CtIP and MRN promote non-homologous end-joining of etoposide-induced DNA double-strand breaks in G1

Nucleic Acids Research

Volumn 39, Issue 6, 2011, Pages 2144-2152

  Quennet, Verena ^a   Beucher, Andrea ^a   Barton, Olivia ^a   Takeda, Shunichi ^b   Löbrich, Markus ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARBOXY TERMINAL BINDING PROTEIN INTERACTING PROTEIN; ETOPOSIDE; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETIC PARAMETERS; HUMAN; HUMAN CELL; NON HOMOLOGOUS END JOINING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; ETOPOSIDE; G1 PHASE; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; THREONINE;

MAMMALIA; SCHIZOSACCHAROMYCETACEAE;

EID: 79953708229     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq1175     Document Type: Article

References (65)

1. Jeggo,P.A. and Lobrich,M. (2007) DNA double-strand breaks: their cellular and clinical impact? Oncogene, 26, 7717-7719.
2. Lobrich,M. and Jeggo,P.A. (2007) The impact of a negligent G2/ M checkpoint on genomic instability and cancer induction. Nat. Rev. Cancer, 7, 861-869.
3. van Gent,D.C. and Hoeijmakers,J.H. (2009) DNA double strand break repair: zooming in on the focus. Cell Cycle, 8, 3813-3815.
4. Mansour,W.Y., Schumacher,S., Rosskopf,R., Rhein,T., Schmidt- Petersen,F., Gatzemeier,F., Haag,F., Borgmann,K., Willers,H. and Dahm-Daphi,J. (2008) Hierarchy of nonhomologous end-joining, single-strand annealing and gene conversion at site-directed DNA double-strand breaks. Nucleic Acids Res., 36, 4088-4098. (Pubitemid 351984824)
5. Wyman,C. and Kanaar,R. (2006) DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet., 40, 363-383.
6. Chen,B.P., Chan,D.W., Kobayashi,J., Burma,S., Asaithamby,A., Morotomi-Yano,K., Botvinick,E., Qin,J. and Chen,D.J. (2005) Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem., 280, 14709-14715.
7. Weterings,E. and Chen,D.J. (2007) DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J. Cell Biol., 179, 183-186. (Pubitemid 350004882)
8. Rothkamm,K., Kruger,I., Thompson,L.H. and Lobrich,M. (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell Biol., 23, 5706-5715.
9. Arnaudeau,C., Lundin,C. and Helleday,T. (2001) DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol., 307, 1235-1245.
10. Helleday,T., Lo,J., van Gent,D.C. and Engelward,B.P. (2007) DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair, 6, 923-935. (Pubitemid 46880473)
11. Beucher,A., Birraux,J., Tchouandong,L., Barton,O., Shibata,A., Conrad,S., Goodarzi,A.A., Krempler,A., Jeggo,P.A. and Lobrich,M. (2009) ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J., 28, 3413-3427.
12. Tauchi,H., Kobayashi,J., Morishima,K., van Gent,D.C., Shiraishi,T., Verkaik,N.S., vanHeems,D., Ito,E., Nakamura,A., Sonoda,E. et al. (2002) Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature, 420, 93-98.
13. Uziel,T., Lerenthal,Y., Moyal,L., Andegeko,Y., Mittelman,L. and Shiloh,Y. (2003) Requirement of the MRN complex for ATM activation by DNA damage. EMBO J., 22, 5612-5621. (Pubitemid 37279970)
14. Trujillo,K.M. and Sung,P. (2001) DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex. J. Biol. Chem., 276, 35458-35464.
15. Shrivastav,M., De Haro,L.P. and Nickoloff,J.A. (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res., 18, 134-147.
16. Riballo,E., Kuhne,M., Rief,N., Doherty,A., Smith,G.C., Recio,M.J., Reis,C., Dahm,K., Fricke,A., Krempler,A. et al. (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell, 16, 715-724.
17. Goodarzi,A.A., Noon,A.T., Deckbar,D., Ziv,Y., Shiloh,Y., Lobrich,M. and Jeggo,P.A. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell, 31, 167-177.
18. Robison,J.G., Dixon,K. and Bissler,J.J. (2007) Cell cycle-and proteasome-dependent formation of etoposide-induced replication protein A (RPA) or Mre11/Rad50/Nbs1 (MRN) complex repair foci. Cell Cycle, 6, 2399-2407. (Pubitemid 350058693)
19. Schaeper,U., Subramanian,T., Lim,L., Boyd,J.M. and Chinnadurai,G. (1998) Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J. Biol. Chem., 273, 8549-8552.
20. Chen,L., Nievera,C.J., Lee,A.Y. and Wu,X. (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem., 283, 7713-7720.
21. Yu,X. and Chen,J. (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.
22. Sartori,A.A., Lukas,C., Coates,J., Mistrik,M., Fu,S., Bartek,J., Baer,R., Lukas,J. and Jackson,S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514. (Pubitemid 350190253)
23. Huertas,P. and Jackson,S.P. (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem., 284, 9558-9565.
24. Yun,M.H. and Hiom,K. (2009) CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature, 459, 460-463.
25. Nitiss,J.L. (1998) Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta, 1400, 63-81.
26. Wang,L. and Eastmond,D.A. (2002) Catalytic inhibitors of topoisomerase II are DNA-damaging agents: induction of chromosomal damage by merbarone and ICRF-187. Environ. Mol. Mutagen., 39, 348-356.
27. Champoux,J.J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 70, 369-413.
28. Chen,A.Y. and Liu,L.F. (1994) DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol., 34, 191-218.
29. Chen,G.L., Yang,L., Rowe,T.C., Halligan,B.D., Tewey,K.M. and Liu,L.F. (1984) Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem., 259, 13560-13566.
30. Hartsuiker,E., Neale,M.J. and Carr,A.M. (2009) Distinct requirements for the Rad32(Mre11) nuclease and Ctp1(CtIP) in the removal of covalently bound topoisomerase I and II from DNA. Mol. Cell, 33, 117-123.
31. Nakamura,K., Kogame,T., Oshiumi,H., Shinohara,A., Sumitomo,Y., Agama,K., Pommier,Y., Tsutsui,K.M., Tsutsui,K., Hartsuiker,E. 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.
32. Adachi,N., Suzuki,H., Iiizumi,S. and Koyama,H. (2003) Hypersensitivity of nonhomologous DNA end-joining mutants to VP-16 and ICRF-193: implications for the repair of topoisomerase II-mediated DNA damage. J. Biol. Chem., 278, 35897-35902.
33. Adachi,N., Iiizumi,S., So,S. and Koyama,H. (2004) Genetic evidence for involvement of two distinct nonhomologous end-joining pathways in repair of topoisomerase II-mediated DNA damage. Biochem. Biophys. Res. Commun., 318, 856-861.
34. Malik,M., Nitiss,K.C., Enriquez-Rios,V. and Nitiss,J.L. (2006) Roles of nonhomologous end-joining pathways in surviving topoisomerase II-mediated DNA damage. Mol. Cancer Ther., 5, 1405-1414.
35. Howlett,N.G., Taniguchi,T., Olson,S., Cox,B., Waisfisz,Q., Die-Smulders,C., Persky,N., Grompe,M., Joenje,H., Pals,G. et al. (2002) Biallelic inactivation of BRCA2 in Fanconi anemia. Science, 297, 606-609. (Pubitemid 34815345)
36. Riballo,E., Critchlow,S.E., Teo,S.H., Doherty,A.J., Priestley,A., Broughton,B., Kysela,B., Beamish,H., Plowman,N., Arlett,C.F. et al. (1999) Identification of a defect in DNA ligase IV in a radiosensitive leukaemia patient. Curr. Biol., 9, 699-702.
37. Kegel,P., Riballo,E., Kuhne,M., Jeggo,P.A. and Lobrich,M. (2007) X-irradiation of cells on glass slides has a dose doubling impact. DNA Repair, 6, 1692-1697. (Pubitemid 47610758)
38. Caldecott,K., Banks,G. and Jeggo,P. (1990) DNA double-strand break repair pathways and cellular tolerance to inhibitors of topoisomerase II. Cancer Res., 50, 5778-5783. (Pubitemid 20331376)
39. Jensen,P.B., Sorensen,B.S., Demant,E.J., Sehested,M., Jensen,P.S., Vindelov,L. and Hansen,H.H. (1990) Antagonistic effect of aclarubicin on the cytotoxicity of etoposide and 4′-(9-acridinylamino)methanesulfon-m- anisidide in human small cell lung cancer cell lines and on topoisomerase II-mediated DNA cleavage. Cancer Res., 50, 3311-3316. (Pubitemid 20190137)
40. Petersen,L.N., Jensen,P.B., Sorensen,B.S., Engelholm,S.A. and Spang-Thomsen,M. (1994) Postincubation with aclarubicin reverses topoisomerase II mediated DNA cleavage, strand breaks, and cytotoxicity induced by VP-16. Invest. New Drugs, 12, 289-297.
41. Shibata,A., Barton,O., Noon,A.T., Dahm,K., Deckbar,D., Goodarzi,A.A., Lobrich,M. and Jeggo,P.A. (2010) Role of ATM and the damage response mediator proteins 53BP1 and MDC1 in the maintenance of G(2)/M checkpoint arrest. Mol. Cell Biol., 30, 3371-3383.
42. Shivji,M.K. and Venkitaraman,A.R. (2004) DNA recombination, chromosomal stability and carcinogenesis: insights into the role of BRCA2. DNA Repair, 3, 835-843. (Pubitemid 38997925)
43. Ahnesorg,P., Smith,P. and Jackson,S.P. (2006) XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell, 124, 301-313. (Pubitemid 43121979)
44. Dai,Y., Kysela,B., Hanakahi,L.A., Manolis,K., Riballo,E., Stumm,M., Harville,T.O., West,S.C., Oettinger,M.A. and Jeggo,P.A. (2003) Nonhomologous end joining and V(D)J recombination require an additional factor. Proc. Natl Acad. Sci. USA, 100, 2462-2467.
45. Aylon,Y., Liefshitz,B. and Kupiec,M. (2004) The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J., 23, 4868-4875. (Pubitemid 40069716)
46. Ira,G., Pellicioli,A., Balijja,A., Wang,X., Fiorani,S., Carotenuto,W., Liberi,G., Bressan,D., Wan,L., Hollingsworth,N.M. et al. (2004) DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature, 431, 1011-1017. (Pubitemid 39434425)
47. De Azevedo,W.F., Leclerc,S., Meijer,L., Havlicek,L., Strnad,M. and Kim,S.H. (1997) Inhibition of cyclin-dependent kinases by purine analogues: crystal structure of human cdk2 complexed with roscovitine. Eur. J. Biochem., 243, 518-526.
48. Huertas,P., Cortes-Ledesma,F., Sartori,A.A., Aguilera,A. and Jackson,S.P. (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature, 455, 689-692.
49. Lengsfeld,B.M., Rattray,A.J., Bhaskara,V., Ghirlando,R. and Paull,T.T. (2007) Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell, 28, 638-651.
50. Connelly,J.C. and Leach,D.R. (2004) Repair of DNA covalently linked to protein. Mol. Cell, 13, 307-316.
51. Montecucco,A. and Biamonti,G. (2007) Cellular response to etoposide treatment. Cancer Lett., 252, 9-18. (Pubitemid 46734551)
52. Campos-Nebel,M., Larripa,I. and Gonzalez-Cid,M. (2010) Topoisomerase II-mediated DNA damage is differently repaired during the cell cycle by non-homologous end joining and homologous recombination. PLoS One, 5.
53. Deckbar,D., Birraux,J., Krempler,A., Tchouandong,L., Beucher,A., Walker,S., Stiff,T., Jeggo,P. and Lobrich,M. (2007) Chromosome breakage after G2 checkpoint release. J. Cell Biol., 176, 749-755. (Pubitemid 46425534)
54. Deckbar,D., Stiff,T., Koch,B., Reis,C., Lobrich,M. and Jeggo,P.A. (2010) The limitations of the G1-S checkpoint. Cancer Res., 70, 4412-4421.
55. Krempler,A., Deckbar,D., Jeggo,P.A. and Lobrich,M. (2007) An imperfect G2M checkpoint contributes to chromosome instability following irradiation of S and G2 phase cells. Cell Cycle, 6, 1682-1686. (Pubitemid 47327917)
56. Kinner,A., Wu,W., Staudt,C. and Iliakis,G. (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res., 36, 5678-5694.
57. Lobrich,M., Shibata,A., Beucher,A., Fisher,A., Ensminger,M., Goodarzi,A.A., Barton,O. and Jeggo,P.A. (2010) gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle, 9, 662-669.
58. Buis,J., Wu,Y., Deng,Y., Leddon,J., Westfield,G., Eckersdorff,M., Sekiguchi,J.M., Chang,S. and Ferguson,D.O. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell, 135, 85-96.
59. Neale,M.J., Pan,J. and Keeney,S. (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature, 436, 1053-1057. (Pubitemid 41191692)
60. Di Virgilio,M. and Gautier,J. (2005) Repair of double-strand breaks by nonhomologous end joining in the absence of Mre11. J. Cell Biol., 171, 765-771. (Pubitemid 41746579)
61. Huang,J. and Dynan,W.S. (2002) Reconstitution of the mammalian DNA double-strand break end-joining reaction reveals a requirement for an Mre11/Rad50/NBS1-containing fraction. Nucleic Acids Res., 30, 667-674. (Pubitemid 34679631)
62. Cortes,L.F., El Khamisy,S.F., Zuma,M.C., Osborn,K. and Caldecott,K.W. (2009) A human 5'-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature, 461, 674-678.
63. Hartsuiker,E., Mizuno,K., Molnar,M., Kohli,J., Ohta,K. and Carr,A.M. (2009) Ctp1CtIP and Rad32Mre11 nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions. Mol. Cell. Biol., 29, 1671-1681.
64. Zhu,Z., Chung,W.H., Shim,E.Y., Lee,S.E. and Ira,G. (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell, 134, 981-994.
65. Yu,X. and Baer,R. (2000) Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J. Biol. Chem., 275, 18541-18549.