The carboxyl-terminal of BRCA1 is required for subnuclear assembly of RAD51 after treatment with cisplatin but not ionizing radiation in human breast and ovarian cancer cells

Biochemical and Biophysical Research Communications

Volumn 336, Issue 3, 2005, Pages 952-960

  Zhou, Chenyi ^a   Huang, Peng ^a   Liu, Jinsong ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Radiation; BRCA1; Breast and ovarian cancer; Cisplatin; Rad51

Indexed keywords

BRCA1 PROTEIN; CISPLATIN; RAD51 PROTEIN; RETROVIRUS VECTOR; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CANCER RADIOTHERAPY; CARBOXY TERMINAL SEQUENCE; CELL STRAIN; CONTROLLED STUDY; DNA DAMAGE; FEMALE; HUMAN; HUMAN CELL; INTRANUCLEAR SPACE; IONIZING RADIATION; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

ANTINEOPLASTIC AGENTS; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CISPLATIN; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, BRCA1; HUMANS; OVARIAN NEOPLASMS; PHOSPHORYLATION; RAD51 RECOMBINASE; RADIATION, IONIZING; RNA INTERFERENCE; SEQUENCE DELETION;

EID: 25144498670     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.08.197     Document Type: Article

References (52)

1. J.M. Hall, M.K. Lee, B. Newman, J.E. Morrow, L.A. Anderson, B. Huey, and M.C. King Linkage of early-onset familial breast cancer to chromosome 17q21 Science 250 1990 1684 1689
2. Y. Miki, J. Swensen, D. Shattuck-Eidens, P.A. Futreal, K. Harshman, S. Tavtigian, Q. Liu, C. Cochran, L.M. Bennett, and W. Ding A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1 Science 266 1994 66 71
3. A.G. Knudson Jr., H.W. Hethcote, and B.W. Brown Mutation and childhood cancer: a probabilistic model for the incidence of retinoblastoma Proc. Natl. Acad. Sci. USA 72 1975 5116 5120
4. I. Callebaut, and J.P. Mornon From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair FEBS Lett. 400 1997 25 30
5. P. Bork, K. Hofmann, P. Bucher, A.F. Neuwald, S.F. Altschul, and E.V. Koonin A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins FASEB J. 11 1997 68 76
6. R. Scully, J. Chen, R.L. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, and D.M. Livingston Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage Cell 90 1997 425 435
7. R. Scully, J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, T. Ashley, and D.M. Livingston Association of BRCA1 with Rad51 in mitotic and meiotic cells Cell 88 1997 265 275
8. J.N. Snouwaert, L.C. Gowen, A.M. Latour, A.R. Mohn, A. Xiao, L. DiBiase, and B.H. Koller 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 1999 7900 7907
9. K. Somasundaram, H. Zhang, Y.X. Zeng, Y. Houvras, Y. Peng, G.S. Wu, J.D. Licht, B.L. Weber, and W.S. El-Deiry Arrest of the cell cycle by the tumour-suppressor BRCA1 requires the CDK-inhibitor p21WAF1/CiP1 Nature 389 1997 187 190
10. M.E. Moynahan, J.W. Chiu, B.H. Koller, and M. Jasin Brca1 controls homology-directed DNA repair Mol. Cell 4 1999 511 518
11. A.N. Monteiro, A. August, and H. Hanafusa Evidence for a transcriptional activation function of BRCA1 C-terminal region Proc. Natl. Acad. Sci. USA 93 1996 13595 13599
12. J.S. Larson, J.L. Tonkinson, and M.T. Lai A BRCA1 mutant alters G2-M cell cycle control in human mammary epithelial cells Cancer Res. 57 1997 3351 3355
13. D.P. Harkin, J.M. Bean, D. Miklos, Y.H. Song, V.B. Truong, C. Englert, F.C. Christians, L.W. Ellisen, S. Maheswaran, J.D. Oliner, and D.A. Haber Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1 Cell 97 1999 575 586
14. L.C. Gowen, A.V. Avrutskaya, A.M. Latour, B.H. Koller, and S.A. Leadon BRCA1 required for transcription-coupled repair of oxidative DNA damage Science 281 1998 1009 1012
15. Y. Wang, D. Cortez, P. Yazdi, N. Neff, S.J. Elledge, and J. Qin BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures Genes Dev. 14 2000 927 939
16. Q. Zhong, C.F. Chen, S. Li, Y. Chen, C.C. Wang, J. Xiao, P.L. Chen, Z.D. Sharp, and W.H. Lee Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response [see comments] Science 285 1999 747 750
17. M.E. Moynahan, T.Y. Cui, and M. Jasin Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation Cancer Res. 61 2001 4842 4850
18. D.W. Abbott, M.E. Thompson, C. Robinson-Benion, G. Tomlinson, R.A. Jensen, and J.T. Holt BRCA1 expression restores radiation resistance in BRCA1-defective cancer cells through enhancement of transcription-coupled DNA repair J. Biol. Chem. 274 1999 18808 18812
19. I. Garcia-Higuera, T. Taniguchi, S. Ganesan, M.S. Meyn, C. Timmers, J. Hejna, M. Grompe, and A.D. D'Andrea Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway Mol. Cell 7 2 2001 249 262
20. I.A. Manke, D.M. Lowery, A. Nguyen, and M.B. Yaffe BRCT repeats as phosphopeptide-binding modules involved in protein targeting Science 302 2003 636 639
21. X. Yu, C.C. Chini, M. He, G. Mer, and J. Chen The BRCT domain is a phospho-protein binding domain Science 302 2003 639 642
22. R. Hakem, J.L. de la Pompa, C. Sirard, R. Mo, M. Woo, A. Hakem, A. Wakeham, J. Potter, A. Reitmair, F. Billia, E. Firpo, C.C. Hui, J. Roberts, J. Rossant, and T.W. Mak The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse Cell 85 1996 1009 1023
23. P. Baumann, F.E. Benson, and S.C. West Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro Cell 87 1996 757 766
24. T. Haaf, E.I. Golub, G. Reddy, C.M. Radding, and D.C. Ward Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes Proc. Natl. Acad. Sci. USA 92 1995 2298 2302
25. J.J. Chen, D. Silver, S. Cantor, D.M. Livingston, and R. Scully BRCA1, BRCA2, and Rad51 operate in a common DNA damage response pathway Cancer Res. 59 1999 1752s 1756s
26. S.S. Yuan, S.Y. Lee, G. Chen, M. Song, G.E. Tomlinson, and E.Y. Lee BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo Cancer Res. 59 15 1999 3547 3551
27. A. Bhattacharyya, U.S. Ear, B.H. Koller, R.R. Weichselbaum, and D.K. Bishop 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 2000 23899 23903
28. S.L. Gasior, A.K. Wong, Y. Kora, A. Shinohara, and D.K. Bishop Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes Genes Dev. 12 1998 2208 2221
29. D.K. Bishop, U. Ear, A. Bhattacharyya, C. Calderone, M. Beckett, R.R. Weichselbaum, and A. Shinohara Xrcc3 is required for assembly of Rad51 complexes in vivo J. Biol. Chem. 273 1998 21482 21488
30. T. Tsuzuki, Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, M. Sekiguchi, A. Matsushiro, Y. Yoshimura, and T. Morita Targeted disruption of the Rad51 gene leads to lethality in embryonic mice Proc. Natl. Acad. Sci. USA 93 1996 6236 6240
31. D.S. Lim, and P. Hasty A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53 Mol. Cell. Biol. 16 1996 7133 7143
32. K. Wozniak, and J. Blasiak Recognition and repair of DNA-cisplatin adducts Acta. Biochim. Pol. 49 2002 583 596
33. M. Kartalou, and J.M. Essigmann Mechanisms of resistance to cisplatin Mutat. Res. 478 2001 23 43
34. Z.H. Siddik Cisplatin: mode of cytotoxic action and molecular basis of resistance Oncogene 22 2003 7265 7279
35. S.J. Araâujo, F. Tirode, F. Coin, H. Pospiech, J.E. Syvèaoja, M. Stucki, U. Hèubscher, J.M. Egly, and R.D. Wood Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK Genes Dev. 14 3 2000 349 359
36. J. de Boer, and J.H. Hoeijmakers Nucleotide excision repair and human syndromes Carcinogenesis 21 3 2000 453 460
37. W.L. de Laat, N.G. Jaspers, and J.H. Hoeijmakers Molecular mechanism of nucleotide excision repair Genes Dev. 13 7 1999 768 785
38. Z.Z. Zdraveski, J.A. Mello, M.G. Marinus, and J.M. Essigmann Multiple pathways of recombination define cellular responses to cisplatin Chem. Biol. 7 1 2000 39 50
39. S. Hussain, J.B. Wilson, A.L. Medhurst, J. Hejna, E. Witt, S. Ananth, A. Davies, J.Y. Masson, R. Moses, S.C. West, J.P. de Winter, A. Ashworth, N.J. Jones, and C.G. Mathew Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways Hum. Mol. Genet. 13 2004 1241 1248
40. C. Zhou, J.L. Smith, and J. Liu Role of BRCA1 in cellular resistance to paclitaxel and ionizing radiation in an ovarian cancer cell line carrying a defective BRCA1 Oncogene 22 2003 2396 2404
41. C.F. Chen, S. Li, Y. Chen, P.L. Chen, Z.D. Sharp, and W.H. Lee The nuclear localization sequences of the BRCA1 protein interact with the importin-alpha subunit of the nuclear transport signal receptor J. Biol. Chem. 271 1996 32863 32868
42. G. Yang, J.A. Thompson, B. Fang, and J. Liu Silencing of H-ras gene expression by retrovirus-mediated siRNA decreases transformation efficiency and tumor growth in a model of human ovarian cancer Oncogene 22 2003 5694 5701
43. G. Yang, K.Q. Cai, J.A. Thompson-Lanza, R.C. Bast Jr., and J. Liu Inhibition of breast and ovarian tumor growth through multiple signaling pathways by using retrovirus-mediated small interfering RNA against Her-2/neu gene expression J. Biol. Chem. 279 2004 4339 4345
44. S. Corde, J. Balosso, H. Elleaume, M. Renier, A. Joubert, M.C. Biston, J.F. Adam, A.M. Charvet, T. Brochard, J.F. Le Bas, F. Estáeve, and N. Foray Synchrotron photoactivation of cisplatin elicits an extra number of DNA breaks that stimulate RAD51-mediated repair pathways Cancer Res. 63 12 2003 3221 3227
45. C. Spiro, and C.T. McMurray Nuclease-deficient FEN-1 blocks Rad51/BRCA1-mediated repair and causes trinucleotide repeat instability Mol. Cell. Biol. 23 17 2003 6063 6074
46. N.G. Howlett, T. Taniguchi, S. Olson, B. Cox, Q. Waisfisz, C. De Die-Smulders, N. Persky, M. Grompe, H. Joenje, G. Pals, H. Ikeda, E.A. Fox, and A.D. D'Andrea Biallelic inactivation of BRCA2 in Fanconi anemia Science 297 2002 606 609
47. D. Cortez, Y. Wang, J. Qin, and S.J. Elledge Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks Science 286 1999 1162 1166
48. Y. Chen, A.A. Farmer, C.F. Chen, D.C. Jones, P.L. Chen, W.H. Lee, BRCA1 is a 220-kDa nuclear phosphoprotein that is expressed and phosphorylated in a cell cycle-dependent manner [erratum appears in Cancer Res. 56 (17) (1996) 4074], Cancer Res. 56 (1996) 3168-3172.
49. R. Scully, S. Ganesan, K. Vlasakova, J. Chen, M. Socolovsky, and D.M. Livingston Genetic analysis of BRCA1 function in a defined tumor cell line Mol. Cell 4 1999 1093 1099
50. R.S. Tibbetts, D. Cortez, K.M. Brumbaugh, R. Scully, D. Livingston, S.J. Elledge, and R.T. Abraham Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress Genes Dev. 14 2000 2989 3002
51. J.S. Lee, K.M. Collins, A.L. Brown, C.H. Lee, and J.H. Chung hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response Nature 404 2000 201 204
52. P. Pichierri, and F. Rosselli The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways EMBO J. 23 2004 1178 1187