BRCA1 and BRCA2 in breast cancer predisposition and recombination control

Journal of Mammary Gland Biology and Neoplasia

Volumn 9, Issue 3, 2004, Pages 237-246

  Scully, Ralph ^a   Xie, Anyong ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHECKPOINT KINASE 2; DNA POLYMERASE; HISTONE H2A; HYDROXYUREA; MRE11 PROTEIN; PROTEIN UBC9; RAD50 PROTEIN; RAD51 PROTEIN; RAD52 PROTEIN; RAD54 PROTEIN; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANTINEOPLASTIC ACTIVITY; BREAST CANCER; BREAST CARCINOGENESIS; CANCER INHIBITION; CANCER SUSCEPTIBILITY; CHROMATIN; CHROMOSOME ABERRATION; DNA DAMAGE; DNA SYNTHESIS; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC SUSCEPTIBILITY; HETEROZYGOSITY LOSS; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; NONHUMAN; OPEN READING FRAME; OVARY CANCER; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; TISSUE SPECIFICITY;

BREAST NEOPLASMS; DNA; FEMALE; GENES, BRCA1; GENES, BRCA2; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MUTATION; OVARIAN NEOPLASMS; RECOMBINATION, GENETIC;

EID: 9144260592     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:JOMG.0000048771.93906.3e     Document Type: Review

References (121)

1. Y. Miki, J. Swensen, D. Shattuck-Eidens, P. A. Futreal, K. Harshman, S. Tavtigian, et al. (1994). A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266 5182):66-71.
2. R. Wooster, G. Bignell, J. Lancaster, S. Swift, S. Seal, J. Mangion, et al. (1995). Identification of the breast cancer susceptibility gene BRCA2. Nature 378(6559):789-792.
3. A. G. Knudson, Jr. (1971). Mutation and cancer: Statistical study of retinoblastoma. Proc. Natl. Acad. Sci. U.S.A. 68(4 ):820-823.
4. N. G. Howlett, T. Taniguchi, S. Olson, B. Cox, Q. Waisfisz, C. De Die-Smulders, et al. (2002). Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297(5581):606-609.
5. H. Meijers-Heijboer, A. van den Ouweland, J. Klijn, M. Wasielewski, A. de Snoo, R. Oldenburg, et al. (2002). Low-penetrance susceptibility to breast cancer due to CHEK2(*)1100delC in noncarriers of BRCA1 or BRCA2 mutations. Nat. Genet. 31(1):55-59.
6. J. E. Garber, A. M. Goldstein, A. F. Kantor, M. G. Dreyfus, J. F. Fraumeni, Jr., and F. P. Li (1991). Follow-up study of twenty-four families with Li-Fraumeni syndrome. Cancer Res. 51 22):6094-6097.
7. R. Wooster and B. L. Weber (2003). Breast and ovarian cancer. N. Engl. J. Med. 348(23):2339-2347.
8. R. Hakem, J. L. de la Pompa, C. Sirard, R. Mo, M. Woo, A. Hakem, et al. (1996). The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85 7):1009-1023.
9. S. K. Sharan, M. Morimatsu, U. Albrecht, D. S. Lim, E. Regel, C. Dinh, et al. (1997). Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386 6627):804-810.
10. T. Ludwig, 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 10):1226-1241.
11. A. Suzuki, J. I. de la Pompa, R. Hakem, A. Elia, R. Yoshida, R. Mo, et al. (1997). Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev. 11(10):1242-1252.
12. R. Hakem, J. I. de la Pompa, A. Elia, J. Potter, and T. W. Mak (1997). Partial rescue of Brca1 (5-6) early embryonic lethality by p53 or p21 null mutation. Nat. Genet. 16(3):298-302.
13. R. Scully, J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, et al. (1997). Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88(2):265-275.
14. Q. Zhong, C. F. Chen, S. Li, Y. Chen, C. C. Wang, J. Xiao, et al. (1999). Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science 285(5428):747-750.
15. S. C. West (2003). Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4(6):435-445.
16. K. J. Patel, V. P. Vu, H. Lee, A. Corcoran, F. C. Thistlethwaite, M. J. Evans, et al. (1998). Involvement of Brca2 in DNA repair. Mol. Cell 1(3):347-357.
17. S. X. Shen, Z. Weaver, X. Xu, C. Li, M. Weinstein, L. Chen, et al. (1998). A targeted disruption of the murine Brca1 gene causes gamma-irradiation hypersensitivity and genetic instability. Oncogene 17(24):3115-3124.
18. F. Connor, D. Bertwistle, P. J. Mee, G. M. Ross, S. Swift, E. Grigorieva, et al. (1997). Tumorigenesis and a DNA repair defect in mice with a truncating Brca2 mutation. Nat. Genet. 17(4 ):423-430.
19. A. Tutt, A. Gabriel, D. Bertwistle, F. Connor, H. Paterson, J. Peacock, et al. (1999). Absence of Brca2 causes genome instability by chromosome breakage and loss associated with centrosome amplification. Curr. Biol. 9(19):1107-1110.
20. R. Scully and D. M. Livingston (2000). In search of the tumor suppressor functions of BRCA1 and BRCA2. Nature 408:429-432.
21. A. R. Venkitaraman (2002). Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108(2):171-182.
22. D. O. Ferguson and F. W. Alt (2001). DNA double strand break repair and chromosomal translocation: Lessons from animal models. Oncogene 20(40):5572-5579.
23. V. P. Yu, M. Koehler, C. Steinlein, M. Schmid, L. A. Hanakahi, A. J. van Gool, et al. (2000). Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev. 14(11):1400-1406.
24. R. Scully (2000). Role of BRCA gene dysfunction in breast and ovarian cancer predisposition. Breast Cancer Res. 2:324-330.
25. S. J. Elledge and A. Amon (2002). The BRCA1 suppressor hypothesis: An explanation for the tissue-specific tumor development in BRCA1 patients. Cancer Cell 1(2):129-132.
26. A. N. Monteiro (2003). BRCA1: The enigma of tissue-specific tumor development. Trends Genet. 19(6):312-315.
27. X. Xu, Z. Weaver, S. P. Linke, C. Li, J. Gotay, X. W. Wang, et al. (1999). Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell 3(3):389-395.
28. B. Xu, 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(10):3445-3450.
29. M. Kraakman-van der Zwet, W. J. Overkamp, R. E. van Lange, J. Essers, A. van Duijn-Goedhart, I. Wiggers, et al. (2002). Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol. Cell Biol. 22(2):669-679.
30. A. N. Monteiro (2000). BRCA1: Exploring the links to transcription. Trends Biochem. Sci. 25(10):469-474.
31. J. D. Parvin (2001). BRCA1 at a branch point. Proc. Natl. Acad. Sci. U.S.A. 98(11):5952-5954.
32. L. M. Starita and J. D. Parvin (2003). The multiple nuclear functions of BRCA1: Transcription, ubiquitination and DNA repair. Curr. Opin. Cell Biol. 15(3):345-350.
33. L. Hughes-Davies, D. Huntsman, M. Ruas, F. Fuks, J. Bye, S. F. Chin, et al. (2003). EMSY links the BRCA2 pathway to sporadic breast and ovarian cancer. Cell 115(5):523-535.
34. J. Milner, B. Ponder, L. Hughes-Davies, M. Seltmann, and T. Kouzarides (1997). Transcriptional activation functions in BRCA2. Nature 386(6627):772-773.
35. F. Fuks, J. Milner, and T. Kouzarides (1998). BRCA2 associates with acetyltransferase activity when bound to P/CAF. Oncogene 17 19):2531-2534.
36. X. Yu, 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(39):25388-25392.
37. S. Li, P. L. Chen, T. Subramanian, G. Chinnadurai, G. Tomlinson, C. K. Osborne, et al. (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(16):11334-11338.
38. L. Zheng, H. Pan, S. Li, A. Flesken-Nikitin, P. Chen, T. G. Boyer, et al. (2000). Sequence-specific transcriptional core-pressor function for brca1 through a novel zinc finger protein, ZBRK1. Mol. Cell 6(4):757-768.
39. S. Ganesan, D. P. Silver, R. A. Greenberg, D. Avni, R. Drapkin, A. Miron, et al. (2002). BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111(3):393-405.
40. F. E. Kleiman and J. L. Manley. (2001). The BARD1-CstF-50 interaction links mRNA 3′ end formation to DNA damage and tumor suppression. Cell 104(5):743-753.
41. F. E. Kleiman and J. L. Manley (1999). Functional interaction of BRCA1-associated BARD1 with polyadenylation factor CstF-50. Science 285(5433):1576-1579.
42. R. Scully, 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(6):1093-1099.
43. M. E. Moynahan, 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 12):4842-4850.
44. M. E. Moynahan, J. W. Chiu, B. H. Koller, and M. Jasin (1999). Brca1 controls homology-directed DNA repair. Mol. Cell 4 4):511-518.
45. J. Zhang, H. Willers, Z. Feng, J. C. Ghosh, S. Kim, D. T. Weaver, et al. (2004). Chk2 phosphorylation of BRCA1 regulates DNA double-strand break repair. Mol. Cell Biol. 24(2):708-718.
46. F. Xia, D. G. Taghian, J. S. DeFrank, Z. C. Zeng, H. Willers, G. Iliakis, et al. (2001). Deficiency of human BRCA2 leads to impaired homologous recombination but maintains normal nonhomologous endjoining. Proc. Natl. Acad. Sci. U.S.A. 98(15):8644-8649.
47. M. Tarsounas, D. Davies, and S. C. West (2003). BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 22 8):1115-1123.
48. R. Scully, J. Chen, R. L. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, et al. (1997). Dynamic changes of BRCA1 sub-nuclear location and phosphorylation state are initiated by DNA damage. Cell 90 3):425-435.
49. R. S. Tibbetts, D. Cortez, K. M. Brumbaugh, R. Scully, D. M. Livingston, S. J. Elledge, et al. (2000). Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes. Dev. 14:2989-3002.
50. J. M. Sogo, M. Lopes, and M. Foiani (2002). Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297(5581):599-602.
51. B. Michel, M. J. Flores, E. Viguera, G. Grompone, M. Seigneur, and V. Bidnenko (2001). Rescue of arrested replication forks by homologous recombination. Proc. Natl. Acad. Sci. U.S.A. 98 15):8181-8188.
52. M. M. Cox, M. F. Goodman, K. N. Kreuzer, D. J. Sherratt, S. J. Sandler, and K. J. Marians (2000). The importance of repairing stalled replication forks. Nature 404(6773):37-41.
53. S. C. Kowalczykowski (2000). Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25 4):156-165.
54. H. Flores-Rozas and R. D. Kolodner (2000). Links between replication, recombination and genome instability in eukaryotes. Trends Biochem. Sci. 25(4):196-200.
55. R. Scully, N. Puget, and K. Vlasakova (2000). DNA polymerase stalling, sister chromatid recombination and the BRCA genes. Oncogene 19:6176-6183.
56. N. J. Bentley, D. A. Holtzman, G. Flaggs, K. S. Keegan, A. DeMaggio, J. C. Ford, et al. (1996). The schizosaccharomyces pombe rad3 checkpoint gene. Embo. J. 15(23):6641-6651.
57. T. A. Weinert, G. L. Kiser, and L. H. Hartwell (1994). Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes. Dev. 8(6):652-665.
58. A. G. Paulovich and L. H. Hartwell (1995). A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82(5):841-847.
59. C. Santocanale and J. F. Diffley (1998). A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395(6702):615-618.
60. M. Lopes, C. Cotta-Ramusino, A. Pellicioli, G. Liberi, P. Plevani, M. Muzi-Falconi, et al. (2001). The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412 6846):557-561.
61. J. A. Tercero and J. F. Diffley (2001). Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412(6846):553-557.
62. R. S. Cha and N. Kleckner (2002). ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297(5581):602-606.
63. K. Myung, A. Datta, and R. D. Kolodner (2001). Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104(3):397-408.
64. A. M. Casper, P. Nghiem, M. F. Arlt, and T. W. Glover (2002). ATR regulates fragile site stability. Cell 111(6):779-789.
65. Y. Wang, 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(8):927-939.
66. A. D. D'Andrea and M. Grompe (2003). The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 3(1):23-34.
67. M. Lomonosov, S. Anand, M. Sangrithi, R. Davies, and A. R. Venkitaraman (2003). Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev. 17 24):3017-3022.
68. D. S. Yu, E. Sonoda, S. Takeda, C. L. Huang, L. Pellegrini, T. L. Blundell, et al. (2003). Dynamic control of Rad51 recombinase by self-association and interaction with BRCA2. Mol. Cell 12 4):1029-1041.
69. E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273(10):5858-5868.
70. E. P. Rogakou, C. Boon, C. Redon, and W. M. Bonner (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146(5):905-916.
71. T. P. Paull, E. P. Rogakou, V. Yamazaki, C. U. Kirchgessner, M. Gellert, and Bonner WM (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10:886-895.
72. J. A. Downs, N. F. Lowndes, and S. P. Jackson (2000). A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408(6815):1001-1004.
73. C. Redon, D. Pilch, E. Rogakou, O. Sedelnikova, K. Newrock, and W. Bonner (2002). Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12(2):162-169.
74. C. H. Bassing, K. F. Chua, J. Sekiguchi, H. Suh, S. R. Whitlow, J. C. Fleming, et al. (2002). Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U.S.A. 99(12):8173-8178.
75. A. Celeste, S. Petersen, P. J. Romanienko, O. Fernandez-Capetillo, H. T. Chen, O. A. Sedelnikova, et al. (2002). Genomic instability in mice lacking histone H2AX. Science 296(5569):922-927.
76. O. Fernandez-Capetillo, H. T. Chen, A. Celeste, I. Ward, P. J. Romanienko, J. C. Morales, et al. (2002). DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4(12):993-997.
77. O. Fernandez-Capetillo, S. K. Mahadevaiah, A. Celeste, P. J. Romanienko, R. D. Camerini-Otero, W. M. Bonner, et al. (2003). H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4(4):497-508.
78. J. A. Aten, J. Stap, P. M. Krawczyk, C. H. van Oven, R. A. Hoebe, J. Essers, et al. (2004). Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303(5654):92-95.
79. L. B. Schultz, N. H. Chehab, A. Malikzay, and T. D. Halazonetis (2000). p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151 7):1381-1390.
80. I. Rappold, K. Iwabuchi, T. Date, and J. Chen (2001). Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153(3):613-620.
81. J. Kobayashi, H. Tauchi, S. Sakamoto, A. Nakamura, K. Morishima, S. Matsuura, et al. (2002). NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12 21):1846-1851.
82. G. S. Stewart, 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(6926):961-966.
83. Z. Lou, K. Minter-Dykhouse, X. Wu, and J. Chen (2003). MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421(6926):957-961.
84. M. Goldberg, M. Stucki, J. Falck, D. D'Amours, D. Rahman, D. Pappin, et al. (2003). MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421(6926):952-956.
85. C. H. Bassing, H. Suh, D. O. Ferguson, K. F. Chua, J. Manis, M. Eckersdorff, et al. (2003). Histone H2AX: A dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114 3):359-370.
86. A. Celeste, S. Difilippantonio, M. J. Difilippantonio, O. Fernandez-Capetillo, D. R. Pilch, O. A. Sedelnikova, et al. (2003 . H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114(3):371-383.
87. M. Warren, C. J. Lord, J. Masabanda, D. Griffin, and A. Ashworth (2003). Phenotypic effects of heterozygosity for a BRCA2 mutation. Hum. Mol. Genet. 12(20):2645-2656.
88. A. Celeste, O. Fernandez-Capetillo, M. J. Kruhlak, D. R. Pilch, D. W. Staudt, A. Lee, et al. (2003). Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5(7):675-679.
89. T. Tsuzuki, Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, M. Sekiguchi, et al. (1996). Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. U.S.A. 93 13):6236-6240.
90. D. S. Lim and Hasty P. (1996). A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell Biol. 16(12):7133-7143.
91. A. D. D'Andrea (2003). The Fanconi road to cancer. Genes Dev. 17 16):1933-1936.
92. J. C. Morales, Z. Xia, T. Lu, M. B. Aldrich, B. Wang, C. Rosales, et al. (2003). Role for the BRCA1 C-terminal repeats (BRCT) protein 53BP1 in maintaining genomic stability. J. Biol. Chem. 278 17):14971-14977.
93. I. M. Ward, K. Minn, van Deursen J, and J. Chen (2003). p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell Biol. 23(7):2556-2563.
94. L. C. Wu, Z. W. Wang, J. T. Tsan, M. A. Spillman, A. Phung, X. L. Xu, et al. (1996). Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nature Gene. 14 4):430-440.
95. V. Joukov, 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. U.S.A. 98(21):12078-12083.
96. P. S. Brzovic, 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(10):833-837.
97. K. L. Lorick, 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. U.S.A. 96(20):11364-11369.
98. R. Hashizume, M. Fukuda, I. Maeda, H. Nishikawa, D. Oyake, Y. Yabuki, et al. (2001). The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276(18):14537-14540.
99. I. Garcia-Higuera, T. Taniguchi, S. Ganesan, M. S. Meyn, C. Timmers, J. Hejna, et al. (2001). Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7(2):249-262.
100. C. J. Vandenberg, F. Gergely, C. Y. Ong, P. Pace, D. L. Mallery, K. Hiom, et al. (2003). BRCA1-independent ubiquitination of FANCD2. Mol. Cell 12(1):247-254.
101. F. Wu-Baer, K. Lagrazon, W. Yuan, and R. Baer (2003). The BRCA1/BARD1 heterodimer assembles polyubiquitin chains through an unconventional linkage involving lysine residue K6 of ubiquitin. J. Biol. Chem. 278(37):34743-34746.
102. H. Nishikawa, S. Ooka, K. Sato, K. Arima, J. Okamoto, R. E. Klevit, et al. (2004). Mass spectrometric and mutational analyses reveal Lys-6-linked polyubiquitin chains catalyzed by BRCA1-BARD1 ubiquitin ligase. J. Biol. Chem. 279(6):3916-3924.
103. P. S. Brzovic, 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. 28: 8.
104. H. Ruffner, 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. U.S.A. 98 9):5134-5139.
105. B. J. Orelli, J. M. Logsdon Jr., and D. K. Bishop (2001). Nine novel conserved motifs in BRCA1 identified by the chicken orthologue. Oncogene 20(32):4433-4438.
106. S. J. Boulton, J. S. Martin, J. Polanowska, D. E. Hill, A. Gartner, and M. Vidal (2004). BRCA1/BARD1 orthologs required for DNA repair in Caenorhabditis elegans. Curr. Biol. 14(1):33-39.
107. C. A. Wilson, M. N. Payton, G. S. Elliott, F. W. Buaas, E. E. Cajulis, D. Grosshans, et al. (1997). Differential subcellular localization, expression and biological toxicity of BRCA1 and the splice variant BRCA1-delta11b. Oncogene 14(1):1-16.
108. L. J. Huber, 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(12):4005-4015.
109. S. B. Cantor, D. W. Bell, S. Ganesan, E. M. Kass, R. Drapkin, S. Grossman, et al. (2001). BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105(1):149-160.
110. X. Yu, C. C. Chini, M. He, G. Mer, and J. Chen (2003). The BRCT domain is a phospho-protein binding domain. Science 302(5645 ):639-642.
111. T. T. Paull, D. Cortez, B. Bowers, S. J. Elledge, and M. Gellert (2001). Direct DNA binding by Brca1. Proc. Natl. Acad. Sci. U.S.A. 98(11):6086-6091.
112. R. Mizuta, J. M. LaSalle, H. L. Cheng, A. Shinohara, H. Ogawa, N. Copeland, et al. (1997). RAB22 and RAB163/mouse BRCA2: Proteins that specifically interact with the RAD51 protein. Proc. Natl. Acad. Sci. U.S.A. 94(13):6927-6932.
113. A. K. Wong, R. Pero, P. A. Ormonde, S. V. Tavtigian, and P. L. Bartel (1997). RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J. Biol. Chem. 272(51):31941-31944.
114. J. Chen, D. P. Silver, D. Walpita, S. B. Cantor, A. F. Gazdar, G. Tomlinson, et al. (1998). Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell. 2(3):317-328.
115. A. A. Davies, J. Y. Masson, M. J. McIlwraith, A. Z. Stasiak, A. Stasiak, A. R. Venkitaraman, et al. (2001). Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell. 7(2):273-282.
116. L. Pellegrini, D. S. Yu, T. Lo, S. Anand, M. Lee, T. L. Blundell, et al. (2002). Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420(6913):287-293.
117. Y. Dong, M. A. Hakimi, X. Chen, E. Kumaraswamy, N. S. Cooch, A. K. Godwin, et al. (2003). Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol. Cell. 12(5):1087-1099.
118. N. J. Marston, W. J. Richards, D. Hughes, D. Bertwistle, C. J. Marshall, and A. Ashworth (1999). Interaction between the product of the breast cancer susceptibility gene BRCA2 and DSS1, a protein functionally conserved from yeast to mammals. Mol. Cell Biol. 19 7):4633-4642.
119. M. Kojic, C. F. Kostrub, A. R. Buchman, and W. K. Holloman (2002). BRCA2 homolog required for proficiency in DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell. 10 3):683-691.
120. M. Kojic, H. Yang, C. F. Kostrub, N. P. Pavletich, and W. K. Holloman (2003). The BRCA2-interacting protein DSS1 is vital for DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell. 12(4):1043-1049.
121. H. Yang, P. D. Jeffrey, J. Miller, E. Kinnucan, Y. Sun, N. H. Thoma, et al. (2002). BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297(5588 :1837-1848.