BARD1 Participates with BRCA1 in Homology-Directed Repair of Chromosome Breaks

Molecular and Cellular Biology

Volumn 23, Issue 21, 2003, Pages 7926-7936

  Westermark, Ulrica K ^a   Reyngold, Marsha ^b   Olshen, Adam B ^a   Baer, Richard ^b   Jasin, Maria ^a   Moynahan, Mary Ellen ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; CELL PROTEIN; DOUBLE STRANDED DNA; PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER INHIBITION; CHROMOSOME BREAKAGE; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; EXON; GENE DELETION; GENE FUNCTION; HOMOLOGOUS RECOMBINATION; INTRACELLULAR TRANSPORT; MOLECULAR CLONING; MOLECULAR STABILITY; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RNA SPLICING; TUMOR SUPPRESSOR GENE; WILD TYPE;

ANIMALS; BRCA1 PROTEIN; CARRIER PROTEINS; CELL LINE; CHROMOSOMES; DNA DAMAGE; DNA REPAIR; GENES, REPORTER; HUMANS; MACROMOLECULAR SUBSTANCES; MICE; MICE, KNOCKOUT; MITOMYCIN; NUCLEIC ACID SYNTHESIS INHIBITORS; PEPTIDES; PROTEIN BINDING; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

ANIMALIA;

EID: 0142123148     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.21.7926-7936.2003     Document Type: Article

References (61)

1. Ayi, T. C., J. T. Tsan, L. Y. Hwang, A. M. Bowcock, and R. Baer. 1998. Conservation of function and primary structure in the Brca1-associated ring domain (Bard1) protein. Oncogene 17:2143-2148.
2. Baer, R., and T. Ludwig. 2002. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 12:86-91.
3. 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.
4. Brodie, S. G., X. Xu, W. Qiao, W. M. Li, L. Cao, and C. X. Deng. 2001. Multiple genetic changes are associated with mammary tumorigenesis in Brca1 conditional knockout mice. Oncogene 20:7514-7523.
5. Brzovic, P. S., J. E. Meza, M. C. King, and R. E. Klevit. 2001. BRCA1 RING domain cancer-predisposing mutations. Structural consequences and effects on protein-protein interactions. J. Biol. Chem. 276:41399-41406.
6. Brzovic, P. S., P. Rajagopal, D. W. Hoyt, M. C. King, and R. E. Klevit. 2001. Structure of a BRCA1-BARD1 heterodimeric RING-RING complex. Nat. Struct. Biol. 8:833-837.
7. Castilla, L. H., F. J. Couch, M. R. Erdos, K. F. Hoskins, K. Calzone, J. E. Garber, J. Boyd, M. B. Lubin, M. L. Deshano, L. C. Brody, et al. 1994. Mutations in the BRCA1 gene in families with early-onset breast and ovarian cancer. Nat. Genet. 8:387-391.
8. Chen, A., F. E. Kleiman, J. L. Manley, T. Ouchi, and Z. Q. Pan. 2002. Autoubiquitination of the BRCA1*BARD1 RING ubiquitin ligase. J. Biol. Chem. 277:22085-22092.
9. Deng, C. X., and S. G. Brodie. 2001. Knockout mouse models and mammary tumorigenesis. Semin. Cancer Biol. 11:387-394.
10. Fabbro, M., J. A. Rodriguez, R. Baer, and B. R. Henderson. 2002. BARD1 induces BRCA1 intranuclear foci formation by increasing RING-dependent BRCA1 nuclear import and inhibiting BRCA1 nuclear export. J. Biol. Chem. 277:21315-21324.
11. Friedberg, E. C., and L. B. Meira. 2003. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage, version 5. DNA Repair 2:501-530.
12. Friedman, L. S., E. A. Ostermeyer, C. I. Szabo, P. Dowd, E. D. Lynch, S. E. Rowell, and M. C. King. 1994. Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families. Nat. Genet. 8:399-404.
13. Ghimenti, C., E. Sensi, S. Presciuttini, I. M. Brunetti, P. Conte, G. Bevilacqua, and M. A. Caligo. 2002. Germline mutations of the BRCA1-associated ring domain (BARD1) gene in breast and breast/ovarian families negative for BRCA1 and BRCA2 alterations. Genes Chromosomes Cancer 33:235-242.
14. Gowen, L. C., B. L. Johnson, A. M. Latour, K. K. Sulik, and B. H. Koller. 1996. Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nat. Genet. 12:191-194.
15. Hashizume, R., M. Fukuda, I. Maeda, H. Nishikawa, D. Oyake, Y. Yabuki, H. Ogata, and T. Ohta. 2001. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276:14537-14540.
16. Huber, L. J., T. W. Yang, C. J. Sarkisian, S. R. Master, C. X. Deng, and L. A. Chodosh. 2001. Impaired DNA damage response in cells expressing an exon 11-deleted murine Brca1 variant that localizes to nuclear foci. Mol. Cell. Biol. 21:4005-4015.
17. Irminger-Finger, I., W. C. Leung, J. Li, M. Dubois-Dauphin, J. Harb, A. Feki, C. E. Jefford, J. V. Soriano, M. Jaconi, R. Montesano, and K. H. Krause. 2001. Identification of BARD1 as mediator between proapoptotic stress and p53-dependent apoptosis. Mol. Cell 8:1255-1266.
18. Irminger-Finger, I., J. V. Soriano, G. Vaudan, R. Montesano, and A. P. Sappino. 1998. In vitro repression of Brca1-associated RING domain gene, Bard1, induces phenotypic changes in mammary epithelial cells. J. Cell Biol. 143:1329-1339.
19. Jasin, M. 2002. Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene 21:8981-8993.
20. 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 ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16:1097-1112.
21. Jin, Y., X. L. Xu, M. C. W. Yang, F. L. Wei, T. C. Ayi, A. M. Bowcock, and R. Baer. 1997. Cell cycle-dependent colocalization of Bard1 and Brca1 proteins in discrete nuclear domains. Proc. Natl. Acad. Sci. USA 94:12075-12080.
22. Joukov, V., J. Chen, E. A. Fox, J. B. Green, and D. M. Livingston. 2001. Functional communication between endogenous BRCA1 and its partner, BARD1, during Xenopus laevis development. Proc. Natl. Acad. Sci. USA 98:12078-12083.
23. Kentsis, A., R. E. Gordon, and K. L. Borden. 2002. Control of biochemical reactions through supramolecular RING domain self-assembly. Proc. Natl. Acad. Sci. USA 99:15404-15409.
24. Kleiman, F. E., and J. L. Manley. 1999. Functional interaction of BRCA1-associated BARD1 with polyadenylation factor CstF-50. Science 285:1576-1579.
25. Lorick, K. L., J. P. Jensen, S. Fang, A. M. Ong, S. Hatakeyama, and A. M. Weissman. 1999. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96:11364-11369.
26. Mallery, D. L., C. J. Vandenberg, and K. Hiom. 2002. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 21:6755-6762.
27. Marians, K. J. 2000. Replication and recombination intersect. Curr. Opin. Genet. Dev. 10:151-156.
28. McCarthy, E. E., J. T. Celebi, R. Baer, and T. Ludwig. 2003. Loss of Bard1, the heterodimeric partner of the Brca1 tumor suppressor, results in early embryonic lethality and chromosomal instability. Mol. Cell. Biol. 23:5056-5063.
29. Meza, J. E., P. S. Brzovic, M. C. King, and R. E. Klevit. 1999. Mapping the functional domains of BRCA1: interaction of the ring finger domains of BRCA1 and BARD1. J. Biol. Chem. 274:5659-5665.
30. Miki, Y., J. Swensen, D. Shattuck-Eidens, P. A. Futreal, K. Harshman, S. Tavtigian, Q. Liu, C. Cochran, L. M. Bennett, W. Ding, R. Bell, J. Rosenthal, C. Hussey, T. Tran, M. McClure, C. Frye, T. Hattier, R. Phelps, D. Haugren-Strano, H. Katcher, K. Yakumo, Z. Gholami, D. Shaffer, S. Stone, S. Bayer, C. Wray, R. Bogden, P. Dayanath, J. Ward, P. Tonin, S. Narod, P. Bristow, F. Norris, L. Helvering, P. Morrison, P. Rostecl, M. Lai, C. Barrett, C. Lewis, S. Neuhasen, L. Cannon-Albright, D. Goldgar, R. Wiseman, A. Kamb, and M. Skolnick. 1994. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266:66-71.
31. Moynahan, M. E. 2002. The cancer connection: BRCA1 and BRCA2 tumor suppression in mice and humans. Oncogene 21:8994-9007.
32. Moynahan, M. E., J. W. Chiu, B. H. Koller, and M. Jasin. 1999. Brca1 controls homology-directed DNA repair. Mol. Cell 4:511-518.
33. 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.
34. Moynahan, M. E., A. J. Pierce, and M. Jasin. 2001. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 7:263-272.
35. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
36. Pickart, C. M. 2001. Ubiquitin enters the new millennium. Mol. Cell 8:499-504.
37. Pierce, A. J., P. Hu, M. Han, N. Ellis, and M. Jasin. 2001. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15:3237-3242.
38. 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.
39. 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.
40. Richardson, C., M. E. Moynahan, and M. Jasin. 1998. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:3831-3842.
41. Rodriguez, J. A., and B. R. Henderson. 2000. Identification of a functional nuclear export sequence in BRCA1. J. Biol. Chem. 275:38589-38596.
42. Ruffner, H., C. A. Joazeiro, D. Hemmati, T. Hunter, and I. M. Verma. 2001. Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc. Natl. Acad. Sci. USA 98:5134-5139.
43. Saurin, A. J., K. L. Borden, M. N. Boddy, and P. S. Freemont. 1996. Does this have a familiar RING? Trends Biochem. Sci. 21:208-214.
44. Scully, R., J. Chen, R. L. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, and D. M. Livingston. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425-435.
45. 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.
46. Scully, R., and D. M. Livingston. 2000. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature 408:429-432.
47. Sharan, S. K., M. Wims, and A. Bradley. 1995. Murine Brca1: sequence and significance for human missense mutations. Hum. Mol. Genet. 4:2275-2278.
48. 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.
49. Sonoda, E., M. S. Sasaki, C. Morrison, Y. Yamaguchi-Iwai, M. Takata, and S. Takeda. 1999. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19:5166-5169.
50. Stark, J. M., P. Hu, A. J. Pierce, M. E. Moynahan, N. Ellis, and M. Jasin. 2002. ATP hydrolysis by mammalian RAD51 has a key role during homology-directed DNA repair. J. Biol. Chem. 277:20185-20194.
51. Stewart, G. S., B. Wang, C. R. Bignell, A. M. Taylor, and S. J. Elledge. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961-966.
52. Thai, T. H., F. H. Du, J. T. Tsan, Y. Jin, A. Phung, M. A. Spillman, H. F. Massa, C. Y. Muller, R. Ashfaq, J. M. Mathis, D. S. Miller, B. J. Trask, R. Baer, and A. M. Bowcock. 1998. Mutations in the Brca1-associated ring domain (Bard1) gene in primary breast, ovarian and uterine cancers. Hum. Mol. Genet. 7:195-202.
53. Thakur, S., H. B. Zhang, Y. Peng, H. Le, B. Carroll, T. Ward, J. Yao, L. M. Farid, F. J. Couch, R. B. Wilson, and B. L. Weber. 1997. Localization of BRCA1 and a splice variant identifies the nuclear localization signal. Mol. Cell. Biol. 17:444-452.
54. Tsan, J. T., Z. Wang, J. Y., L. Y. Hwang, R. O. Bash, and R. Baer. 1997. Mammalian cells as hosts for two-hybrid studies of protein-protein interaction, p. 217-232. In P. L. Bartel and S. Fields (ed.), The yeast two-hybrid system. Oxford University Press, Oxford, England.
55. Tutt, A., D. Bertwistle, J. Valentine, A. Gabriel, S. Swift, G. Ross, C. Griffin, J. Thacker, and A. Ashworth. 2001. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20:4704-4716.
56. Wang, H., N. Shao, Q. M. Ding, J. Cui, E. S. Reddy, and V. N. Rao. 1997. BRCA1 proteins are transported to the nucleus in the absence of serum and splice variants BRCA1a, BRCA1b are tyrosine phosphoproteins that associate with E2F, cyclins and cyclin dependent kinases. Oncogene 15:143-157.
57. 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.
58. Wilson, C. A., M. N. Payton, G. S. Elliott, F. W. Buaas, E. E. Cajulis, D. Grosshans, L. Ramos, D. M. Reese, D. J. Slamon, and F. J. Calzone. 1997. Differential subcellular localization, expression and biological toxicity of BRCA1 and the splice variant BRCA1-Δ11b. 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. Nature Genetics 14:430-440.
60. Xia, Y., G. Pao, H. W. Chen, I. M. Verma, and T. Hunter. 2003. Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J. Biol. Chem. 278:5255-5263.
61. Yu, X., and R. Baer. 2000. Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J. Biol. Chem. 275:18541-18549.