Chk2 Phosphorylation of BRCA1 Regulates DNA Double-Strand Break Repair

Molecular and Cellular Biology

Volumn 24, Issue 2, 2004, Pages 708-718

  Zhang, Junran ^a   Willers, Henning ^a   Feng, Zhihui ^a   Ghosh, Jagadish C ^a   Kim, Sang ^b   Weaver, David T ^c   Chung, Jay H ^d   Powell, Simon N ^a   Xia, Fen ^a,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^c CENTER FOR BLOOD RESEARCH   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 2; DOUBLE STRANDED DNA; PLASMID DNA; RAD51 PROTEIN; SERINE;

ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CELL TRANSFORMATION; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; GENE MUTATION; GENE STRUCTURE; GENETIC PREDISPOSITION; GENETIC RECOMBINATION; GENETIC STABILITY; GERM LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TUMOR SUPPRESSOR GENE;

BINDING SITES; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA REPAIR; DNA-BINDING PROTEINS; FEMALE; HUMANS; MODELS, BIOLOGICAL; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PLASMIDS; PROTEIN-SERINE-THREONINE KINASES; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SERINE; TUMOR SUPPRESSOR PROTEINS;

EID: 0346095320     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.2.708-718.2004     Document Type: Article

References (76)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Attikum, H. V., P. Bundock, and P. J. J. Hooykaas. 2001. Non-homologous end-joining proteins are required for Agrobacterium T-DNA integration. EMBO J. 20:6550-6558.
3. Baumann, P., and S. C. West. 1998. DNA end-joining catalyzed by human cell-free extracts. Proc. Natl. Acad. Sci. USA 95:14066-14070.
4. Bell, D. W., J. M. Varley, T. E. Szydlo, D. H. Kang, D. C. R. Wahrer, K. E. Shannon, M. Lubratovich, S. J. Verselis, K. J. Isselbacher, J. F. Fraumeni, J. M. Birch, F. P. Li, J. E. Garber, and D. A. Haber. 1999. Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science 286:2528-2531.
5. Bhattacharyya, A., U. S. Ear, B. H. Koller, R. R. Weichselbaum, and D. K. Bishop. 2000. The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J. Biol. Chem. 275:23899-23903.
6. Bochar, D. A., L. Wang, H. Beniya, A. Kinev, Y. Xue, W. S. Lane, W. Wang, F. Kashanchi, and R. Shiekhattar. 2000. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 102:257-265.
7. Buscemi, G., C. Savio, L. Zannini, F. Micciche, D. Masnada, M. Nakanishi, H. Tauchi, K. Komatsu, S. Mizutani, K. Khanna, P. Chen, P. Concannon, L. Chessa, and D. Delia. 2001. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 21:5214-5222.
8. Carney, J. P., R. S. Maser, H. Olivares, E. M. Davis, M. Le Beau, J. R. Yates, 3rd, L. Hays, W. F. Morgan, and J. H. Petrini. 1998. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477-486.
9. Caspari, T., J. M. Murray, and A. M. Carr. 2002. Cdc2-cyclin B kinase activity links Crb2 and Rqhl-topoisomerase III. Genes Dev. 16:1195-1208.
10. Chen, J., D. P. Silver, D. Walpita, S. B. Cantor, A. F. Gazdar, G. Tomlinson, F. J. Couch, B. L. Weber, T. Ashley, D. M. Livingston, and R. Scully. 1998. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell 2:317-328.
11. Chen, L., K. Trujillo, W. Ramos, P. Sung, and A. E. Tomkinson. 2001. Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdfl/Hdf2 complexes. Mol. Cell 8:1105-1115.
12. Cortez, D., Y. Wang, J. Qin, and S. J. Elledge. 1999. Requirement of ATM-dependent phosphorylation of BRCA1 in the DNA damage response to double-strand breaks. Science 286:1162-1166.
13. Critchlow, S. E., and S. P. Jackson. 1998. DNA end-joining: from yeast to man. Trends Biochem. Sci. 23:394-398.
14. Dai, Y., B. Kysela, L. A. Hanakahi, K. Manolis, E. Riballo, M. Stumm, T. O. Harville, S. C. West, M. A. Oettinger, and P. A. Jeggo. 2003. Nonhomologous end joining and V(D)J recombination require an additional factor. Proc. Natl. Acad. Sci. USA 100:2462-2467.
15. Desai-Mehta, A., K. M. Cerosaletti, and P. Concannon. 2001. Distinct functional domains of nibrin mediate Mrell binding, focus formation, and nuclear localization. Mol. Cell. Biol. 21:2184-2191.
16. Dronkert, M. L., and R. Kanaar. 2001. Repair of DNA interstrand cross-links. Mutat. Res. 486:217-247.
17. Falck, J., J. H. J. Petrini, B. R. Williams, J. Lukas, and J. Bartek. 2002. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet. 30:290-294.
18. Finnie, N. J., T. M. Gottlieb, T. Blunt, P. A. Jeggo, and S. P. Jackson. 1995. DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 92:320-324.
19. Gatel, 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.
20. Girard, P. M., N. Foray, M. Stumm, A. Waugh, E. Riballo, R. S. Maser, W. P. Phillips, J. Petrini, C. F. Arlett, and P. A. Jeggo. 2000. Radiosensitivity in Nijmegen Breakage syndrome cells is attributable to a repair defect and not cell cycle checkpoint defects. Cancer Res. 60:4881-4888.
21. Haber, J. E. 1998. The many interfaces of Mre11. Cell 95:583-586.
22. Harfst, E., S. Cooper, S. Neubauer, L. Distel, and U. Grawunder. 2000. Normal V(D)J recombination in cells from patients with Nijmegen breakage syndrome. Mol. Immunol. 37:915-929.
23. Harrington, J., C. L. Hsieh, J. Gerton, G. Bosma, and M. R. Lieber. 1992. Analysis of the defect in DNA end joining in the murine scid mutation. Mol. Cell. Biol. 12:4758-4768.
24. Jeggo, P. A., and J. Smith-Ravin. 1989. Decreased stable transfection frequencies of six X-ray-sensitive CHO strains, all members of the xrs complementation group. Mutat. Res. 218:75-86.
25. Johnson, A. P., and M. P. Fairman. 1996. The identification and characterization of mammalian proteins involved in the rejoining of DNA double-strand breaks in vitro. Mutat. Res. 364:103-116.
26. Kabotyanski, E. B., L. Gomelsky, J. O. Han, T. D. Stamato, and D. B. Roth. 1998. Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res. 26:5333-5342.
27. Kastan, M. B., and D. S. Lim. 2000. The many substrates and functions of ATM. Nat. Rev. Mol. Cell. Biol. 1:179-186.
28. Kerr P, A. A. 2001. New complexities for BRCA1 and BRCA2. Curr. Biol. 11:R668-R676.
29. Khanna, K. K., and S. P. Jackson. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:247-254.
30. Lee, J. S., K. M. Collins, A. L. Brown, C. H. Lee, and J. H. Chung. 2000. hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature 404:201-204.
31. Lee, S. B., S. H. Kim, D. W. Bell, D. C. Wahrer, T. A. Schiripo, M. M. Jorczak, D. C. Sgroi, J. E. Garber, F. P. Li, K. E. Nichols, J. M. Varley, A. K. Godwin, K. M. Shannon, E. Harlow, and D. A. Haber. 2001. Destabilization of CHK2 by a missense mutation associated with Li-Fraumeni Syndrome. Cancer Res. 61:8062-8067.
32. Luo, C. M., W. Tang, K. L. Mekeel, J. S. DeFrank, P. R. Anne, and S. N. Powell. 1996. High frequency and error-prone DNA recombination in ataxia telangiectasia cell lines. J. Biol. Chem. 271:4497-4503.
33. MacQueen, A. J., and A. M. Villeneuve. 2001. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 15:1674-1687.
34. Manolis, K. G., E. R. Nimmo, E. Hartsuiker, A. M. Carr, P. A. Jeggo, and R. C. Allshire. 2001. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20:210-221.
35. Maser, R. S., O. K. Mirzoeva, J. Wells, H. Olivares, B. R. Williams, R. A. Zinkel, P. J. Farnham, and J. H. J. Petrini. 2001. Mrell complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol. 21:6006-6016.
36. 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.
37. Meijers-Heijboer, H., A. van den Ouweland, J. Klijn, M. Wasielewski, A. de Snoo, R. Oldenburg, A. Hollestelle, M. Houben, E. Crepin, M. van Veghel-Plandsoen, F. Elstrodt, C. van Duijn, C. Bartels, C. Meijers, M. Schutte, L. McGuffog, D. Thompson, D. Easton, N. Sodha, S. Seal, R. Barfoot, J. Mangion, J. Chang-Claude, D. Eccles, R. Eeles, D. G. Evans, R. Houlston, V. Murday, S. Narod, T. Peretz, J. Peto, C. Phelan, H. X. Zhang, C. Szabo, P. Devilee, D. Goldgar, P. A. Futreal, K. L. Nathanson, B. Weber, N. Rahman, and M. R. Stratton. 2002. Low-penetrance susceptibility to breast cancer due to CHEK2(*)1100delC in noncarriers of BRCA1 or BRCA2 mutations. Nat. Genet. 31:55-59.
38. Mekeel, K. L., W. Tang, L. A. Kachnic, C. M. Luo, J. S. DeFrank, and S. N. Powell. 1997. Inactivation of p53 results in high rates of homologous recombination. Oncogene 14:1847-1857.
39. Mirzoeva, O. K., and J. H. Petrini. 2001. DNA damage-dependent nuclear dynamics of the Mrell complex. Mol. Cell. Biol. 21:281-288.
40. Moynahan, M. E., J. W. Chiu, B. H. Koller, and M. Jasin. 1999. Brca1 controls homology-directed DNA repair. Mol. Cell 4:511-518.
41. Moynahan, M. E., T. Y. Cui, and M. Jasin. 2001. Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer Res. 61:4842-4850.
42. Okada, S., and T. Ouchi. 2003. Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. J. Biol. Chem. 278:2015-2020.
43. Parvin, J. D. 2001. BRCA1 at a branch point. Proc. Natl. Acad. Sci. USA 98:5952-5954.
44. Paull, T. T., D. Cortez, B. Bowers, S. J. Elledge, and M. Gellert. 2001. From the cover: direct DNA binding by Brca1. Proc. Natl. Acad. Sci. USA 98:6086-6091.
45. Paull, T. T., and M. Gellert. 1999. Nbsl potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13:1276-1288.
46. Paull, T. T., E. P. Rogakou, V. Yamazaki, C. U. Kirchgessner, M. Gellert, and W. M. Bonner. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10:886-895.
47. Pierce, A. J., R. D. Johnson, L. H. Thompson, and M. Jasin. 1999. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13:2633-2638.
48. Pierce, A. J., J. M. Stark, F. D. Araujo, M. E. Moynahan, M. Berwick, and M. Jasin. 2001, Double-strand breaks and tumorigenesis. Trends Cell Biol. 11:S52-S59.
49. Prudden, J., J. S. Evans, S. P. Hussey, B. Deans, P. O'Neill, J. Thacker, and T. Humphrey. 2003. Pathway utilization in response to a site-specific DNA double-strand break in fission yeast. EMBO J. 22:1419-1430.
50. Rahman, N., and M. R. Stratton. 1998. The genetics of breast cancer susceptibility. Annu. Rev. Genet. 32:95-121.
51. Schiestl, R. H., J. Zhu, and T. D. Petes. 1994. Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 4493-4500.
52. 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.
53. 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.
54. Scully, R., and D. M. Livingston. 2000. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature 408:429-432.
55. Snouwaert, J. N., L. C. Gowen, A. M. Latour, A. R. Mohn, A. Xiao, L. DiBiase, and B. H. Koller. 1999. BRCA1 deficient embryonic stem cells display a decreased homologous recombination frequency and an increased frequency of non-homologous recombination that is corrected by expression of a Brca1 transgene. Oncogene 18:7900-7907.
56. Stewart, G. S., R. S. Maser, T. Stankovic, D. A. Bressan, M. I. Kaplan, N. G. J. Jaspers, A. Raams, P. J. Byrd, J. H. J. Petrini, and A. M. R. Taylor. 1999. The DNA double-strand break repair gene hMREll is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99:577-587.
57. Taniguchi, T., I. Garcia-Higuera, B. Xu, P. R. Andreassen, R. C. Gregory, S. T. Kim, W. S. Lane, M. B. Kastan, and A. D. D'Andrea. 2002. Convergence of the fanconi anemia and ataxia telangiectasia signaling pathways. Cell 109:459-472.
58. Tauchi, H., J. Kobayashi, K. Morishima, D. C. van Gent, T. Shiraishi, N. S. Verkaik, D. vanHeems, E. Ito, A. Nakamura, E. Sonoda, M. Takata, S. Takeda, S. Matsuura, and K. Komatsu. 2002. Nbsl is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 420: 93-98.
59. Thompson, L. H., and D. Schild. 2001. Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat. Res. 477:131-153.
60. 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.
61. Tomlinson, G. E., T. T. Chen, V. A. Stastny, A. K. Virmani, M. A. Spillman, V. Tonk, J. L. Blum, N. R. Schneider, Wistuba II, J. W. Shay, J. D. Minna, and A. F. Gazdar. 1998. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58:3237-3242.
62. van Gent, D. C., J. H. Hoeijmakers, and R. Kanaar. 2001. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2:196-206.
63. Venkitaraman, A. R. 2002. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108:171-182.
64. Wang, H., Z. C. Zeng, T. A. Bui, S. J. DiBiase, W. Qin, F. Xia, S. N. Powell, and G. Iliakis. 2001. Nonhomologous end-joining of ionizing radiation-induced DNA double-stranded breaks in human tumor cells deficient in BRCA1 or BRCA2. Cancer Res. 61:270-277.
65. Wang, Y., D. Cortez, P. Yazdi, N. Neff, S. J. Elledge, and J. Qin. 2000. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:927-939.
66. Willers, H., E. E. McCarthy, P. Hubbe, J. Dahm-Daphi, and S. N. Powell. 2001. Homologous recombination in extrachromosomal plasmid substrates is not suppressed by p53. Carcinogenesis 22:1757-1763.
67. Willers, H., E. E. McCarthy, B. Wu, H. Wunsch, W. Tang, D. G. Taghian, F. Xia, and S. N. Powell. 2000. Dissociation of p53-mediated suppression of homologous recombination from G1/S cell cycle checkpoint control. Oncogene 19: 632-639.
68. Wu, X., V. Ranganathan, D. S. Weisman, W. F. Heine, D. N. Ciccone, T. B. O'Neill, K. E. Crick, K. A. Pierce, W. S. Lane, G. Rathbum, D. M. Livingston, and D. T. Weaver. 2000. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405:477-482.
69. Wu, X. H., J. H. Petrini, W. F. Heine, D. T. Weaver, D. M. Livingston, and J. J. Chen. 2000. Independence of R/M/N focus formation and the presence of intact BRCA1. Science 289: 11a.
70. Xia, F., D. G. Taghian, J. S. DeFrank, Z. C. Zeng, H. Willers, G. Iliakis, and S. N. Powell. 2001. Deficiency of human BRCA2 leads to impaired homologous recombination but maintains normal nonhomologous end joining. Proc. Natl. Acad. Sci. USA 98:8644-8649.
71. Xu, B., S. Kim, and M. B. Kastan. 2001. Involvement of Brca1 in S-phase and G(2)-phase checkpoints after ionizing irradiation. Mol. Cell. Biol. 21:3445-3450.
72. Xu, B., S. T. Kim, D. S. Lim, and M. B. Kastan. 2002. Two molecularly distinct G(2)/M checkpoints are induced by ionizing irradiation. Mol. Cell. Biol. 22:1049-1059.
73. Yeo, T. C., D. Xia, S. Hassouneh, X. O. Yang, D. E. Sabath, K. Sperling, R. A. Gatti, P. Concannon, and D. M. Willerford. 2000. V(D)J rearrangement in Nijmegen breakage syndrome. Mol. Immunol. 37:1131-1139.
74. Zhong, Q., T. G. Boyer, P. L. Chen, and W. H. Lee. 2002. Deficient nonhomologous end-joining activity in cell-free extracts from Brca1-null fibroblasts. Cancer Res. 62:3966-3970.
75. Zhong, Q., C. F. Chen, P. L. Chen, and W. H. Lee. 2002. BRCA1 facilitates microhomology-mediated end joining of DNA double strand breaks. J. Biol. Chem. 277:28641-28647.
76. Zhong, Q., C. F. Chen, S. Li, Y. Chen, C. C. Wang, J. Xiao, P. L. Chen, Z. D. Sharp, and W. H. Lee. 1999. Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science 285:747-750.