Deletion of BRCA2 exon 27 causes defects in response to both stalled and collapsed replication forks

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 766-767, Issue , 2014, Pages 66-72

  Kim, Tae Moon ^a   Son, Mi Young ^a   Dodds, Sherry ^a   Hu, Lingchuan ^a   Hasty, Paul ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

BRCA2; Chromosomal instability; Double strand break; RAD51; Replication fork stalling

Indexed keywords

BRCA2 PROTEIN; HYDROXYUREA; MRE11 PROTEIN; RAD51 PROTEIN; REPLICATION FACTOR A; BRCA2 PROTEIN, MOUSE; DNA BINDING PROTEIN; DNA LIGASE; MRE11A PROTEIN, MOUSE; NUCLEIC ACID SYNTHESIS INHIBITOR; PROTEIN BINDING; RAD51 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CHROMATIN; CHROMOSOMAL INSTABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; EMBRYONIC STEM CELL; EXON; GENOMIC INSTABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REPLICATION FORK; TUMOR SUPPRESSOR GENE; ANIMAL; BINDING SITE; CELL CULTURE; DNA REPAIR; DNA REPLICATION ORIGIN; DRUG EFFECTS; GENE DELETION; GENETICS; METABOLISM;

ANIMALS; BINDING SITES; BRCA2 PROTEIN; CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPAIR ENZYMES; DNA REPLICATION; DNA-BINDING PROTEINS; EXONS; GENE DELETION; GENOMIC INSTABILITY; HYDROXYUREA; MICE; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN BINDING; RAD51 RECOMBINASE; REPLICATION ORIGIN;

EID: 84903837239     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2014.06.003     Document Type: Article

References (43)

1. Wooster R., Bignell G., Lancaster J., Swift S., Seal S., Mangion J., Collins N., Gregory S., Gumbs C., Micklem G. Identification of the breast cancer susceptibility gene BRCA2. Nature 1995, 378:789-792. [see comments] [published erratum appears in Nature 1996 Feb 22;379(6567):749].
2. 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. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 2002, 297:606-609.
3. Haber D.A. The BRCA2-EMSY connection: implications for breast and ovarian tumorigenesis. Cell 2003, 115:507-508.
4. Hughes-Davies L., Huntsman D., Ruas M., Fuks F., Bye J., Chin S.F., Milner J., Brown L.A., Hsu F., Gilks B., Nielsen T., Schulzer M., Chia S., Ragaz J., Cahn A., Linger L., Ozdag H., Cattaneo E., Jordanova E.S., Schuuring E., Yu D.S., Venkitaraman A., Ponder B., Doherty A., Aparicio S., Bentley D., Theillet C., Ponting C.P., Caldas C., Kouzarides T. EMSY links the BRCA2 pathway to sporadic breast and ovarian cancer. Cell 2003, 115:523-535.
5. Klein H.L. The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair (Amst.) 2008, 7:686-693.
6. San Filippo J., Sung P., Klein H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 2008, 77:229-257.
7. Williams R.S., Moncalian G., Williams J.S., Yamada Y., Limbo O., Shin D.S., Groocock L.M., Cahill D., Hitomi C., Guenther G., Moiani D., Carney J.P., Russell P., Tainer J.A. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 2008, 135:97-109.
8. Mimitou E.P., Symington L.S. DNA end resection: many nucleases make light work. DNA Repair (Amst.) 2009, 8:983-995.
9. Schlacher K., Christ N., Siaud N., Egashira A., Wu H., Jasin M. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 2011, 145:529-542.
10. Schlacher K., Wu H., Jasin M. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 2012, 22:106-116.
11. Petermann E., Orta M.L., Issaeva N., Schultz N., Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37:492-502.
12. Carr A.M., Lambert S. Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J. Mol. Biol. 2013.
13. Sirbu B.M., Couch F.B., Feigerle J.T., Bhaskara S., Hiebert S.W., Cortez D. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 2011, 25:1320-1327.
14. Kim T.M., Ko J.H., Hu L., Kim S.A., Bishop A.J., Vijg J., Montagna C., Hasty P. RAD51 mutants cause replication defects and chromosomal instability. Mol. Cell. Biol. 2012, 32:3663-3680.
15. 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. Nat. Acad. Sci. U.S.A. 1998, 95:5287-5292.
16. 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. 1999, 274:32931-32935.
17. 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. [see comments].
18. Morimatsu M., Donoho G., Hasty P. Cells deleted for Brca2 COOH terminus exhibit hypersensitivity to gamma-radiation and premature senescence. Cancer Res. 1998, 58:3441-3447.
19. Carreira A., Kowalczykowski S.C. Two classes of BRC repeats in BRCA2 promote RAD51 nucleoprotein filament function by distinct mechanisms. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:10448-10453.
20. Esashi F., Galkin V.E., Yu X., Egelman E.H., West S.C. Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2. Nat. Struct. Mol. Biol. 2007, 14:468-474.
21. Davies O.R., Pellegrini L. Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats. Nat. Struct. Mol. Biol. 2007, 14:475-483.
22. Esashi F., Christ N., Gannon J., Liu Y., Hunt T., Jasin M., West S.C. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 2005, 434:598-604.
23. Szekeres T., Fritzer-Szekeres M., Elford H.L. The enzyme ribonucleotide reductase: target for antitumor and anti-HIV therapy. Crit. Rev. Clin. Lab. Sci. 1997, 34:503-528.
24. Hu L., Kim T.M., Son M.Y., Kim S.A., Holland C.L., Tateishi S., Kim D.H., Yew P.R., Montagna C., Dumitrache L.C., Hasty P. Two replication fork maintenance pathways fuse inverted repeats to rearrange chromosomes. Nature 2013, 501:569-572.
25. Krijger P.H., Lee K.Y., Wit N., van den Berk P.C., Wu X., Roest H.P., Maas A., Ding H., Hoeijmakers J.H., Myung K., Jacobs H. HLTF and SHPRH are not essential for PCNA polyubiquitination, survival and somatic hypermutation: existence of an alternative E3 ligase. DNA Repair (Amst.) 2011, 10:438-444.
26. Motegi A., Liaw H.J., Lee K.Y., Roest H.P., Maas A., Wu X., Moinova H., Markowitz S.D., Ding H., Hoeijmakers J.H., Myung K. Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:12411-12416.
27. Marple T., Li H., Hasty P. A genotoxic screen: rapid analysis of cellular dose-response to a wide range of agents that either damage DNA or alter genome maintenance pathways. Mutat. Res. 2004, 554:253-266.
28. Donoho G., Brenneman M.A., Cui T.X., Donoviel D., Vogel H., Goodwin E.H., Chen D.J., Hasty P. Deletion of Brca2 exon 27 causes hypersensitivity to DNA crosslinks, chromosomal instability, and reduced life span in mice. Genes, Chromosomes Cancer 2003, 36:317-331.
29. Moynahan M.E., Pierce A.J., Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 2001, 7:263-272.
30. Marple T., Kim T.M., Hasty P. Embryonic stem cells deficient for Brca2 or Blm exhibit divergent genotoxic profiles that support opposing activities during homologous recombination. Mutat. Res. 2006, 602:110-120.
31. Recolin B., Van der Laan S., Maiorano D. Role of replication protein A as sensor in activation of the S-phase checkpoint in Xenopus egg extracts. Nucleic Acids Res. 2012, 40:3431-3442.
32. Anantha R.W., Vassin V.M., Borowiec J.A. Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem. 2007, 282:35910-35923.
33. Pilch D.R., Sedelnikova O.A., Redon C., Celeste A., Nussenzweig A., Bonner W.M. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem. Cell Biol. 2003, 81:123-129.
34. Xie A., Puget N., Shim I., Odate S., Jarzyna I., Bassing C.H., Alt F.W., Scully R. Control of sister chromatid recombination by histone H2AX. Mol. Cell 2004, 16:1017-1025.
35. 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. 2000, 10:886-895.
36. Bassing C.H., Chua K.F., Sekiguchi J., Suh H., Whitlow S.R., Fleming J.C., Monroe B.C., Ciccone D.N., Yan C., Vlasakova K., Livingston D.M., Ferguson D.O., Scully R., Alt F.W. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Nat. Acad. Sci. U.S.A. 2002, 99:8173-8178.
37. Tittel-Elmer M., Alabert C., Pasero P., Cobb J.A. The MRX complex stabilizes the replisome independently of the S phase checkpoint during replication stress. EMBO J. 2009, 28:1142-1156.
38. Bryant H.E., Petermann E., Schultz N., Jemth A.S., Loseva O., Issaeva N., Johansson F., Fernandez S., McGlynn P., Helleday T. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 2009, 28:2601-2615.
39. Stracker T.H., Petrini J.H. The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell Biol. 2011, 12:90-103.
40. Paull T.T., Gellert M. The 3' to 5' exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1998, 1:969-979.
41. Guenatri M., Bailly D., Maison C., Almouzni G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 2004, 166:493-505.
42. Sirbu B.M., Couch F.B., Cortez D. Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat. Protoc. 2012, 7:594-605.
43. Moses J.E., Moorhouse A.D. The growing applications of click chemistry. Chem. Soc. Rev. 2007, 36:1249-1262.