The breast cancer susceptibility gene, BRCA2: At the crossroads between DNA replication and recombination?

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 355, Issue 1394, 2000, Pages 191-198

  Venkitaraman, Ashok R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

BRCA2; Cancer; DNA replication; Homologous recombination

Indexed keywords

BREAST CANCER SUSCEPTIBILITY GENE; CELL DIVISION; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; GENETIC STABILITY; GENETIC SUSCEPTIBILITY; HOMOLOGOUS RECOMBINATION; MODEL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 0034728447     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2000.0558     Document Type: Article

References (91)

1. Albala J. S., Thelen, M. P., Prange, C., Fan, W., Christensen, M., Thompson, L. H. & Lennon, G. G. 1997 Identification of a novel human RAD51 homolog, RAD51B. Genomics 46, 476-479.
2. Baumann, P., Benson, F. E. & West, S. C. 1997 Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87, 757-766.
3. Benson, F. E., Baumann, P. & West, S. C. 1998 Synergistic actions of Rad51 and Rad52 in recombination and DNA repair [see comments]. Nature 391, 401-404.
4. Bertwistle, D., Swift, S., Marston, N. J., Jackson, L. E., Crossland, S., Crompton, M. R., Marshall, C. J. & Ashworth, A. 1997 Nuclear location and cell cycle regulation of the BRCA2 protein. Cancer Res. 57, 5485-5488.
5. Bezzubova, O., Silbergleit, A., Yamaguchi-Iwai, Y., Takeda, S. & Buerstedde, J. M. 1997 Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line. Cell 89, 185-193.
6. Bignell, G., Micklem, G., Stratton, M. R., Ashworth, A. & Wooster, R. 1997 The BRC repeats are conserved in mammalian BRCA2 proteins. Hum. Mol. Genet. 6, 53-58.
7. Bishop, D. K., Park, D., Xu, L. & Kleckner, N. 1992 DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439-456.
8. Bork, P., Blomberg, N. & Nilges, M. 1996 Internal repeats in the BRCA2 protein sequence [letter]. Nature Genet. 13, 22-23.
9. Cartwright, R., Tambini, C. E., Simpson, P. J. & Thacker, J. 1998 The XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family. Nucl. Acids Res. 26, 3084-3089.
10. Chapman, M. S. & Verma, I. M. 1996 Transcriptional activation by BRCA1 [letter; comment]. Nature 382, 678-679.
11. Chen, C., Umezu, K. & Kolodner, R. D. 1998a Chromosomal rearrangements occur in S. cerevisiae rfal mutator mutants due to mutagenic lesions processed by double-strand-break repair. Mol. Cell 2, 9-22.
12. Chen, P. L., Chen, C. F., Chen, Y., Xiao, J., Sharp, Z. D. & Lee, W. H. 1998b The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc. Natl Acad. Sci. USA 95, 5287-5292.
13. Chen, J. (and 10 others) 1998c Stable interaction between the products of the BRCA1 and BRCA2 tumour suppressor genes in mitotic and meiotic cells. Mol. Cell 2, 317-328.
14. Cheong, N., Wang, X., Wang, Y. & Iliakis, G. 1994 Loss of S-phase dependent radioresistance in irs-1 cells exposed to cross-linking agents. Mutat. Res. 314, 77-85.
15. Collins, N., McManus, R., Wooster, R., Mangion, J., Seal, S., Lakhani, S., Ormiston, W. & Daly, P. A. 1995 Consistent loss of the wild-type allele in breast cancers from a family linked to the BRCA2 gene on chromosome 13q12-13. Oncogene 10, 1673-1675.
16. Connor, F., Bertwistle, D., Mee, P. J., Ross, G. M., Swift, S., Grigorieva, E., Tybulewicz, V. L. & Ashworth, A. 1997 Tumorigenesis and a DNA repair defect in mice with a truncating Brca2 mutation. Nature Genet. 17, 423-430.
17. Courcelle, J., Carswell-Crumpton, C. & Hanawalt, P. C. 1997 recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc. Natl Acad. Sci. USA 94, 3714-3719.
18. Cox, M. M. 1997 Recombinational crossroads: eukaryotic enzymes and the limits of bacterial precedents. Proc. Natl Acad. Sci. USA 94, 11 764-11 766.
19. Dosanjh, M. K., Collins, D.W., Fan, W., Lennon, G. G., Albala, J. S., Shen, Z. & Schild, D. 1998 Isolation and characterization of RAD51C, a new human member of the RAD51 family of related genes. Nucl. Acids Res. 26, 1179-1184.
20. Essers, J., Hendriks, R. W., Swagemakers, S. M., Troelstra, C., De Wit, J., Bootsma, D., Hoeijmakers, J. H. & Kanaar, R. 1997 Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89, 195-204.
21. Friedberg, E. C., Walker, G. C. & Siede, W. 1995 DNA repair and mutagenesis. Washington, DC: ASM Press.
22. Friedman, L. S. (and 11 others) 1998 Thymic lymphomas in mice with a truncating mutation in Brca2. Cancer Res. 58, 1338-1343.
23. Fuks, F., Milner, J. & Kouzarides, T. 1998 BRCA2 associates with acetyltransferase activity when bound to P/CAF. Oncogene 17, 2531-2534.
24. Gayther, S. A., Mangion, J., Russell, P., Seal, S., Barfoot, R., Ponder, B. A., Stratton, M. R. & Easton, D. 1997 Variation of risks of breast and ovarian cancer associated with different germline mutations of the BRCA2 gene. Nature Genet. 15, 103-105.
25. German, J. 1993 Bloom syndrome: a Mendelian prototype of somatic mutational disease. Medicine 72, 393-406.
26. Gowen, L. C., Johnson, B. L., Latour, A. M., Sulik, K. K. & Koller, B. H. 1996 Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nature Genet. 12, 191-194.
27. Gowen, L. C., Avrutskaya, A. V., Latour, A. M., Koller, B. H. & Leadon, S. A. 1998 BRCA1 required for transcription-coupled repair of oxidative DNA damage. Science 281, 1009-1012.
28. Gudmundsson, J., Johannesdottir, G., Bergthorsson, J., Arason, A., Ingvarsson, S., Egilsson, V. & Barkardottir, R. 1995 Different tumour types from BRCA2 carriers show wild-type chromosome deletions on 13q12q13. Cancer Res. 55, 4830-4832.
29. Gudmundsson, J., Johannesdottir, G., Arason, A., Bergthorsson, J. T., Ingvarsson, S., Egilsson, V. & Barkardottir, R. B. 1996 Frequent occurrence of BRCA2 linkage in Icelandic breast cancer families and segregation of a common BRCA2 haplotype. Am. J. Hum. Genet. 58, 749-756.
30. Gupta, R. C., Bazemore, L. R., Golub, E. I. & Radding, C. M. 1997 Activities of human recombination protein Rad51. Proc. Natl Acad. Sci. USA 94, 463-468.
31. Haber, J. E. 1997 A super new twist on the initiation of meiotic recombination. Cell 89, 163-166.
32. Hakem, R. (and 14 others) 1996 The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85, 1009-1023.
33. Jackson, S. P. & Jeggo, P. A. 1995 DNA double-strand break repair and V(D)J recombination: involvement of DNA-PK. Trends Biochem. Sci. 20, 412-415.
34. Jin, Y., Xu, X. L., Yang, M. C., Wei, F., Ayi, T. C., Bowcock, A. M. & Baer, R. 1997 Cell cycle-dependent colocalization of BARD1 and BRCA1 proteins in discrete nuclear domains. Proc. Natl Acad. Sci. USA 94, 12 075-12 080.
35. Johannesdottir, G. (and 11 others) 1996 High prevalence of the 999del5 mutation in icelandic breast and ovarian cancer patients. Cancer Res. 56, 3663-3665.
36. Jones, N. J., Cox, R. & Thacker, J. 1987 Isolation and cross-sensitivity of X-ray-sensitive mutants of V79-4 hamster cells. Mutat. Res. 183, 279-286.
37. Keeney, S., Giroux, C. N. & Kleckner, N. 1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spoll, a member of a widely conserved protein family. Cell 88, 375-384.
38. Kogoma, T. 1996 Recombination by replication. Cell 85, 625-627.
39. Kogoma, T. 1997 Stable DNA replication: an interplay between DNA replication, homologous recombination and transcription. Microbiol. Mol. Biol. Rev. 61, 212-238.
40. Kuzminov, A. 1995 Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16, 373-384.
41. Lee, H., Trainer, A. H., Thistlethwaite, F. C., Evans, M. J., Friedman, L. S., Ponder, B. A. J. & Venkitaraman, A. R. 1999 Mitotic checkpoint inactivation fosters the transformation of cells lacking the breast cancer susceptibility gene BRCA2. Mol. Cell. 4, 1-10.
42. Liang, F., Han, M., Romanienko, P. J. & Jasin, M. 1998 Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl Acad. Sci. USA 95, 5172-5177.
43. Lim, D. S. & 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, 7133-7143.
44. Lindahl, T. 1993 Instability and decay of the primary structure of DNA [see comments]. Nature 362, 709-715.
45. Lindahl, T. 1996 The Croonian Lecture, 1996. Endogenous damage to DNA. Phil. Trans. R. Soc. Lond. B 351, 1529-1538.
46. Liu, C. Y., Flesken-Nikitin, A., Li, S., Zeng, Y. & Lee, W. H. 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.
47. Liu, J., Xu, L., Sandler, S. J. & Marians, K. J. 1999 Replication fork assembly at recombination intermediates is required for bacterial growth. Proc. Natl Acad. Sci. USA 96, 3552-3555.
48. Liu, N. (and 16 others) 1998 XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol. Cell 1, 783-793.
49. Ludwig, T., Chapman, D. L., Papaioannou, V. E. & Efstratiadis, A. 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.
50. Meselson, M. S. & Radding, C. M. 1975 A general model for genetic recombination. Proc. Natl Acad. Sci. USA 72, 358-361.
51. Michel, B., Ehrlich, S. D. & Uzest, M. 1997 DNA double-strand breaks caused by replication arrest. EMBO J. 16, 430-438.
52. Miki, Y., Swensen, J., Shattuck-Eidens, D., Futreal, P., Harshmann, K., Tavtigian, S., Liu, Q., Cochran, C., Bennett, L. M. & Ding, W. 1994 A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266, 66-71.
53. Mizuta, R., LaSalle, J. M., Cheng, H., Shinohara, A., Ogawa, H., Copeland, N., Jenkins, N. A., Lalande, M. & Alt, F. W. 1997 RAB22 and RAB163/mouse BRCA2: proteins that interact specifically with the RAD51 protein. Proc. Natl Acad. Sci. USA 94, 6927-6932.
54. Neuhausen, S. (and 13 others) 1996 Recurrent BRCA2 6174delT mutations in Ashkenazi Jewish women affected by breast cancer. Nature Genet. 13, 126-128.
55. New, J. H., Sugiyama, T., Zaitseva, E. & Kowalczykowski, S. C. 1998 Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A [see comments]. Nature 391, 407-410.
56. Ogawa, T., Yu, X., Shinohara, A. & Egelman, E. H. 1993 Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259, 1896-1899.
57. Patel, K. J., Yu, V. P. C. C., Lee, H., Corcoran, A., Thistlethwaite, F. C., Evans, M. J., Colledge, W. H., Friedman, L. S., Ponder, B. A. & Venkitaraman, A. R. 1998 Involvement of Brca2 in DNA repair. Mol. Cell 1, 347-357.
58. Pittman, D. L., Weinberg, L. R. & Schimenti, J. C. 1998 Identification, characterization, and genetic mapping of Rad51d, a new mouse and human RAD51/RecA-related gene. Genomics 49, 103-111.
59. Rahman, N. & Stratton, M. R. 1998 The genetics of breast cancer susceptibility. A. Rev. Genet. 32, 95-121.
60. Rajan, J. V., Wang, M., Marquis, S. T. & Chodosh, L. A. 1996 Brca2 is co-ordinately regulated with Brca1 during proliferation and differentiation in mammary epithelial cells. Proc. Natl Acad. Sci. USA 93, 7131-7136.
61. Roca, A. I. & Cox, M. M. 1997 RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acids Res. Mol. Biol. 56, 129-223.
62. Rothstein, R. & Gangloff, S. 1995 Hyper-recombination and Bloom's syndrome: microbes again provide clues about cancer. Genome Res. 5, 421-426.
63. Rouct, P., Smih, F. & Jasin, M. 1994 Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14, 8096-8106.
64. Scully, R., Chen, J., Plug, A., Xiao, Y., Weaver, D., Feunteun, J., Ashley, T. & Livingston, D. M. 1997 Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88, 265-275.
65. Seigneur, M., Bidnenko, V., Ehrlich, S. D. & Michel, B. 1998 RuvAB acts at arrested replication forks. Cell 95, 419-430.
66. Sharan, S. K. & Bradley, A. 1997 Murine Brca2: sequence, map position, and expression pattern. Genomics 40, 234-241.
67. Sharan, S. K., Morimatsu, M., Albrecht, U., Lim, D., Regel, E., Dinh, C., Sands, A., Eichele, G., Hasty, P. & Bradley, A. 1997 Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386, 804-810.
68. Shinohara, A., Ogawa, H. & Ogawa, T. 1992a Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457-470.
69. Shinohara, A., Ogawa, H. & Ogawa, T. 1992b Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457-470. [Published erratum appears in Cell 71, following 180 (1992)].
70. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S. & Ogawa, T. 1998 Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells 3, 145-156.
71. Sonoda, E., Sasaki, M. S., Buerstedde, J. M., Bezzubova, O., Shinohara, A., Ogawa, H., Takata, M., Yamaguchi-Iwai, Y. & Takeda, S. 1998 Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17, 598-608.
72. Stamato, T. D., Dipatri, A. & Giaccia, A. 1988 Cell-cycle-dependent repair of potentially lethal damage in the XR-1 gamma-ray-sensitive Chinese hamster ovary cell. Radiat. Res. 115, 325-333.
73. Sturzbecher, H. W., Donzelmann, B., Henning, W., Knippschild, U. & Buchhop, S. 1996 p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO J. 15, 1992-2002.
74. Sung, P. 1994 Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265, 1241-1243.
75. Sung, P. 1997 Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272, 28 194-28 197.
76. Sung, P. & Robberson, D. L. 1995 DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82, 453-461.
77. Sung, P. & Stratton, S. A. 1996 Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem. 271, 27 983-27 986.
78. Suzuki, A. (and 15 others) 1997 Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev. 11, 1242-1252.
79. Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J. & Stahl, F. W. 1983 The double-strand-break repair model for recombination. Cell 33, 25-35.
80. Takata, M., Sasaki, M. S., Sonoda, E., Morrison, C., Hashimoto, M., Utsumi, H., Yamaguchi-Iwai, Y., Shinohara, A. & Takeda, S. 1998 Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17, 5497-5508.
81. Tavtigian, S. V. (and 27 others) 1996 The complete BRCA2 gene and mutations in chromosome 13q-linked kindreds [see comments]. Nature Genet. 12, 333-337.
82. Thorlacius, S., Olafsdottir, G., Tryggvadottir, L., Neuhausen, S., Jonasson, J. G., Tavtigian, S. V., Tulinius, H., Ogmundsdottir, H. M. & Eyfjord, J. E. 1996 A single BRCA2 mutation in male and female breast cancer families from Iceland with varied cancer phenotypes [see comments]. Nature Genet. 13, 117-119.
83. Tsuzuki, T., Fujii, Y., Sakumi, K., Tominaga, Y., Nakao, K., Sekiguchi, M., Matsushiro, A., Yoshimura, Y. & Morita, T. 1996 Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl Acad. Sci. USA 93, 6236-6240.
84. Venkitaraman, A. R. 1999 What makes breast cancer cells tick? Cell 99, 270-272.
85. West, S. C., Cassuto, E. & Howard-Flanders, P. 1981 Mechanism of E. coli RecA protein directed strand exchanges in post-replication repair of DNA. Nature 294, 659-662.
86. Whitmore, G. F., Varghese, A. J. & Gulyas, S. 1989 Cell cycle responses of two X-ray sensitive mutants defective in DNA repair. Int. J. Radiat. Biol. 56, 657-665.
87. Wong, A. K. C., Pero, R., Ormonde, P. A., Tavtigian, S. V. & Bartel, P. L. 1997 RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J. Biol. Chem. 272, 31 941-31 944.
88. Wooster, R. (and 40 others) 1994 Localization of a breast cancer susceptibility gene, BRCA2, to chromosome 13q12-13. Science 265, 2088-2090.
89. Wooster, R., Bignell, J., Lancaster, S., Swift, S., Seal, S., Mangion, N., Collins, S., Gregory, C., Gumbs, G. & Micklem, R. 1995 Identification of the breast-cancer susceptibility gene BRCA2. Nature 378, 789-792.
90. Xu, X., Weaver, Z., Linke, S. P., Li, C., Gotay, J., Wang, X. W., Harris, C. C., Ried, T. & Deng, C. X. 1999 Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell 3, 389-395.
91. Zou, H. & Rothstein, R. 1997 Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90, 87-96.