Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells

Nature Structural and Molecular Biology

Volumn 16, Issue 8, 2009, Pages 819-824

  Rass, Emilie ^a   Grabarz, Anastazja ^a   Plo, Isabelle ^a   Gautier, Jean ^b   Bertrand, Pascale ^a   Lopez, Bernard S ^a  

^a DIF   (France)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; MRE11 PROTEIN; NIBRIN; NUCLEASE; RAD50 PROTEIN; SINGLE STRANDED DNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA REPAIR; ENZYME ACTIVITY; GENE REARRANGEMENT; HUMAN; HUMAN CELL; MAMMAL CELL; NONHOMOLOGOUS END JOINING PATHWAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; FLOW CYTOMETRY; HUMANS; MICROSCOPY, FLUORESCENCE; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINONES; RECOMBINATION, GENETIC; RNA, SMALL INTERFERING; THIONES; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA; MAMMALIA;

EID: 68249138694     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1641     Document Type: Article

References (63)

1. Allen, C., Kurimasa, A., Brenneman, M.A., Chen, D.J. & Nickoloff, J.A. DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. USA 99, 3758-3763 (2002).
2. Delacôte, F., Han, M., Stamato, T.D., Jasin, M. & Lopez, B.S. An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by doublestrand breaks in mammalian cells. Nucleic Acids Res. 30, 3454-3463 (2002).
3. Pierce, A.J., Hu, P., Han, M., Ellis, N. & Jasin, M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242 (2001).
4. Chen, J.M., Cooper, D.N., Chuzhanova, N., Ferec, C. & Patrinos, G.P. Gene conversion: mechanisms, evolution and human disease. Nat. Rev. Genet. 8, 762-775 (2007).
5. Purandare, S.M. & Patel, P.I. Recombination hot spots and human disease. Genome Res. 7, 773-786 (1997).
6. Guirouilh-Barbat, J. et al. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol. Cell 14, 611-623 (2004).
7. Michel, B. et al. Rescue of arrested replication forks by homologous recombination. Proc. Natl. Acad. Sci. USA 98, 8181-8188 (2001).
8. Saintigny, Y. et al. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20, 3861-3870 (2001).
9. Couëdel, C. et al. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev 18, 1293-1304 (2004).
10. Mills, K.D. et al. Rad54 and DNA ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev. 18, 1283-1292 (2004).
11. Bartkova, J. et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870 (2005).
12. Gorgoulis, V.G. et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913 (2005).
13. Audebert, M., Salles, B. & Calsou, P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 279, 55117-55126 (2004).
14. Corneo, B. et al. Rag mutations reveal robust alternative end joining. Nature 449, 483-486 (2007).
15. Guirouilh-Barbat, J., Rass, E., Plo, I., Bertrand, P. & Lopez, B.S. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl. Acad. Sci. USA 104, 20902-20907 (2007).
16. McVey, M. & Lee, S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 24, 529-538 (2008).
17. Soulas-Sprauel, P. et al. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 204, 1717-1727 (2007).
18. Wang, H., Perrault, A.R., Takeda, Y., Qin, W. & Iliakis, G. Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res. 31, 5377-5388 (2003).
19. Yan, C.T. et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449, 478-482 (2007).
20. Gao, Y. et al. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 404, 897-900 (2000).
21. Weinstock, D.M., Brunet, E. & Jasin, M. Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol. 9, 978-981 (2007).
22. Boulton, S.J. & Jackson, S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17, 1819-1828 (1998).
23. Moore, J.K. & Haber, J.E. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 2164-2173 (1996).
24. Zhang, X. & Paull, T.T. The Mre11/Rad50/Xrs2 complex and non-homologous end-joining of incompatible ends in S. cerevisiae. DNA Repair (Amst.) 4, 1281-1294 (2005).
25. Ma, J.L., Kim, E.M., Haber, J.E. & Lee, S.E. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23, 8820-8828 (2003).
26. Mimitou, E.P. & Symington, L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774 (2008).
27. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E. & Ira, G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994 (2008).
28. Lee, J.H. & Paull, T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304, 93-96 (2004).
29. Di Virgilio, M. & Gautier, J. Repair of double-strand breaks by nonhomologous end joining in the absence of Mre11. J. Cell Biol. 171, 765-771 (2005).
30. Huang, J. & Dynan, W.S. 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 (2002).
31. Deriano, L., Stracker, T.H., Baker, A., Petrini, J.H. & Roth, D.B. Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Mol. Cell 34, 13-25 (2009).
32. Helmink, B.A. et al. MRN complex function in the repair of chromosomal Rag-mediated DNA double-strand breaks. J. Exp. Med. 206, 669-679 (2009).
33. de Jager, M. et al. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8, 1129-1135 (2001).
34. Buis, J. et al. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135, 85-96 (2008).
35. Williams, R.S. et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135, 97-109 (2008).
36. Ira, G. et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431, 1011-1017 (2004).
37. Jazayeri, A. et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45 (2006).
38. Chen, L., Nievera, C.J., Lee, A.Y. & Wu, X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem. 283, 7713-7720 (2008).
39. Lee, K. & Lee, S.E. Saccharomyces cerevisiae Sae2- and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 176, 2003-2014 (2007).
40. Lengsfeld, B.M., Rattray, A.J., Bhaskara, V., Ghirlando, R. & Paull, T.T. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28, 638-651 (2007).
41. Limbo, O. et al. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28, 134-146 (2007).
42. Sartori, A.A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
43. Dupré, A. et al. A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat. Chem. Biol. 4, 119-125 (2008).
44. Lee, J.H. & Paull, T.T. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26, 7741-7748 (2007).
45. Farah, J.A., Cromie, G., Steiner, W.W. & Smith, G.R. A novel recombination pathway initiated by the Mre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe. Genetics 169, 1261-1274 (2005).
46. Neale, M.J., Pan, J. & Keeney, S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436, 1053-1057 (2005).
47. Paull, T.T. & Gellert, M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1, 969-979 (1998).
48. Hartsuiker, E. et al. Ctp1CtIP and the 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 (2009).
49. Dinkelmann, M. et al. Multiple functions of MRN in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol. advance online publication, doi:10.1038/nsmb.1639 (26 July 2009).
50. Deng, Y., Guo, X., Ferguson, D.O. & Chang, S. Multiple roles for Mre11 at uncapped telomeres. Nature advance online publication, doi:10.1038/naturexxx (26 July 2009).
51. Xie, A., Kwok, A. & Scully, R. Role of mammalian Mre11 in classical and alternative non-homologous end joining. Nat. Struct. Mol. Biol. advance online publication, doi:10.1038/nsmb.1640 (26 July 2009).
52. Haince, J.F. et al. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem. 283, 1197-1208 (2008).
53. Wang, M. et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 34, 6170-6182 (2006).
54. Huertas, P., Cortes-Ledesma, F., Sartori, A.A., Aguilera, A. & Jackson, S.P. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455, 689-692 (2008).
55. Johnson, R.D. & Jasin, M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19, 3398-3407 (2000).
56. Saintigny, Y., Delacote, F., Boucher, D., Averbeck, D. & Lopez, B.S. XRCC4 in G1 suppresses homologous recombination in S/G2, in G1 checkpoint-defective cells. Oncogene 26, 2769-2780 (2007).
57. Paull, T.T., Cortez, D., Bowers, B., Elledge, S.J. & Gellert, M. Direct DNA binding by Brca1. Proc. Natl. Acad. Sci. USA 98, 6086-6091 (2001).
58. Baldeyron, C. et al. A single mutated BRCA1 allele leads to impaired fidelity of double strand break end-joining. Oncogene 21, 1401-1410 (2002).
59. Zhong, Q., Boyer, T.G., Chen, P.L. & Lee, W.H. Deficient nonhomologous end-joining activity in cell-free extracts from Brca1-null fibroblasts. Cancer Res. 62, 3966-3970 (2002).
60. Guirouilh-Barbat, J., Huck, S. & Lopez, B.S. S-phase progression stimulates both the mutagenic KU-independent pathway and mutagenic processing of KU-dependent intermediates, for nonhomologous end joining. Oncogene 27, 1726-1736 (2008).
61. Ausubel, F. et al. Current Protocols in Molecular Biology (John Wiley & Sons, Inc., Boston, 1999).
62. Liang, F., Han, M., Romanienko, P.J. & Jasin, M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA 95, 5172-5177 (1998).
63. Yu, X. & Chen, J. 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 (2004).