NBS1 cooperates with homologous recombination to counteract chromosome breakage during replication

DNA Repair

Volumn 8, Issue 12, 2009, Pages 1363-1370

  Brugmans, Linda ^a   Verkaik, Nicole S ^a   Kunen, Maurice ^a   van Drunen, Ellen ^a   Williams, Bret R ^b   Petrini, John H J ^b   Kanaar, Roland ^a   Essers, Jeroen ^a   van Gent, Dik C ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b Weill Cornell Medical Center   (United States)

Author keywords

Cell cycle checkpoint; Chromosomal instability; DNA damage response; DNA double strand break repair; MRE11 RAD50 NBS1 complex; RAD54

Indexed keywords

CAMPTOTHECIN; DOUBLE STRANDED DNA; MITOMYCIN C; MRE11 PROTEIN; NIBRIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; RAD50 PROTEIN; RAD54 PROTEIN;

ANIMAL CELL; ARTICLE; CANCER SUSCEPTIBILITY; CELL CYCLE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CYTOGENETICS; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; EMBRYO; EMBRYONIC STEM CELL; GAMMA IRRADIATION; GENE MUTATION; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; MOUSE; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; SISTER CHROMATID EXCHANGE; WESTERN BLOTTING;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMOSOME BREAKAGE; DNA; DNA DAMAGE; DNA REPLICATION; FEMALE; MICE; NIJMEGEN BREAKAGE SYNDROME; NUCLEAR PROTEINS; RECOMBINATION, GENETIC;

EID: 70450223903     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.09.002     Document Type: Article

References (36)

1. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 411 (2001) 366-374
2. Helleday T., Lo J., van Gent D.C., and Engelward B.P. DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst.) 6 (2007) 923-935
3. van Gent D.C., Hoeijmakers J.H., and Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2 (2001) 196-206
4. Wyman C., and Kanaar R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40 (2006) 363-383
5. van Veelen L.R., Essers J., van de Rakt M.W., Odijk H., Pastink A., Zdzienicka M.Z., Paulusma C.C., and Kanaar R. Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat. Res. 574 (2005) 34-49
6. Lim D.S., and 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
7. Tsuzuki T., Fujii Y., Sakumi K., Tominaga Y., Nakao K., Sekiguchi M., Matsushiro A., Yoshimura Y., and 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
8. Essers J., Hendriks R.W., Swagemakers S.M., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H., and Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89 (1997) 195-204
9. Essers J., van Steeg H., de Wit J., Swagemakers S.M., Vermeij M., Hoeijmakers J.H., and Kanaar R. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J. 19 (2000) 1703-1710
10. Couedel C., Mills K.D., Barchi M., Shen L., Olshen A., Johnson R.D., Nussenzweig A., Essers J., Kanaar R., Li G.C., Alt F.W., and Jasin M. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev. 18 (2004) 1293-1304
11. Bartek J., Lukas C., and Lukas J. Checking on DNA damage in S phase. Nat. Rev. Mol. Cell Biol. 5 (2004) 792-804
12. Stracker T.H., Theunissen J.W., Morales M., and Petrini J.H. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst.) 3 (2004) 845-854
13. D'Amours D., and Jackson S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3 (2002) 317-327
14. Lavin M.F. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene 26 (2007) 7749-7758
15. Riballo E., Kuhne M., Rief N., Doherty A., Smith G.C., Recio M.J., Reis C., Dahm K., Fricke A., Krempler A., Parker A.R., Jackson S.P., Gennery A., Jeggo P.A., and Lobrich M. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16 (2004) 715-724
16. Painter R.B. Radioresistant DNA synthesis: an intrinsic feature of ataxia telangiectasia. Mutat. Res. 84 (1981) 183-190
17. Petrini J.H. The Mre11 complex and ATM: collaborating to navigate S phase. Curr. Opin. Cell. Biol. 12 (2000) 293-296
18. Stiff T., Reis C., Alderton G.K., Woodbine L., O'Driscoll M., and Jeggo P.A. Nbs1 is required for ATR-dependent phosphorylation events. EMBO J. 24 (2005) 199-208
19. Williams B.R., Mirzoeva O.K., Morgan W.F., Lin J., Dunnick W., and Petrini J.H. A murine model of Nijmegen breakage syndrome. Curr. Biol. 12 (2002) 648-653
20. Dahm-Daphi J., Sass C., and Alberti W. Comparison of biological effects of DNA damage induced by ionizing radiation and hydrogen peroxide in CHO cells. Int. J. Radiat. Biol. 76 (2000) 67-75
21. Desai S.D., Zhang H., Rodriguez-Bauman A., Yang J.M., Wu X., Gounder M.K., Rubin E.H., and Liu L.F. Transcription-dependent degradation of topoisomerase I-DNA covalent complexes. Mol. Cell. Biol. 23 (2003) 2341-2350
22. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., Martin N.M., Jackson S.P., Smith G.C., and Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434 (2005) 917-921
23. McCabe N., Turner N.C., Lord C.J., Kluzek K., Bialkowska A., Swift S., Giavara S., O'Connor J., Tutt M.A.N., Zdzienicka M.Z., Smith G.C., and Ashworth A. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res. 66 (2006) 8109-8115
24. Buscemi G., Carlessi L., Zannini L., Lisanti S., Fontanella E., Canevari S., and Delia D. DNA damage-induced cell cycle regulation and function of novel Chk2 phosphoresidues. Mol. Cell. Biol. 26 (2006) 7832-7845
25. Buscemi G., Savio C., Zannini L., Micciche F., Masnada D., Nakanishi M., Tauchi H., Komatsu K., Mizutani S., Khanna K., Chen P., Concannon P., Chessa L., and Delia D. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 21 (2001) 5214-5222
26. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., and Smith G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64 (2004) 9152-9159
27. Budzowska M., Jaspers I., Essers J., de Waard H., van Drunen E., Hanada K., Beverloo B., Hendriks R.W., de Klein A., Kanaar R., Hoeijmakers J.H., and Maas A. Mutation of the mouse Rad17 gene leads to embryonic lethality and reveals a role in DNA damage-dependent recombination. EMBO J. 23 (2004) 3548-3558
28. Costanzo V., Paull T., Gottesman M., and Gautier J. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2 (2004) E110
29. Mills K.D., Ferguson D.O., Essers J., Eckersdorff M., Kanaar R., and Alt F.W. Rad54 and DNA ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev. 18 (2004) 1283-1292
30. van Gent D.C., and van der Burg M. Non-homologous end-joining, a sticky affair. Oncogene 26 (2007) 7731-7740
31. Nelms B.E., Maser R.S., MacKay J.F., Lagally M.G., and Petrini J.H. In situ visualization of DNA double-strand break repair in human fibroblasts. Science 280 (1998) 590-592
32. de Jager M., van Noort J., van Gent D.C., Dekker C., Kanaar R., and Wyman C. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8 (2001) 1129-1135
33. Hopfner K.P., Craig L., Moncalian G., Zinkel R.A., Usui T., Owen B.A., Karcher A., Henderson B., Bodmer J.L., McMurray C.T., Carney J.P., Petrini J.H., and Tainer J.A. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418 (2002) 562-566
34. Essers J., Hendriks R.W., Wesoly J., Beerens C.E., Smit B., Hoeijmakers J.H., Wyman C., Dronkert M.L., and Kanaar R. Analysis of mouse Rad54 expression and its implications for homologous recombination. DNA Repair (Amst.) 1 (2002) 779-793
35. Dronkert M.L., Beverloo H.B., Johnson R.D., Hoeijmakers J.H., Jasin M., and Kanaar R. Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol. Cell. Biol. 20 (2000) 3147-3156
36. Jaspers N.G., and Zdzienicka M.Z. Inhibition of DNA synthesis by ionizing radiation: a marker for an S-phase checkpoint. Methods Mol. Biol. 314 (2006) 51-59