The fission yeast MRN complex tethers dysfunctional telomeres for NHEJ repair

EMBO Journal

Volumn 31, Issue 24, 2012, Pages 4576-4586

  Reis, Clara Correia ^a   Batista, Sílvia ^a   Ferreira, Miguel Godinho ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

DNA repair; fission yeast; MRN; NHEJ; telomeres

Indexed keywords

DNA; FISSION YEAST MRN PROTEIN; FUNGAL PROTEIN; METAL ION; MRE11 PROTEIN; NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; DNA END JOINING REPAIR; ENZYME ACTIVITY; LETHALITY; MUTANT; MUTATION; NONHUMAN; PRIORITY JOURNAL; TELOMERE;

CELL SURVIVAL; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA END-JOINING REPAIR; DNA PRIMERS; ELECTROPHORESIS, GEL, PULSED-FIELD; EXODEOXYRIBONUCLEASES; G1 PHASE; MULTIPROTEIN COMPLEXES; POLYMERASE CHAIN REACTION; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TELOMERE; TELOMERE-BINDING PROTEINS;

SCHIZOSACCHAROMYCETACEAE;

EID: 84871012289     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.313     Document Type: Article

References (41)

1. Boulton SJ, Jackson SP (1996) Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res 24: 4639-4648 (Pubitemid 26413339)
2. Boulton SJ, Jackson SP (1998) Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J 17: 1819-1828 (Pubitemid 28119135)
3. Carneiro T, Khair L, Reis CC, Borges V, Moser BA, Nakamura TM, Ferreira MG (2010) Telomeres avoid end detection by severing the checkpoint signal transduction pathway. Nature 467: 228-232
4. Celli GB, de Lange T (2005) DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat Cell Biol 7: 712-718 (Pubitemid 40975753)
5. Costanzo V, Robertson K, Bibikova M, Kim E, Grieco D, Gottesman M, Carroll D, Gautier J (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol Cell 8: 137-147 (Pubitemid 32772912)
6. Denchi EL, de Lange T (2007) Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448: 1068-1071 (Pubitemid 47345583)
7. Deng Y, Guo X, Ferguson DO, Chang S (2009) Multiple roles for MRE11 at uncapped telomeres. Nature 460: 914-918
8. Dimitrova N, de Lange T (2009) Cell cycle-dependent role of MRN at dysfunctional telomeres: ATM signaling-dependent induction of nonhomologous end joining (NHEJ) in G1 and resection-mediated inhibition of NHEJ in G2. Mol Cell Biol 29: 5552-5563
9. Dinkelmann M, Spehalski E, Stoneham T, Buis J, Wu Y, Sekiguchi JM, Ferguson DO (2009) Multiple functions of MRN in endjoining pathways during isotype class switching. Nat Struct Mol Biol 16: 808-813
10. Falck J, Coates J, Jackson SP (2005) Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434: 605-611 (Pubitemid 40488547)
11. Ferreira MG, Cooper JP (2001) The fission yeast Taz1 protein protects chromosomes from Ku-dependent end-to-end fusions. Mol Cell 7: 55-63 (Pubitemid 32162899)
12. Ferreira MG, Cooper JP (2004) Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle. Genes Dev 18: 2249-2254 (Pubitemid 39209573)
13. Ferreira MG, Miller KM, Cooper JP (2004) Indecent exposure: when telomeres become uncapped. Mol Cell 13: 7-18 (Pubitemid 38117111)
14. Frank-Vaillant M, Marcand S (2002) Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol Cell 10: 1189-1199 (Pubitemid 35453835)
15. Hartsuiker E, Mizuno K, Molnar M, Kohli J, Ohta K, Carr AM (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
16. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455: 689-692
17. Huertas P, Jackson SP (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284: 9558-9565
18. Jain D, Cooper JP (2010) Telomeric strategies: means to an end. Annu Rev Genet 44: 243-269
19. Karlseder J, Broccoli D, Dai Y, Hardy S, de Lange T (1999) p53-and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283: 1321-1325
20. Konishi A, de Lange T (2008) Cell cycle control of telomere protection and NHEJ revealed by a ts mutation in the DNA-binding domain of TRF2. Genes Dev 22: 1221-1230 (Pubitemid 351656580)
21. Langerak P, Mejia-Ramirez E, Limbo O, Russell P (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
22. Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: implications for telomere evolution. Cell 101: 471-483
23. Limbo O, Chahwan C, Yamada Y, de Bruin RA, Wittenberg C, Russell P (2007) 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 (Pubitemid 47531975)
24. Manolis KG, Nimmo ER, Hartsuiker E, Carr AM, Jeggo PA, Allshire RC (2001) Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J 20: 210-221 (Pubitemid 32099117)
25. Miller KM, Ferreira MG, Cooper JP (2005) Taz1, Rap1 and Rif1 act both interdependently and independently to maintain telomeres. EMBO J 24: 3128-3135 (Pubitemid 41486348)
26. Miller KM, Rog O, Cooper JP (2006) Semi-conservative DNA replication through telomeres requires Taz1. Nature 440: 824-828
27. Mimitou EP, Symington LS (2011) DNA end resection-unraveling the tail. DNA Repair (Amst) 10: 344-348
28. Moreau S, Ferguson JR, Symington LS (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol 19: 556-566 (Pubitemid 29018457)
29. Naito T, Matsuura A, Ishikawa F (1998) Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat Genet 20: 203-206 (Pubitemid 28455457)
30. Pardo B, Marcand S (2005) Rap1 prevents telomere fusions by nonhomologous end joining. EMBO J 24: 3117-3127 (Pubitemid 41486347)
31. Paull TT, Gellert M (1998) The 30 to 50 exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol Cell 1: 969-979 (Pubitemid 128379258)
32. Porter-Goff ME, Rhind N (2009) The role of MRN in the S-phase DNA damage checkpoint is independent of its Ctp1-dependent roles in double-strand break repair and checkpoint signaling. Mol Biol Cell 20: 2096-2107
33. Rog O, Miller KM, Ferreira MG, Cooper JP (2009) Sumoylation of RecQ helicase controls the fate of dysfunctional telomeres. Mol Cell 33: 559-569
34. Tomita K, Kibe T, Kang HY, Seo YS, Uritani M, Ushimaru T, Ueno M (2004) Fission yeast Dna2 is required for generation of the telomeric single-strand overhang. Mol Cell Biol 24: 9557-9567 (Pubitemid 39391691)
35. Tomita K, Matsuura A, Caspari T, Carr AM, Akamatsu Y, Iwasaki H, Mizuno K, Ohta K, Uritani M, Ushimaru T, Yoshinaga K, Ueno M (2003) Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol Cell Biol 23: 5186-5197 (Pubitemid 36950874)
36. Trenz K, Smith E, Smith S, Costanzo V (2006) ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J 25: 1764-1774
37. Wang H, Perrault AR, Takeda Y, Qin W, Iliakis G (2003) Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res 31: 5377-5388 (Pubitemid 37441906)
38. Williams GJ, Lees-Miller SP, Tainer JA (2010) Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair (Amst) 9: 1299-1306
39. Williams GJ, Williams RS, Williams JS, Moncalian G, Arvai AS, Limbo O, Guenther G, SilDas S, Hammel M, Russell P, Tainer JA (2011) ABC ATPase signature helices in Rad50 link nucleotide state to Mre11 interface for DNA repair. Nat Struct Mol Biol 18: 423-431
40. Williams RS, Moncalian G, Williams JS, Yamada Y, Limbo O, Shin DS, Groocock LM, Cahill D, Hitomi C, Guenther G, Moiani D, Carney JP, Russell P, Tainer JA (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strandbreak repair. Cell 135: 97-109
41. You Z, Chahwan C, Bailis J, Hunter T, Russell P (2005) ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol Cell Biol 25: 5363-5379 (Pubitemid 40853574)