DNA recombination, chromosomal stability and carcinogenesis: Insights into the role of BRCA2

DNA Repair

Volumn 3, Issue 8-9, 2004, Pages 835-843

  Shivji, Mahmud K K ^a   Venkitaraman, Ashok R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

BRCA2; Carcinogenesis; DNA recombination

Indexed keywords

BRCA2 PROTEIN; DOUBLE STRANDED DNA; RAD51 PROTEIN; RECOMBINASE;

ALLELE; BREAST CANCER; CANCER SUSCEPTIBILITY; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CHROMOSOME STRUCTURE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRAND; DNA STRAND BREAKAGE; FANCONI ANEMIA; GENE MUTATION; GENETIC STABILITY; HUMAN; INHERITANCE; NONHUMAN; OLIGOMERIZATION; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW;

ALLELES; ANIMALS; BRCA2 PROTEIN; CELL NUCLEUS; CHROMOSOMES; CRYSTALLOGRAPHY, X-RAY; DNA; DNA DAMAGE; DNA REPLICATION; DNA-BINDING PROTEINS; GENETIC PREDISPOSITION TO DISEASE; GERM-LINE MUTATION; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NEOPLASMS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RAD51 RECOMBINASE; RECOMBINATION, GENETIC;

EID: 3242878504     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2004.03.008     Document Type: Review

References (57)

1. Rahman N., Stratton M.R. The genetics of breast cancer susceptibility. Annu. Rev. Genet. 32:1998;95-121
2. Nathanson K.N., Wooster R., Weber B.L. Breast cancer genetics: what we know and what we need. Nat. Med. 7:2001;552-556
3. Thorlacius S., Olafsdottir G., Tryggvadottir L., Neuhausen S., Jonasson J.G., Tavtigian S.V., Tulinius H., Ogmundsdottir H.M., Eyfjord J.E. A single BRCA2 mutation in male and female breast cancer families from Iceland with varied cancer phenotypes. Nat. Genet. 13:1996;117-119
4. Struewing J.P., Hartge P., Wacholder S., Baker S.M., Berlin M., McAdams M., Timmerman M.M., Brody L.C., Tucker M.A. The risk of cancer associated with specific mutations of BRCA1 and BRCA2 among Ashkenazi Jews. N. Engl. J. Med. 336:1997;1401-1408
5. Cancer risks in BRCA2 mutation carriers, The Breast Cancer Linkage Consortium, J. Natl. Cancer Inst. 91 (1999) 1310-1316.
6. Thompson D., Easton D.F. Cancer incidence in BRCA1 mutation carriers. J. Natl. Cancer Inst. 94:2002;1358-1365
7. Howlett N.G., Taniguchi T., Olson S., Cox B., Waisfisz Q., De Die-Smulders C., Persky N., Grompe M., Joenje H., Pals G., Ikeda H., Fox E.A., D'Andrea A.D. Bi-allelic inactivation of BRCA2 in Fanconi anemia. Science. 297:2002;606-609
8. Offit K., Levran O., Mullaney B., Mah K., Nafa K., Batish S.D., Diotti R., Schneider H., Deffenbaugh A., Scholl T., Proud V.K., Robson M., Norton L., Ellis N., Hanenberg H., Auerbach A.D. Shared genetic susceptibility to breast cancer, brain tumors, and Fanconi anemia. J. Natl. Cancer Inst. 95:2003;1548-1551
9. Bork P., Blomberg N., Nilges M. Internal repeats in the BRCA2 protein sequence. Nat. Genet. 13:1996;22-23. (letter)
10. Chen P.L., Chen C.F., Chen Y., Xiao J., Sharp Z.D., Lee W.H. The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc. Natl. Acad. Sci. U.S.A. 95:1998;5287-5292
11. Wong A.K.C., Pero R., Ormonde P.A., Tavtigian S.V., Bartel P.L. RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J. Biol. Chem. 272:1997;31941-31944
12. Egelman E.H. A tale of two polymers: new insights into helical filaments. Nat. Rev. Mol. Cell Biol. 4:2003;621-630
13. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4:2003;435-445
14. Sharan S.K., Morimatsu M., Albrecht U., Lim D., Regel E., Dinh C., Sands A., Eichele G., Hasty P., Bradley A. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature. 386:1997;804-810
15. Mizuta R., LaSalle J.M., Cheng H.L., Shinohara A., Ogawa H., Copeland N., Jenkins N.A., Lalande M., Alt F.W. RAB22 and RAB163/mouse BRCA2: proteins that specifically interact with the RAD51 protein. Proc. Natl. Acad. Sci. U.S.A. 94:1997;6927-6932
16. Lim D.S., Hasty P. 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
17. Tsuzuki T., Fujii Y., Sakumi K., Tominaga Y., Nakao K., Sekiguchi M., Matsushiro A., Yoshimura Y., Morita T. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. U.S.A. 93:1996;6236-6240
18. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:1998;598-608
19. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S. 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. 17:1998;5497-5508
20. Sung P. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272:1997;28194-28197
21. Sugiyama T., Zaitseva E.M., Kowalczykowski S.C. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272:1997;7940-7945
22. New J.H., Sugiyama T., Zaitseva E., Kowalczykowski S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature. 391:1998;407-410
23. Benson F.E., Baumann P., West S.C. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature. 391:1998;401-404
24. Yu X., Jacobs S.A., West S.C., Ogawa T., Egelman E.H. Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc. Natl. Acad. Sci. U.S.A. 98:2001;8419-8424
25. Haaf T., Golub E.I., Reddy G., Radding C.M., Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. U.S.A. 92:1995;2298-2302
26. Chen J., Silver D.P., Walpita D., Cantor S.B., Gazdar A.F., Tomlinson G., Couch F.J., Weber B.L., Ashley T., Livingston D.M., Scully R. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell. 2:1998;317-328
27. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10:2000;886-895
28. Yuan S.S., Lee S.Y., Chen G., Song M., Tomlinson G.E., Lee E.Y. BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res. 59:1999;3547-3551
29. Chen C.F., Chen P.L., Zhong Q., Sharp Z.D., Lee W.H. Expression of BRC repeats in breast cancer cells disrupts the BRCA2-Rad51 complex and leads to radiation hypersensitivity and loss of G(2)/M checkpoint control. J. Biol. Chem. 274:1999;32931-32935
30. Yu V.P.C.C., Koehler M., Steinlein C., Schmid M., Hanakahi L., van Gool A., West S.C., Venkitaraman A.R. Gross chromosomal rearrangements and genetic exchange between non-homologous chromosomes following BRCA2 inactivation. Genes Dev. 14:2000;1400-1406
31. Tarsounas M., Davies D., West S.C. BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene. 22:2003;1115-1123
32. Davies A.A., Masson J.Y., McIlwraith M.J., Stasiak A.Z., Stasiak A., Venkitaraman A.R., West S.C. Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell. 7:2001;273-282
33. Pellegrini L., Yu D.S., Lo T., Anand S., Lee M., Blundell T.L., Venkitaraman A.R. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature. 420:2002;287-293
34. Shin D.S., Pellegrini L., Daniels D.S., Yelent B., Craig L., Bates D., Yu D.S., Shivji M.K., Hitomi C., Arvai A.S., Volkmann N., Tsuruta H., Blundell T.L., Venkitaraman A.R., Tainer J.A. Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J. 22:2003;4566-4576
35. Aihara H., Ito Y., Kurumizaka H., Yokoyama S., Shibata T. The N-terminal domain of the human Rad51 protein binds DNA: structure and a DNA binding surface as revealed by NMR. J. Mol. Biol. 290:1999;495-504
36. Selmane T., Camadro J.M., Conilleau S., Fleury F., Tran V., Prevost C., Takahashi M. Identification of the subunit-subunit interface of Xenopus Rad51.1 protein: similarity to RecA. J. Mol. Biol. 335:2004;895-904
37. Bignell G., Micklem G., Stratton M.R., Ashworth A., Wooster R. The BRC repeats are conserved in mammalian BRCA2 proteins. Hum. Mol. Genet. 6:1997;53-58
38. Lo T., Pellegrini L., Venkitaraman A.R., Blundell T.L. Sequence fingerprints in BRCA2 and RAD51: implications for DNA repair and cancer. DNA Repair (Amst.). 2:2003;1015-1028
39. Kojic M., Kostrub C.F., Buchman A.R., Holloman W.K. BRCA2 homolog required for proficiency in DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell. 10:2002;683-691
40. Yu D.S., Sonoda E., Takeda S., Huang C.L., Pellegrini L., Blundell T.L., Venkitaraman A.R. Dynamic control of Rad51 recombinase by self-association and interaction with BRCA2. Mol. Cell. 12:2003;1029-1041
41. VanLoock M.S., Yu X., Yang S., Lai A.L., Low C., Campbell M.J., Egelman E.H. ATP-mediated conformational changes in the RecA filament. Structure (Camb.). 11:2003;187-196
42. Moynahan M.E., Pierce A.J., Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell. 7:2001;263-272
43. Tutt A., Bertwistle D., Valentine J., Gabriel A., Swift S., Ross G., Griffin C., Thacker J., Ashworth A. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20:2001;4704-4716
44. Xia F., Taghian D.G., DeFrank J.S., Zeng Z.C., Willers H., Iliakis G., Powell S.N. Deficiency of human BRCA2 leads to impaired homologous recombination but maintains normal non-homologous end-joining. Proc. Natl. Acad. Sci. U.S.A. 98:2001;8644-8649
45. Venkitaraman A.R. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell. 108:2002;171-182
46. Yang H., Jeffrey P.D., Miller J., Kinnucan E., Sun Y., Thoma N.H., Zheng N., Chen P.L., Lee W.H., Pavletich N.P. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science. 297:2002;1837-1848
47. Takata M., Tachiiri S., Fujimori A., Thompson L.H., Miki Y., Hiraoka M., Takeda S., Yamazoe M. Conserved domains in the chicken homologue of BRCA2. Oncogene. 21:2002;1130-1134
48. Warren M., Smith A., Partridge N., Masabanda J., Griffin D., Ashworth A. Structural analysis of the chicken BRCA2 gene facilitates identification of functional domains and disease causing mutations. Hum. Mol. Genet. 11:2002;841-851
49. Marston N.J., Richards W.J., Hughes D., Bertwistle D., Marshall C.J., Ashworth A. Interaction between the product of the breast cancer susceptibility gene BRCA2 and DSS1, a protein functionally conserved from yeast to mammals. Mol. Cell Biol. 19:1999;4633-4642
50. Kojic M., Yang H., Kostrub C.F., Pavletich N.P., Holloman W.K. The BRCA2-interacting protein DSS1 is vital for DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell. 12:2003;1043-1049
51. Connor F., Bertwistle D., Mee P.J., Ross G.M., Swift S., Grigorieva E., Tybulewicz V.L., Ashworth A. Tumorigenesis and a DNA repair defect in mice with a truncating Brca2 mutation. Nat. Genet. 17:1997;423-430
52. Patel K.J., Lee H., Corcoran A., Thistlethwaite F.C., Evans M.J., Colledge W.H., Friedman L.S., Ponder B.A., Venkitaraman A.R. Involvement of Brca2 in DNA repair. Mol. Cell. 1:1998;347-357
53. Tutt A., Gabriel A., Bertwistle D., Connor F., Paterson H., Peacock J., Ross G., Ashworth A. Absence of brca2 causes genome instability by chromosome breakage and loss associated with centrosome amplification. Curr. Biol. 9:1999;1107-1110. (in process citation)
54. Venkitaraman A.R. The breast cancer susceptibility gene. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 355:2000;191-198
55. Cox M.M., Goodman M.F., Kreuzer K.N., Sherratt D.J., Sandler S.J., Marians K.J. The importance of repairing stalled replication forks. Nature. 404:2000;37-41
56. Akkari Y.M., Bateman R.L., Reifsteck C.A., Olson S.B., Grompe M. DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol. Cell Biol. 20:2000;8283-8289
57. Kraakman-van der Zwet M., Overkamp W.J., van Lange R.E., Essers J., van Duijn-Goedhart A., Wiggers I., Swaminathan S., van Buul P.P., Errami A., Tan R.T., Jaspers N.G., Sharan S.K., Kanaar R., Zdzienicka M.Z. Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol. Cell Biol. 22:2002;669-679