Impaired DNA damage response in cells expressing an exon 11-deleted murine Brca1 variant that localizes to nuclear foci

Molecular and Cellular Biology

Volumn 21, Issue 12, 2001, Pages 4005-4015

  Huber, L Julie ^a   Yang, Thomas W ^a   Sarkisian, Christopher J ^a   Master, Stephen R ^a   Deng, Chu Xia ^b   Chodosh, Lewis A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL CYCLE; CELL NUCLEUS; DNA DAMAGE; EMBRYO DEVELOPMENT; GAMMA IRRADIATION; GENE DELETION; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN VARIANT;

ALTERNATIVE SPLICING; ANIMALS; ANTIBODIES, MONOCLONAL; BRCA1 PROTEIN; CELL CYCLE; CELL LINE; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; EXONS; GENES, BRCA1; HUMANS; MICE; PHOSPHORYLATION; RAD51 RECOMBINASE; RNA, MESSENGER; SEQUENCE DELETION; VARIATION (GENETICS);

ANIMALIA; MURINAE;

EID: 0035018530     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.21.12.4005-4015.2001     Document Type: Article

References (66)

1. Abbott, D. W., M. E. Thompson, C. Robinson-Benion, G. Tomlinson, R. A. Jensen, and J. T. Holt. 1999. BRCA1 expression restores radiation resistance in BRCA1-defective cancer cells through enhancement of transcription-coupled DNA repair. J. Biol. Chem. 274:18808-18812.
2. Anderson, S. F., B. P. Schlegel, T. Nakajima, E. S. Wolpin, and J. D. Parvin. 1998. BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat. Genet. 19:254-256.
3. Aprelikova, O., B. Fang, E. Meissner, S. Cotter, M. Campbell, A. Kuthiala, M. Bessho, R. Jensen, and E. Liu. 1999. BRCA1-associated growth arrest is RB-dependent. Proc. Natl. Acad. Sci. USA 96:11866-11871.
4. Bachelier, R., N. Dalla Venezia, S. Mazoyer, L. Frappart, G. M. Lenoir, and A. Vincent. 2000. Differential expression and subcellular localization of murine BRCA1 and BRCA1-delta 11 isoforms in murine and human cell lines. Int. J. Cancer 88:519-524.
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. Blasina, A., I. V. de Weyer, M. C. Laus, W. H. Luyten, A. E. Parker, and C. H. McGowan. 1999. A human homologue of the checkpoint kinase Cds1 directly inhibits Cdc25 phosphatase. Curr. Biol. 9:1-10.
7. 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.
8. Boyd, J. 1995. BRCA1: more than a hereditary breast cancer gene? Nat. Genet. 9:335-336.
9. Brown, A. L., C. H. Lee, J. K. Schwarz, N. Mitiku, H. Piwnica-Worms, and J. H. Chung. 1999. A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 96:3745-3750.
10. Chai, Y. L., J. Cui, N. Shao, E. Shyam, P. Reddy, and V. N. Rao. 1999. The second BRCT domain of BRCA1 proteins interacts with p53 and stimulates transcription from the p21WAF1/CIP1 promoter. Oncogene 18:263-268.
11. Chen, C.-F., S. Li, Y. Chen, P.-L. Chen, Z. Sharp, and W.-H. Lee. 1996. The nuclear localization sequences of the BRCA1 protein interact with the importin-α subunit of the nuclear transport signal receptor. J. Biol. Chem. 271:32863-32868.
12. Chen, J. 2000. Ataxia telangiectasia-related protein is involved in the phosphorylation of BRCA1 following deoxyribonucleic acid damage. Cancer Res. 60:5037-5039.
13. Chen, Y., A. Farmer, C.-F. Chen, D. Jones, P.-L. Chen, and W.-H. Lee. 1996. BRCA1 is a 220-kDa nuclear phosphoprotein that is expressed and phosphorylated in a cell cycle-dependent manner. Cancer Res. 56:3168-3172.
14. Chen, Y. M., C. F. Chen, D. J. Riley, D. C. Allred, P. L. Chen, D. Von Hoff, C. Osborne, and W.-H. Lee. 1995. Aberrant subcellular localization of BRCA1 in breast cancer. Science 270:789-791.
15. Christophe, D., C. Christophe-Hobertus, and B. Pichon. 2000. Nuclear targeting of proteins: how many different signals? Cell. Signal. 12:337-341.
16. Cortez, D., Y. Wang, J. Qin, and S. Elledge. 1999. Requirement of ATM-dependent phosphorylation of Brca1 in the DNA damage response to double-strand breaks. Science 286:1162-1166.
17. Cressman, V., D. Backlund, A. Avrutsdaya, S. Leadon, V. Godfrey, and B. Koller. 1999. Growth retardation, DNA repair defects, and lack of spermatogenesis in BRCA1-deficient mice. Mol. Cell. Biol. 19:7061-7075.
18. Easton, D., L. Steele, P. Fields, W. Ormiston, D. Averill, P. Daly, R. McManus, S. Neuhausen, D. Ford, R. Wooster, L. Cannon-Albright, M. Stratton, and D. Goldgar. 1997. Cancer risks in two large breast cancer families linked to BRCA2 on chromosome 13q12-13. Am. J. Hum. Genet. 61:120-128.
19. Flygare, J., F. Benson, and D. Hellgren. 1996. Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes, Biochim. Biophys. Acta 1312:231-236.
20. Gowen, L. C., B. L. Johnson, A. M. Latour, K. K. Sulik, and B. Koller. 1996. Brca1 deficiency results in early embryonic lethality characterized by neuro-epithelial abnormalities. Nat. Genet. 12:191-194.
21. Gudas, J., T. Li, H. Nguyen, D. Jensen, F. I. Rauscher, and K. Cowan. 1996. Cell cycle regulation of BRCA1 messenger RNA in human breast epithelial cells. Cell Growth Differ. 7:717-723.
22. Haile, D. T., and J. D. Parvin. 1999. Activation of transcription in vitro by the BRCA1 carboxyl-terminal domain. J. Biol. Chem. 274:2113-2117.
23. Hakem, R., J. de la Pompa, C. Sirard, R. Mo, M. Woo, A. Hakem, A. Wakeham, J. Potter, A. Reitmair, F. Billia, E. Firpo, C. Hui, J. Roberts, J. Rossant, and T. Mak. 1996. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85:1009-1024.
24. Harlow, E., and D. Lane. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
25. Hood, J. K., and P. A. Silver. 1999. In or out? Regulating nuclear transport. Curr. Opin. Cell Biol, 11:241-247.
26. Houvras, Y., M. Benezra, H. Zhang, J. J. Manfredi, B. L. Weber, and J. D. Licht. 2000. BRCA1 physically and functionally interacts with the ATF1 transcription factor. J. Biol. Chem. 275:36230-36237.
27. Jensen, D. E., M. Proctor, S. T. Marquis, H. P. Gardner, S. I. Ha, L. A. Chodosh, A. M. Ishov, N. Tommerup, H. Vissing, Y. Sekido, J. Minna, A. Borodovsky, D. C. Schultz, K. D. Wilkinson, G. G. Maul, N. Barlev, S. L. Berger, G. C. Prendergast, and F. J. Rauscher III. 1998. BAP1: a novel ubiquilin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16:1097-1112.
28. Jensen, R., M. Thompson, T. Jetton, C. Szabo, R. van der Meer, B. Helou, S. Tronick, D. Page, M.-C. King, and J. Holt. 1996. BRCA1 is secreted and exhibits properties of a granin. Nat. Genet. 12:303-308.
29. 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.
30. Li, S., P. L. Chen, T. Subramanian, G. Chinnadurai, G. Tomlinson, C. K. Osborne, Z. D. Sharp, and W. H. Lee. 1999. Binding of CtIP to the BRCT repeats of BRCA1 involved in the transcription regulation of p21 is disrupted upon DNA damage. J. Biol. Chem. 274:11334-11338.
31. Liu, C.-Y., A. Flesken-Nikitin, S. Li, Y. Zeng, and W.-H. Lee. 1996. Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes Dev. 10:1835-1843.
32. Ludwig, T., D. L. Chapman, V. E. Papaioannou, and A. Efstratiadis. 1997 Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev. 11:1226-1241.
33. Magdinier, F., N. Dalla Venezia, G. M. Lenoir, L. Frappart, and R. Dante. 1999. BRCA1 expression during prenatal development of the human mammary gland. Oncogene 18:4039-4043.
34. Matsuoka, S., M. Huang, and S. J. Elledge. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282:1893-1897.
35. Monteiro, A., A. August, and H. Hanafusa. 1996. Evidence for a transcriptional activation function of BRCA1 C-terminal region. Proc. Natl. Acad. Sci. USA 93:13595-13599.
36. Moroianu, J. 1999. Nuclear import and export pathways. J. Cell. Biochem. 32-33(Suppl):76-83.
37. Moynahan, M., J. Chiu, B. Koller, and M. Jasin. 1999. Brca1 controls homology-directed DNA repair. Mol. Cell 4:511-518.
38. Narod, S. A., D. Ford, P. Devilee, R. B. Barkardottir, H. T. Lynch, S. A. Smith, B. A. Ponder, B. L. Weber, J. E. Garber, J. M. Birch, et al. 1995. An evaluation of genetic heterogeneity in 145 breast-ovarian cancer families. Breast Cancer Linkage Consortium. Am. J. Hum. Genet. 56:254-264.
39. Neish, A. S., S. F. Anderson, B. P. Schlegel, W. Wei, and J. D. Parvin. 1998. Factors associated with the mammalian RNA polymerase II holoenzyme. Nucleic Acids Res. 26:847-853.
40. Ouchi, T., S. W. Lee, M. Ouchi, S. A. Aaronson, and C. M. Horvath. 2000. Collaboration of signal transducer and activator of transcription 1 (STAT1) and BRCA1 in differential regulation of IFN-gamma target genes. Proc. Natl. Acad. Sci. USA 97:5208-5213.
41. Paull, T. T., E. P. Rogakou, V. Vamazaki, C. U. Kirchgessner, M. Geliert, and W. M. Banner. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10:886-895.
42. Raderschall, E., E. I. Golub, and T. Haaf. 1999. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. USA 96:1921-1926.
43. Rajan, J. V., M. Wang, S. T. Marquis, and L. A. Chodosh. 1996. Brca2 is coordinately regulated with Brca1 during proliferation and differentiation in mammary epithelial cells. Proc. Natl. Acad. Sci. USA 93:13078-13083.
44. Ruffner, H., and I. Verma. 1997. BRCA1 is a cell cycle-regulated nuclear phosphoprotein. Proc. Natl. Acad. Sci. USA 94:7138-7143.
45. Schlegel, B. P., V. J. Green, J. A. Ladias, and J. D. Parvin. 2000. BRCA1 interaction with RNA polymerase II reveals a role for hRPB2 and hRPB10alpha in activated transcription. Proc. Natl. Acad. Sci. USA 97: 3148-3153.
46. Scully, R., S. Anderson, D. Chao, W. Wei, L. Ye, R. Young, D. Livingston, and J. Parvin. 1997. BRCA1 is a component of the RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. USA 94:5605-5610.
47. Scully, R., S. F. Anderson, D. M. Chao, W. Wei, L. Ye, R. A. Young, D. M. Livingston, and J. D. Parvin. 1997. BRCA1 is a component of the RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. USA 94:5605-5610.
48. Scully, R., J. Chen, R. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, and D. Livingston. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425-435.
49. Scully, R., J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, T. Ashley, and D. Livingston. 1997. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88:265-275.
50. Scully, R., S. Ganesan, M. Brown, J. A. De Caprio, S. Cannistra, J. Feunteun, S. Schnitt, and D. M. Livingston. 1996. Location of BRCA1 in human breast and ovarian cancer cells. Science 272:123-125.
51. Scully, R., S. Ganesan, K. Vlasakova, J. Chen, M. Socolovsky, and D. Livingston. 1999. Genetic analysis of BRCA1 function in a defined tumor cell line. Mol. Cell 4:1093-1099.
52. Shen, S. X., Z. Weaver, X. Xu, C. Li, M. Weinstein, L. Chen, X. Y. Guan, T. Ried, and C. X. Deng. 1998. A targeted disruption of the murine Brca1 gene causes gamma-irradiation hypersensitivity and genetic instability. Oncogene 17:3115-3124.
53. Tashiro, S., N. Kotomura, A. Shinohara, K. Tanaka, K. Ueda, and N. Kamada. 1996. S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12:2165-2170.
54. Thakur, S., H. Zhang, Y. Peng, H. Le, B. Carroll, T. Ward, J. Yao, L. Farid, F. Couch, R. Wilson, and B. Weber. 1997. Localization of BRCA1 and a splice variant identifies the nuclear localization signal. Mol. Cell. Biol. 17: 444-452.
55. Thomas, J., M. Smith, J. Tonkinson, B. Rubinfeld, and P. Polakis. 1997. Induction of phosphorylation on BRCA1 during the cell cycle and after DNA damage. Cell Growth Differ. 8:801-809.
56. 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.
57. Vaughn, J., P. Davis, M. Jarboe, G. Huper, A. Evans, R. Wiseman, A. Berchuck, J. Iglehart, P. Futreal, and J. Marks. 1996. BRCA1 expression is induced before DNA synthesis in both normal and tumor-derived breast cells. Cell Growth Differ. 7:711-715.
58. Wilson, C, M. Payton, G. Elliott, F. Buass, E. Cajulis, D. Grosshans, L. Ramos, D. Reese, D. Slamon, and F. Calzone. 1997. Differential subcellular localization, expression and biological toxicity of BRCA1 and the splice variant BRCA1-delta11b. Oncogene 14:1-16.
59. Wu, L. C., Z. W. Wang, J. T. Tsan, M. A. Spillman, A. Phung, X. L. Xu, M. C. Yang, L. Y. Hwang, A. M. Bowcock, and R. Baer. 1996. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat. Genet. 14:430-440.
60. Xu, X., K. U. Wagner, D. Larson, Z. Weaver, C. Li, T. Ried, L. Hennighausen, A. Wynshaw-Boris, and C. X. Deng. 1999. Conditional mutation of Brca1 in mammary epithelial cells results in blunted ductal morphogenesis and tumour formation. Nat. Genet. 22:37-43.
61. Xu, X., Z. Weaver, S. P. Linke, C. Li, J. Gotay, X. W. Wang, C. C. Harris, T. Ried, and C. X. Deng. 1999. Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-delicient cells. Mol. Cell 3:389-395.
62. Yamamoto, A., T. Taki, H. Yagi, T. Habu, K. Yoshida, Y. Yoshimura, K. Yamamoto, A. Matsushiro, Y. Nishimune, and T. Morita. 1996. Cell cycle-dependent expression of the mouse Rad51 gene in proliferating cells. Mol. Gen. Genet. 251:1-12.
63. Yu, X., L. C. Wu, A. M. Bowcock, A. Aronheim, and R. Baer. 1998. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem. 273:25388-25392.
64. Zhang, H., K. Somasundaram, Y. Peng, H. Tian, D. Bi, B. L. Weber, and W. S. El-Deiry. 1998. BRCA1 physically associates with p53 and stimulates its transcriptional activity. Oncogene 16:1713-1721.
65. Zheng, L., H. Pan, S. Li, A. Flesken-Nikitin, P. Chen, T. G. Boyer, and W. Lee. 2000. Sequence-specific transcriptional corepressor function for BRCA1 through a novel zinc finger protein, ZBRK1. Mol. Cell 6:757-768.
66. 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.