CtIP-mediated resection is essential for viability and can operate independently of BRCA1

Journal of Experimental Medicine

Volumn 211, Issue 6, 2014, Pages 1027-1036

  Polato, Federica ^a   Callen, Elsa ^a   Wong, Nancy ^a   Faryabi, Robert ^a   Bunting, Samuel ^a   Chen, Hua Tang ^a   Kozak, Marina ^a   Kruhlak, Michael J ^a   Reczek, Colleen R ^d   Lee, Wen Hwa ^b   Ludwig, Thomas ^c   Baer, Richard ^d   Feigenbaum, Lionel ^e   Jackson, Stephen ^f,g,h   Nussenzweig, André ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^d NewYork Presbyterian Hospital   (United States)

^e SAIC FREDERICK INC   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; BRCA1 PROTEIN; MESSENGER RNA; MUTANT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN; PROTEIN CTIP; PROTEIN KAP 1; PROTEIN P53; PROTEIN S327A; PROTEIN T847A; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL CYCLE; CELL DIVISION; CELL PROLIFERATION; CHROMOSOME ABERRATION; DNA DAMAGE; DNA END RESECTION; EMBRYO DEATH; EMBRYO DEVELOPMENT; EMBRYONIC VIABILTIY; GENOME; GENOMIC INSTABILITY; IMMUNOFLUORESCENCE; LETHALITY; METAPHASE; MOUSE; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SYSTEMATIC REVIEW;

ANIMALS; B-LYMPHOCYTES; BRCA1 PROTEIN; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; ENZYME INHIBITORS; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; IMMUNOBLOTTING; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MUTATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING;

EID: 84901766946     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131939     Document Type: Article

References (47)

1. Bothmer, A., P.C. Rommel, A. Gazumyan, F. Polato, C.R. Reczek, M.F. Muellenbeck, S. Schaetzlein, W. Edelmann, P.L. Chen, R.M. Brosh Jr., et al. 2013. Mechanism of DNA resection during intrachromosomal recombination and immunoglobulin class switching. J. Exp. Med. 210:115-123. http://dx.doi.org/10.1084/jem.20121975.
2. Bouwman, P., A. Aly, J.M. Escandell, M. Pieterse, J. Bartkova, H. van der Gulden, S. Hiddingh, M. Thanasoula, A. Kulkarni, Q. Yang, et al. 2010. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17:688-695. http://dx.doi.org/10.1038/nsmb.1831.
3. Bryant, H.E., N. Schultz, H.D. Thomas, K.M. Parker, D. Flower, E. Lopez, S. Kyle, M. Meuth, N.J. Curtin, and T. Helleday. 2005. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 434:913-917. http://dx.doi.org/10.1038/nature03443.
4. Bunting, S.F., and A. Nussenzweig. 2013. End-joining, translocations and cancer. Nat. Rev. Cancer. 13:443-454. http://dx.doi.org/10.1038/nrc3537.
5. Bunting, S.F., E. Callén, N. Wong, H.T. Chen, F. Polato, A. Gunn, A. Bothmer, N. Feldhahn, O. Fernandez-Capetillo, L. Cao, et al. 2010. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 141:243-254. http://dx.doi.org/ 10.1016/j.cell.2010.03.012.
6. Bunting, S.F., E. Callén, M.L. Kozak, J.M. Kim, N. Wong, A.J. López-Contreras, T. Ludwig, R. Baer, R.B. Faryabi, A. Malhowski, et al. 2012. BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol. Cell. 46:125-135. http://dx.doi.org/10.1016/j.molcel.2012.02.015.
7. Callen, E., M. Di Virgilio, M.J. Kruhlak, M. Nieto-Soler, N. Wong, H.T. Chen, R.B. Faryabi, F. Polato, M. Santos, L.M. Starnes, et al. 2013. 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell. 153:1266-1280. http://dx.doi.org/ 10.1016/j.cell.2013.05.023.
8. Cao, L., X. Xu, S.F. Bunting, J. Liu, R.H. Wang, L.L. Cao, J.J. Wu, T.N. Peng, J. Chen, A. Nussenzweig, et al. 2009. A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol. Cell. 35:534-541. http://dx.doi.org/10.1016/ j.molcel.2009.06.037.
9. Celeste, A., O. Fernandez-Capetillo, M.J. Kruhlak, D.R. Pilch, D.W. Staudt, A. Lee, R.F. Bonner, W.M. Bonner, and A. Nussenzweig. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675-679. http://dx.doi.org/ 10.1038/ncb1004.
10. Chandramouly, G., A. Kwok, B. Huang, N.A. Willis, A. Xie, and R. Scully. 2013. BRCA1 and CtIP suppress long-tract gene conversion between sister chromatids. Nat Commun. 4:2404. http://dx.doi.org/10.1038/ncomms3404.
11. Chapman, J.R., A.J. Sossick, S.J. Boulton, and S.P. Jackson. 2012. BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair. J. Cell Sci. 125:3529-3534. http://dx.doi.org/10.1242/jcs.105353.
12. Chapman, J.R., P. Barral, J.B. Vannier, V. Borel, M. Steger, A. Tomas-Loba, A.A. Sartori, I.R. Adams, F.D. Batista, and S.J. Boulton. 2013. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell. 49:858-871. http://dx.doi.org/10.1016/j.molcel.2013.01.002.
13. Chen, P.L., F. Liu, S. Cai, X. Lin, A. Li, Y. Chen, B. Gu, E.Y. Lee, and W.H. Lee. 2005. Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol. Cell. Biol. 25:3535-3542. http://dx.doi.org/10.1128/MCB.25.9.3535-3542.2005.
14. Chen, L., C.J. Nievera, A.Y. Lee, and X. Wu. 2008. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA doublestrand break repair. J. Biol. Chem. 283:7713-7720. http://dx.doi.org/10.1074/jbc.M710245200.
15. Difilippantonio, S., A. Celeste, O. Fernandez-Capetillo, H.T. Chen, B. Reina San Martin, F. Van Laethem, Y.P. Yang, G.V. Petukhova, M. Eckhaus, L. Feigenbaum, et al. 2005. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat. Cell Biol. 7:675-685. http://dx.doi.org/10.1038/ncb1270.
16. Eid, W., M. Steger, M. El-Shemerly, L.P. Ferretti, J. Peña-Diaz, C. König, E. Valtorta, A.A. Sartori, and S. Ferrari. 2010. DNA end resection by CtIP and exonuclease 1 prevents genomic instability. EMBO Rep. 11:962-968. http://dx.doi.org/10.1038/embor.2010.157.
17. Escribano-Díaz, C., A. Orthwein, A. Fradet-Turcotte, M. Xing, J.T. Young, J. Tkác, M.A. Cook, A.P. Rosebrock, M. Munro, M.D. Canny, et al. 2013. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell. 49:872-883. http://dx.doi.org/10.1016/j.molcel.2013.01.001.
18. Farmer, H., N. McCabe, C.J. Lord, A.N. Tutt, D.A. Johnson, T.B. Richardson, M. Santarosa, K.J. Dillon, I. Hickson, C. Knights, et al. 2005. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 434:917-921. http://dx.doi.org/10.1038/nature03445.
19. Feng, L., K.W. Fong, J. Wang, W. Wang, and J. Chen. 2013. RIF1 counteracts BRCA1-mediated end resection during DNA repair. J. Biol. Chem. 288:11135-11143. http://dx.doi.org/10.1074/jbc.M113.457440.
20. Ferretti, L.P., L. Lafranchi, and A.A. Sartori. 2013. Controlling DNA-end resection: a new task for CDKs. Front Genet. 4:99. http://dx.doi.org/10.3389/fgene.2013.00099.
21. Helmink, B.A., A.T. Tubbs, Y. Dorsett, J.J. Bednarski, L.M. Walker, Z. Feng, G.G. Sharma, P.J. McKinnon, J. Zhang, C.H. Bassing, and B.P. Sleckman. 2011. H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes. Nature. 469:245-249. http://dx.doi.org/10.1038/nature09585.
22. Huertas, P., and S.P. Jackson. 2009. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 284:9558-9565. http://dx.doi.org/10.1074/jbc.M808906200.
23. Jackson, S.P., and J. Bartek. 2009. The DNA-damage response in human biology and disease. Nature. 461:1071-1078. http://dx.doi.org/10.1038/ nature08467.
24. Langerak, P., E. Mejia-Ramirez, O. Limbo, and P. Russell. 2011. Release of Ku and MRN from DNA ends by Mre11 nuclease activity and Ctp1 is required for homologous recombination repair of double-strand breaks. PLoS Genet. 7:e1002271. http://dx.doi.org/10.1371/journal.pgen.1002271.
25. Li, M.L., and R.A. Greenberg. 2012. Links between genome integrity and BRCA1 tumor suppression. Trends Biochem. Sci. 37:418-424. http:// dx.doi.org/10.1016/j.tibs.2012.06.007.
26. Moynahan, M.E., J.W. Chiu, B.H. Koller, and M. Jasin. 1999. Brca1 controls homology-directed DNA repair. Mol. Cell. 4:511-518. http:// dx.doi.org/10.1016/S1097-2765(00)80202-6.
27. Nakamura, K., T. Kogame, H. Oshiumi, A. Shinohara, Y. Sumitomo, K. Agama, Y. Pommier, K.M. Tsutsui, K. Tsutsui, E. Hartsuiker, et al. 2010. Collaborative action of Brca1 and CtIP in elimination of covalent modifications from double-strand breaks to facilitate subsequent break repair. PLoS Genet. 6:e1000828. http://dx.doi.org/10.1371/journal.pgen.1000828.
28. Nussenzweig, A., C. Chen, V. da Costa Soares, M. Sanchez, K. Sokol, M.C. Nussenzweig, and G.C. Li. 1996. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature. 382:551-555. http:// dx.doi.org/10.1038/382551a0.
29. Peterson, S.E., Y. Li, B.T. Chait, M.E. Gottesman, R. Baer, and J. Gautier. 2011. Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J. Cell Biol. 194:705-720. http://dx.doi.org/10.1083/jcb.201103103.
30. Peterson, S.E., Y. Li, F. Wu-Baer, B.T. Chait, R. Baer, H. Yan, M.E. Gottesman, and J. Gautier. 2013. Activation of DSB processing requires phosphorylation of CtIP by ATR. Mol. Cell. 49:657-667. http://dx.doi.org/10.1016/j.molcel.2012.11.020.
31. Reczek, C.R., M. Szabolcs, J.M. Stark, T. Ludwig, and R. Baer. 2013. The interaction between CtIP and BRCA1 is not essential for resectionmediated DNA repair or tumor suppression. J. Cell Biol. 201:693-707. http://dx.doi.org/10.1083/jcb.201302145.
32. Rickert, R.C., J. Roes, and K. Rajewsky. 1997. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 25:1317-1318. http://dx.doi.org/10.1093/nar/25.6.1317.
33. Sartori, A.A., C. Lukas, J. Coates, M. Mistrik, S. Fu, J. Bartek, R. Baer, J. Lukas, and S.P. Jackson. 2007. Human CtIP promotes DNA end resection. Nature. 450:509-514. http://dx.doi.org/10.1038/nature06337.
34. Shakya, R., L.J. Reid, C.R. Reczek, F. Cole, D. Egli, C.S. Lin, D.G. deRooij, S. Hirsch, K. Ravi, J.B. Hicks, et al. 2011. BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science. 334:525-528. http://dx.doi.org/10.1126/science.1209909.
35. Silver, D.P., and D.M. Livingston. 2012. Mechanisms of BRCA1 tumor suppression. Cancer Discov. 2:679-684. http://dx.doi.org/10.1158/2159-8290.CD-12-0221.
36. Srinivas, S., T. Watanabe, C.S. Lin, C.M. William, Y. Tanabe, T.M. Jessell, and F. Costantini. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1:4. http://dx.doi.org/10.1186/1471-213X-1-4.
37. Stark, J.M., A.J. Pierce, J. Oh, A. Pastink, and M. Jasin. 2004. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol. Cell. Biol. 24:9305-9316. http://dx.doi.org/10.1128/ MCB.24.21.9305-9316.2004.
38. Symington, L.S., and J. Gautier. 2011. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45:247-271. http://dx.doi.org/10.1146/annurev-genet-110410-132435.
39. Ward, I.M., B. Reina-San-Martin, A. Olaru, K. Minn, K. Tamada, J.S. Lau, M. Cascalho, L. Chen, A. Nussenzweig, F. Livak, et al. 2004. 53BP1 is required for class switch recombination. J. Cell Biol. 165:459-464. http://dx.doi.org/10.1083/jcb.200403021.
40. Wei, K., A.B. Clark, E. Wong, M.F. Kane, D.J. Mazur, T. Parris, N.K. Kolas, R. Russell, H. Hou Jr., B. Kneitz, et al. 2003. Inactivation of exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev. 17:603-614. http://dx.doi.org/10.1101/gad.1060603.
41. Wong, A.K., P.A. Ormonde, R. Pero, Y. Chen, L. Lian, G. Salada, S. Berry, Q. Lawrence, P. Dayananth, P. Ha, et al. 1998. Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene. 17:2279-2285. http://dx.doi.org/10.1038/sj.onc.1202150.
42. Yamane, A., D.F. Robbiani, W. Resch, A. Bothmer, H. Nakahashi, T. Oliveira, P.C. Rommel, E.J. Brown, A. Nussenzweig, M.C. Nussenzweig, and R. Casellas. 2013. RPA accumulation during class switch recombination represents 5'-3' DNA-end resection during the S-G2/M phase of the cell cycle. Cell Rep. 3:138-147. http://dx.doi.org/10.1016/j.celrep.2012.12.006.
43. You, Z., L.Z. Shi, Q. Zhu, P. Wu, Y.W. Zhang, A. Basilio, N. Tonnu, I.M. Verma, M.W. Berns, and T. Hunter. 2009. CtIP links DNA doublestrand break sensing to resection. Mol. Cell. 36:954-969. http://dx.doi.org/10.1016/j.molcel.2009.12.002.
44. Yu, X., and J. Chen. 2004. DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24:9478-9486. http:// dx.doi.org/10.1128/MCB.24.21.9478-9486.2004.
45. Yu, X., 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. 273:25388-25392. http://dx.doi.org/10.1074/jbc.273.39.25388.
46. Yun, M.H., and K. Hiom. 2009. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature. 459:460-463. http://dx.doi.org/10.1038/nature07955.
47. Zimmermann, M., F. Lottersberger, S.B. Buonomo, A. Sfeir, and T. de Lange. 2013. 53BP1 regulates DSB repair using Rif1 to control 5' end resection. Science. 339:700-704. http://dx.doi.org/10.1126/science.1231573.