BRCA2 is epistatic to the RAD51 paralogs in response to DNA damage

DNA Repair

Volumn 12, Issue 4, 2013, Pages 306-311

  Jensen, Ryan B ^a,b   Ozes, Ali ^a   Kim, Taeho ^a   Estep, Allison ^a   Kowalczykowski, Stephen C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BRCA2; DNA damage; DNA break Repair; RAD51; Recombination

Indexed keywords

BRCA2 PROTEIN; RAD51 PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION; GENETIC EPISTASIS; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MAMMAL CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SISTER CHROMATID;

BRCA2 PROTEIN; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; EPISTASIS, GENETIC; HEK293 CELLS; HUMANS; RAD51 RECOMBINASE; RECOMBINATIONAL DNA REPAIR; RNA, SMALL INTERFERING;

MAMMALIA;

EID: 84874968077     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.12.007     Document Type: Article

References (41)

1. Tebbs R.S., Zhao Y., Tucker J.D., Scheerer J.B., Siciliano M.J., Hwang M., Liu N., Legerski R.J., Thompson L.H. Correction of chromosomal instability and sensitivity to diverse mutagens by a cloned cDNA of the XRCC3 DNA repair gene. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:6354-6358.
2. Albala J.S., Thelen M.P., Prange C., Fan W., Christensen M., Thompson L.H., Lennon G.G. Identification of a novel human RAD51 homolog, RAD51B. Genomics 1997, 46:476-479.
3. Cartwright R., Tambini C.E., Simpson P.J., Thacker J. The XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family. Nucleic Acids Res. 1998, 26:3084-3089.
4. Dosanjh M.K., Collins D.W., Fan W., Lennon G.G., Albala J.S., Shen Z., Schild D. Isolation and characterization of RAD51C, a new human member of the RAD51 family of related genes. Nucleic Acids Res. 1998, 26:1179-1184.
5. Pittman D.L., Weinberg L.R., Schimenti J.C. Identification, characterization, and genetic mapping of Rad51d, a new mouse and human RAD51/RecA-related gene. Genomics 1998, 49:103-111.
6. Masson J.Y., Tarsounas M.C., Stasiak A.Z., Stasiak A., Shah R., McIlwraith M.J., Benson F.E., West S.C. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 2001, 15:3296-3307.
7. Yonetani Y., Hochegger H., Sonoda E., Shinya S., Yoshikawa H., Takeda S., Yamazoe M. Differential collaborative actions of Rad51 paralog proteins in cellular response to DNA damage. Nucleic Acids Res. 2005, 33:4544-4552.
8. Lio Y.C., Mazin A.V., Kowalczykowski S.C., Chen D.J. Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro. J. Biol. Chem. 2003, 278:2469-2478.
9. Sigurdsson S., Van Komen S., Bussen W., Schild D., Albala J.S., Sung P. Mediator function of the human Rad51B-Rad51C complex in Rad51/RPA-catalyzed DNA strand exchange. Genes Dev. 2001, 15:3308-3318.
10. Liu N., Lamerdin J.E., Tebbs R.S., Schild D., Tucker J.D., Shen M.R., Brookman K.W., Siciliano M.J., Walter C.A., Fan W., Narayana L.S., Zhou Z.Q., Adamson A.W., Sorensen K.J., Chen D.J., Jones N.J., Thompson L.H. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol. Cell 1998, 1:783-793.
11. Schild D., Lio Y.C., Collins D.W., Tsomondo T., Chen D.J. Evidence for simultaneous protein interactions between human Rad51 paralogs. J. Biol. Chem. 2000, 275:16443-16449.
12. Takata M., Sasaki M.S., Tachiiri S., Fukushima T., Sonoda E., Schild D., Thompson L.H., Takeda S. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 2001, 21:2858-2866.
13. Godthelp B.C., Wiegant W.W., van Duijn-Goedhart A., Scharer O.D., van Buul P.P., Kanaar R., Zdzienicka M.Z. Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability. Nucleic Acids Res. 2002, 30:2172-2182.
14. Brenneman M.A., Wagener B.M., Miller C.A., Allen C., Nickoloff J.A. XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol. Cell 2002, 10:387-395.
15. Sharan S.K., Morimatsu M., Albrecht U., Lim D.S., 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 1997, 386:804-810.
16. Ludwig T., Chapman D.L., Papaioannou V.E., Efstratiadis A. 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. 1997, 11:1226-1241.
17. Suzuki A., de la Pompa J.L., Hakem R., Elia A., Yoshida R., Mo R., Nishina H., Chuang T., Wakeham A., Itie A., Koo W., Billia P., Ho A., Fukumoto M., Hui C.C., Mak T.W. Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev. 1997, 11:1242-1252.
18. Pittman D.L., Schimenti J.C. Midgestation lethality in mice deficient for the RecA-related gene, Rad51d/Rad51l3. Genesis 2000, 26:167-173.
19. Shu Z., Smith S., Wang L., Rice M.C., Kmiec E.B. Disruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can Be partially rescued in a p53(-/-) background. Mol. Cell Biol. 1999, 19:8686-8693.
20. Deans B., Griffin C.S., Maconochie M., Thacker J. Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice. EMBO J. 2000, 19:6675-6685.
21. Akbari M.R., Tonin P., Foulkes W.D., Ghadirian P., Tischkowitz M., Narod S.A. RAD51C germline mutations in breast and ovarian cancer patients. Breast Cancer Res. 2010, 12:404.
22. A Meindl, Hellebrand H., Wiek C., Erven V., Wappenschmidt B., Niederacher D., Freund M., Lichtner P., Hartmann L., Schaal H., Ramser J., Honisch E., Kubisch C., Wichmann H.E., Kast K., Deissler H., Engel C., Muller-Myhsok B., Neveling K., Kiechle M., Mathew C.G., Schindler D., Schmutzler R.K., Hanenberg H. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat. Genet. 2010, 42:410-414.
23. Somyajit K., Subramanya S., Nagaraju G. RAD51C: a novel cancer susceptibility gene is linked to Fanconi anemia and breast cancer. Carcinogenesis 2010, 31:2031-2038.
24. Zheng Y., Zhang J., Hope K., Niu Q., Huo D., Olopade O.I. Screening RAD51C nucleotide alterations in patients with a family history of breast and ovarian cancer. Breast Cancer Res. Treat. 2010, 124:857-861.
25. Loveday C., Turnbull C., Ramsay E., Hughes D., Ruark E., Frankum J.R., Bowden G., Kalmyrzaev B., Warren-Perry M., Snape K., Adlard J.W., Barwell J., Berg J., Brady A.F., Brewer C., Brice G., Chapman C., Cook J., Davidson R., Donaldson A., Douglas F., Greenhalgh L., Henderson A., Izatt L., Kumar A., Lalloo F., Miedzybrodzka Z., Morrison P.J., Paterson J., Porteous M., Rogers M.T., Shanley S., Walker L., Eccles D., Evans D.G., Renwick A., Seal S., Lord C.J., Ashworth A., Reis-Filho J.S., Antoniou A.C., Rahman N. Germline mutations in RAD51D confer susceptibility to ovarian cancer. Nat. Genet. 2011, 43:879-882.
26. Suwaki N., Klare K., Tarsounas M. RAD51 paralogs: roles in DNA damage signalling, recombinational repair and tumorigenesis. Semin. Cell Dev. Biol. 2011, 22:898-905.
27. Tarunina M., Jenkins J.R. Human p53 binds DNA as a protein homodimer but monomeric variants retain full transcription transactivation activity. Oncogene 1993, 8:3165-3173.
28. Kawabata M., Saeki K. Multiple alternative transcripts of the human homologue of the mouse TRAD/R51H3/RAD51D gene, a member of the rec A/RAD51 gene family, Biochem. Biophys. Res. Commun. 1999, 257:156-162.
29. Gruver A.M., Yard B.D., McInnes C., Rajesh C., Pittman D.L. Functional characterization and identification of mouse Rad51d splice variants. BMC Mol. Biol. 2009, 10:27.
30. Schoenmakers E.F., Huysmans C., Van de Ven W.J. Allelic knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas. Cancer Res. 1999, 59:19-23.
31. Qing Y., Yamazoe M., Hirota K., Dejsuphong D., Sakai W., Yamamoto K.N., Bishop D.K., Wu X., Takeda S. The epistatic relationship between BRCA2 and the other RAD51 mediators in homologous recombination. PLoS Genet. 2011, 7:e1002148.
32. Feng Z., Scott S.P., Bussen W., Sharma G.G., Guo G., Pandita T.K., Powell S.N. Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:686-691.
33. Badie S., Escandell J.M., Bouwman P., Carlos A.R., Thanasoula M., Gallardo M.M., Suram A., Jaco I., Benitez J., Herbig U., Blasco M.A., Jonkers J., Tarsounas M. BRCA2 acts as a RAD51 loader to facilitate telomere replication and capping. Nat. Struct. Mol. Biol. 2010, 17:1461-1469.
34. Tarsounas M., Munoz P., Claas A., Smiraldo P.G., Pittman D.L., Blasco M.A., West S.C. Telomere maintenance requires the RAD51D recombination/repair protein. Cell 2004, 117:337-347.
35. Stagno D'Alcontres M., Mendez-Bermudez A., Foxon J.L., Royle N.J., Salomoni P. Lack of TRF2 in ALT cells causes PML-dependent p53 activation and loss of telomeric DNA. J. Cell Biol. 2007, 179:855-867.
36. Lovejoy C.A., Li W., Reisenweber S., Thongthip S., Bruno J., de Lange T., De S., Petrini J.H., Sung P.A., Jasin M., Rosenbluh J., Zwang Y., Weir B.A., Hatton C., Ivanova E., Macconaill L., Hanna M., Hahn W.C., Lue N.F., Reddel R.R., Jiao Y., Kinzler K., Vogelstein B., Papadopoulos N., Meeker A.K. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet. 2012, 8:e1002772.
37. Sapir E., Gozaly-Chianea Y., Al-Wahiby S., Ravindran S., Yasaei H., Slijepcevic P. Effects of BRCA2 deficiency on telomere recombination in non-ALT and ALT cells. Genome Integr. 2011, 2:9.
38. Jensen R.B., Carreira A., Kowalczykowski S.C. Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 2010, 467:678-683.
39. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 2003, 423:305-309.
40. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 2003, 423:309-312.
41. Liu J., Renault L., Veaute X., Fabre F., Stahlberg H., Heyer W.D. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 2011, 479:245-248.