. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
17. Costanzo, V., D. Shechter, P. J. Lupardus, K. A. Cimprich, M. Gottesman, and J. Gautier. 2003. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell 11:203-213.
18. Daniel, R., G. Kao, K. Taganov, J. G. Greger, O. Favorova, G. Merkel, T. J. Yen, R. A. Katz, and A. M. Skalka. 2003. Evidence that the retroviral DNA integration process triggers an ATR-dependent DNA damage response. Proc. Natl. Acad. Sci. USA 100:4778-4783.
19. de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A. M. Carr, A. R. Lehmann, and J. H. Hoeijmakers. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479-482.
20. Du, L. L., T. M. Nakamura, B. A. Moser, and P. Russell. 2003. Retention but not recruitment of Crb2 at double-strand breaks requires Rad1 and Rad3 complexes. Mol. Cell. Biol. 23:6150-6158.
21. Essers, J., A. B. Houtsmuller, L. van Veelen, C. Paulusma, A. L. Nigg, A. Pastink, W. Vermeulen, J. H. Hoeijmakers, and R. Kanaar. 2002. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J. 21:2030-2037.
22. Foray, N., D. Marot, A. Gabriel, V. Randrianarison, A. M. Carr, M. Perricaudet, A. Ashworth, and P. Jeggo. 2003. A subset of ATM- and ATR-dependent phosphorylation events requires the BRCA1 protein. EMBO J. 22:2860-2871.
23. Franchitto, A., and P. Pichierri. 2002. Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J. Cell Biol. 157:19-30.
24. Gatei, M., B. B. Zhou, K. Hobson, S. Scott, D. Young, and K. K. Khanna. 2001. Ataxia telangiectasia mutated (ATM) kinase and ATM and Rad3 related kinase mediate phosphorylation of Brca1 at distinct and overlapping sites. In vivo assessment using phospho-specific antibodies. J. Biol. Chem. 276:17276-17280.
25. Gaymes, T. J., P. S. North, N. Brady, I. D. Hickson, G. J. Mufti, and F. V. Rassool. 2002. Increased error-prone non homologous DNA end-joining - a proposed mechanism of chromosomal instability in Bloom's syndrome. Oncogene 21:2525-2533.
26. Greer, D. A., B. D. Besley, K. B. Kennedy, and S. Davey. 2003. hRad9 rapidly binds DNA containing double-strand breaks and is required for damage-dependent topoisomerase II beta binding protein 1 focus formation. Cancer Res. 63:4829-4835.
27. Griffith, J. D., L. A. Lindsey-Boltz, and A. Sancar. 2002. Structures of the human Rad17-replication factor C and checkpoint Rad 9-1-1 complexes visualized by glycerol spray/low voltage microscopy. J. Biol. Chem. 277: 15233-15236.
28. + within the DNA-structure checkpoint pathways in Schizosaccharomyces pombe. J. Cell Sci. 116:3519-3529.
29. Haruki, N., H. Saito, Y. Tatematsu, H. Konishi, T. Harano, A. Masuda, H. Osada, Y. Fujii, and T. Takahashi. 2000. Histological type-selective, tumor-predominant expression of a novel CHK1 isoform and infrequent in vivo somatic CHK2 mutation in small cell lung cancer. Cancer Res. 60:4689-4692.
30. Heffernan, T. P., D. A. Simpson, A. R. Frank, A. N. Heinloth, R. S. Paules, M. Cordeiro-Stone, and W. K. Kaufmann. 2002. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol. Cell. Biol. 22:8552-8561.
31. Hirai, I., and H. G. Wang. 2002, A role of the C-terminal region of human Rad9 (hRad9) in nuclear transport of the hRad9 checkpoint complex. J. Biol. Chem. 277:25722-25777.
32. Jiang, K., E. Pereira, M. Maxfield, B. Russell, D. M. Goudelock, and Y. Sanchez. 2003. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J. Biol. Chem. 278:25207-25217.
33. Kastan, M. B., and D. S. Lim. 2000. The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1:179-186.
34. Lee, J., A. Kumagai, and W. G. Dunphy. 2003. Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol. Cell 11:329-340.
35. Lee, J. H., B. Xu, C. H. Lee, J. Y. Ahn, M. S. Song, H. Lee, C. E. Canman, J. S. Lee, M. B. Kastan, and D. S. Lim. 2003. Distinct functions of Nijmegen breakage syndrome in ataxia telangiectasia mutated-dependent responses to DNA damage. Mol. Cancer Res. 1:674-681.
36. Lisby, M., U. H. Mortensen, and R. Rothstein. 2003. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5:572-577.
37. 2/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
38. Lukas, C., J. Falck, J. Bartkova, J. Bartek, and J. Lukas. 2003. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5:255-260.
39. Makiniemi, M., T. Hillukkala, J. Tuusa, K. Reini, M. Vaara, D. Huang, H. Pospiech, I. Majuri, T. Westerling, T. P. Makela, and J. E. Syvaoja. 2001. BRCT domain-containing protein TopBP1 functions in DNA replication and damage response. J. Biol. Chem. 276:30399-30406.
40. Manke, I. A., D. M. Lowery, A. Nguyen, and M. B. Yaffe. 2003. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636-639.
41. Marchetti, M. A., S. Kumar, E. Hartsuiker, M. Maftahi, A. M. Carr, G. A. Freyer, W. C. Burhans, and J. A. Huberman. 2002. A single unbranched S-phase DNA damage and replication fork blockage checkpoint pathway. Proc. Natl. Acad. Sci. USA 99:7472-7477.
42. Maser, R. S., K. J. Monsen, B. E. Nelms, and J. H. Petrini. 1997. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell. Biol. 17:6087-6096.
43. Meister, P., M. Poidevin, S. Francesconi, I. Tratner, P. Zarzov, and G. Baldacci. 2003. Nuclear factories for signalling and repairing DNA double strand breaks in living fission yeast. Nucleic Acids Res. 31:5064-5073.
44. Melo, J., and D. Toczyski. 2002. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14:237-245.
45. Melo, J. A., J. Cohen, and D. P. Toczyski. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15:2809-2821.
46. 1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092-9097.
47. Nghiem, P., P. K. Park, Y.-S. Kim, B. N. Desai, and S. L. Schreiber. 2002. ATR is not required for p53 activation but synergizes with p53 in the replication checkpoint. J. Biol. Chem. 277:4428-4434.
48. Nur, E. K. A., T. K. Li, A. Zhang, H. Qi, E. S. Hars, and L. F. Liu. 2003. Single-stranded DNA induces ataxia telangiectasia mutant (ATM)/p53-dependent DNA damage and apoptotic signals. J. Biol. Chem. 278:12475-12481.
49. Parrilla-Castellar, E. R., and L. M. Karnitz. 2003. Cut5 is required for the binding of Atr and DNA polymerase alpha to genotoxin-damaged chromatin. J. Biol. Chem. 278:45507-45511.
50. Post, S. M., A. E. Tomkinson, and E. Y. Lee. 2003. The human checkpoint Rad protein Rad17 is chromatin-associated throughout the cell cycle, localizes to DNA replication sites, and interacts with DNA polymerase epsilon. Nucleic Acids Res. 31:5568-5575.
51. Raj, K., P. Ogston, and P. Beard. 2001. Virus-mediated killing of cells that lack p53 activity. Nature 412:914-917.
52. Rodriguez, M., X. Yu, J. Chen, and Z. Songyang. 2003. Phosphopeptide binding specificities of BRCA1 COOH-terminal (BRCT) domains. J. Biol. Chem. 278:52914-52918.
53. Roos-Mattjus, P., K. M. Hopkins, A. J. Oestreich, B. T. Vroman, K. L. Johnson, S. Naylor, H. B. Lieberman, and L. M. Karnitz. 2003. Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J. Biol. Chem. 278:24428-24437.
54. Roos-Mattjus, P., B. T. Vroman, M. A. Burtelow, M. Rauen, A. K. Eapen, and L. M. Karnitz. 2002. Genotoxin-induced Rad9-Hus1-Rad1 (9-1-1) chromatin association is an early checkpoint signaling event. J. Biol. Chem. 277:43809-43812.
55. Roshal, M., B. Kim, Y. Zhu, P. Nghiem, and V. Planelles. 2003. Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J. Biol. Chem. 278:25879-25886.
56. Saka, Y., F. Esashi, T. Matsusaka, S. Mochida, and M. Yanagida. 1997. Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chk1. Genes Dev. 11:3387-3400.
57. Salvetti, A., S. Oreve, G. Chadeuf, D. Favre, Y. Cherel, P. Champion-Arnaud, J. David-Ameline, and P. Moullier. 1998. Factors influencing recombinant adeno-associated virus production. Hum. Gene Ther. 9:695-706.
58. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
59. Scully, R., J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, T. Ashley, and D. M. Livingston. 1997. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88:265-275.
60. Scully, R., S. Ganesan, K. Vlasakova, J. Chen, M. Socolovsky, and D. M. Livingston. 1999. Genetic analysis of BRCA1 function in a defined tumor cell line. Mol. Cell 4:1093-1099.
61. Sengupta, S., S. P. Linke, R. Pedeux, Q. Yang, J. Farnsworth, S. H. Garfield, K. Valerie, J. W. Shay, N. A. Ellis, B. Wasylyk, and C. C. Harris. 2003. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J. 22:1210-1222.
62. Sogo, J., A. Stasiak, W. DeBernardin, R. Losa, and T. Koller. 1987. Binding of proteins to nuclear acids as studied by electron microscopy, p. 61-79. In J. Sommerville and U. Scheer (ed.), Electron microscopy in molecular biology. Biology IRL Press, Oxford, United Kingdom.
63. Stasiak, A., and E. H. Egelman. 1994. Structure and function of RecA-DNA complexes. Experientia 50:192-203.
64. St. Onge, R. P., C. M. Udell, R. Casselman, and S. Davey. 1999. The human G2 checkpoint control protein hRAD9 is a nuclear phosphoprotein that forms complexes with hRAD1 and hHUS1. Mol. Biol. Cell 10:1985-1995.
65. Tang, J. Y., B. J. Hwang, J. M. Ford, P. C. Hanawalt, and G. Chu. 2000. Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis. Mol. Cell 5:737-744.
66. Tibbetts, R. S., D. Cortez, K. M. Brumbaugh, R. Scully, D. Livingston, S. J. Elledge, and R. T. Abraham. 2000. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14:2989-3002.
67. Volkmer, E., and L. M. Karnitz. 1999. Human homologs of Schizosaccharomyces pombe Rad1, Hus1, and Rad9 form a DNA damage-responsive protein complex. J. Biol. Chem. 274:567-570.
68. Wakasugi, M., A. Kawashima, H. Morioka, S. Linn, A. Sancar, T. Mori, O. Nikaido, and T. Matsunaga. 2002. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 277:1637-1640.
69. Wang, H., and S. J. Elledge. 2002. Genetic and physical interactions between DPB11 and DDC1 in the yeast DNA damage response pathway. Genetics 160:1295-1304.
70. Weiss, R. S., P. Leder, and C. Vaziri. 2003. Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Mol. Cell. Biol. 23:791-803.
71. Winocour, E., M. Callaham, and E. Huberman. 1988. Perturbation of the cell cycle by adeno-associated virus. Virology 167:393-399.
72. 2 arrests through Cdc25A degradation in response to DNA-damaging agents. J. Biol. Chem. 278:21767-21773.
73. Xu, B., A. H. O'Donnell, S. T. Kim, and M. B. Kastan. 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.
74. 2-M cell cycle checkpoint. Cancer Res. 63:3049-3053.
75. Yamane, K., X. Wu, and J. Chen. 2002. A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol. Cell. Biol. 22:555-566.
76. Yamane, K., M. Kawabata, and T. Tsuruo. 1997. A DNA-topoisomerase-II- binding protein with eight repeating regions similar to DNA-repair enzymes and to a cell-cycle regulator. Eur. J. Biochem. 250:794-799.
77. Yarden, R. I., S. Pardo-Reoyo, M. Sgagias, K. H. Cowan, and L. C. Brody. 2002. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet. 30:285-289.
78. You, Z., L. Kong, and J. Newport. 2002. The role of single-stranded DNA and polymerase alpha in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem. 277:27088-27093.
79. Yu, X., C. C. Chini, M. He, G. Mer, and J. Chen. 2003. The BRCT domain is a phospho-protein binding domain. Science 302:639-642.
80. Yuan, R., S. Fan, M. Achary, D. M. Stewart, I. D. Goldberg, and E. M. Rosen. 2001. Altered gene expression pattern in cultured human breast cancer cells treated with hepatocyte growth factor/scatter factor in the setting of DNA damage. Cancer Res. 61:8022-8031.
81. Zachos, G., M. D. Rainey, and D. A. Gillespie. 2003. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO J. 22:713-723.
82. Ziv, Y., A. Bar-Shira, I. Pecker, P. Russell, T. J. Jorgensen, I. Tsarfati, and Y. Shiloh. 1997. Recombinant ATM protein complements the cellular A-T phenotype. Oncogene 15:159-167.
83. Zou, L., D. Cortez, and S. J. Elledge. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16:198-208.
84. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.