Synthetic viability genomic screening defines Sae2 function in DNA repair

EMBO Journal

Volumn 34, Issue 11, 2015, Pages 1509-1522

  Puddu, Fabio ^a   Oelschlaegel, Tobias ^a   Guerini, Ilaria ^a   Geisler, Nicola J ^a   Niu, Hengyao ^c   Herzog, Mareike ^a   Salguero, Israel ^a   Ochoa Montaño, Bernardo ^a   Viré, Emmanuelle ^a   Sung, Patrick ^c   Adams, David J ^b   Keane, Thomas M ^b   Jackson, Stephen P ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mre11; Sae2; suppressor screening; synthetic viability; whole genome sequencing

Indexed keywords

DNA TOPOISOMERASE; GENOMIC DNA; MRE11 PROTEIN; PROTEIN; SAE2 PROTEIN; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE; ENDONUCLEASE; EXODEOXYRIBONUCLEASE; FUNGAL DNA; MRE11 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SAE2 PROTEIN, S CEREVISIAE; SINGLE STRANDED DNA; SPO11 PROTEIN, S CEREVISIAE;

ARTICLE; CLINICAL ASSESSMENT; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA SEQUENCE; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; GENE MUTATION; GENE SEQUENCE; GENETIC SCREENING; GENETIC VARIABILITY; GENOME ANALYSIS; HIGH THROUGHPUT SEQUENCING; HOMOLOGOUS RECOMBINATION; MEIOSIS; MEIOTIC RECOMBINATION; MUTAGENESIS; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; SENSITIVITY ANALYSIS; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

DNA REPAIR; DNA, FUNGAL; DNA, SINGLE-STRANDED; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; EXODEOXYRIBONUCLEASES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84931574228     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201590973     Document Type: Article

References (53)

1. Andres SN, Appel CD, Westmoreland JW, Williams JS, Nguyen Y, Robertson PD, Resnick MA, Williams RS, (2015) Tetrameric Ctp1 coordinates DNA binding and DNA bridging in DNA double-strand-break repair. Nat Struct Mol Biol 22: 158-166
2. Baroni E, Viscardi V, Cartagena-Lirola H, Lucchini G, Longhese MP, (2004) The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol Cell Biol 24: 4151-4165
3. Barton O, Naumann SC, Diemer-Biehs R, Künzel J, Steinlage M, Conrad S, Makharashvili N, Wang J, Feng L, Lopez BS, Paull TT, Chen J, Jeggo PA, Löbrich M, (2014) Polo-like kinase 3 regulates CtIP during DNA double-strand break repair in G1. J Cell Biol 206: 877-894
4. Benkert P, Tosatto SCE, Schomburg D, (2008) QMEAN: a comprehensive scoring function for model quality assessment. Proteins 71: 261-277
5. Benkert P, Künzli M, Schwede T, (2009) QMEAN server for protein model quality estimation. Nucleic Acids Res 37: W510-W514
6. Cannavo E, Cejka P, (2014) Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature 514, 122-125
7. Cannon B, Kuhnlein J, Yang S-H, Cheng A, Schindler D, Stark JM, Russell R, Paull TT, (2013) Visualization of local DNA unwinding by Mre11/Rad50/Nbs1 using single-molecule FRET. Proc Natl Acad Sci USA 110: 18868-18873
8. Chen H, Donnianni RA, Handa N, Deng SK, Oh J, Timashev LA, Kowalczykowski SC, Symington LS, (2015) Sae2 promotes DNA damage resistance by removing the Mre11-Rad50-Xrs2 complex from DNA and attenuating Rad53 signaling. Proc Natl Acad Sci USA 112: E1880-E1887
9. Clerici M, Mantiero D, Lucchini G, Longhese MP, (2005) The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280: 38631-38638
10. Clerici M, Mantiero D, Lucchini G, Longhese MP, (2006) The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep 7: 212-218
11. Daley JM, Palmbos PL, Wu D, Wilson TE, (2005) Nonhomologous end joining in yeast. Annu Rev Genet 39: 431-451
12. Davies OR, Forment JV, Sun M, Belotserkovskaya R, Coates J, Galanty Y, Demir M, Morton CR, Rzechorzek NJ, Jackson SP, Pellegrini L, (2015) CtIP tetramer assembly is required for DNA-end resection and repair. Nat Struct Mol Biol 22: 150-157
13. Deng C, Brown JA, You D, Brown JM, (2005) Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170: 591-600
14. Fishman-Lobell J, Rudin N, Haber JE, (1992) Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol Cell Biol 12: 1292-1303
15. Foster SS, Balestrini A, Petrini JHJ, (2011) Functional interplay of the Mre11 nuclease and Ku in the response to replication-associated DNA damage. Mol Cell Biol 31: 4379-4389
16. Fukunaga K, Kwon Y, Sung P, Sugimoto K, (2011) Activation of protein kinase Tel1 through recognition of protein-bound DNA ends. Mol Cell Biol 31: 1959-1971
17. Furuse M, Nagase Y, Tsubouchi H, Murakami-Murofushi K, Shibata T, Ohta K, (1998) Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J 17: 6412-6425
18. Goldway M, Sherman A, Zenvirth D, Arbel T, Simchen G, (1993) A short chromosomal region with major roles in yeast chromosome III meiotic disjunction, recombination and double strand breaks. Genetics 133: 159-169
19. Hardy J, Churikov D, Géli V, Simon M-N, (2014) Sgs1 and Sae2 promote telomere replication by limiting accumulation of ssDNA. Nat Commun 5: 5004
20. Hartsuiker E, Neale MJ, Carr AM, (2009) Distinct requirements for the Rad32Mre11 nuclease and Ctp1CtIP in the removal of covalently bound topoisomerase I and II from DNA. Mol Cell 33: 117-123
21. Hopfner KP, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA, (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101: 789-800
22. Huertas P, Cortés-Ledesma F, Sartori AA, Aguilera A, Jackson SP, (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455: 689-692
23. 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
24. Ivanov EL, Sugawara N, White CI, Fabre F, Haber JE, (1994) Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol Cell Biol 14: 3414-3425
25. Jackson SP, Bartek J, (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078
26. Keeney S, Kleckner N, (1995) Covalent protein-DNA complexes at the 5′ strand termini of meiosis-specific double-strand breaks in yeast. Proc Natl Acad Sci USA 92: 11274-11278
27. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384
28. Krogh BO, Llorente B, Lam A, Symington LS, (2005) Mutations in Mre11 phosphoesterase motif I that impair Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex stability in addition to nuclease activity. Genetics 171: 1561-1570
29. Lengsfeld BM, Rattray AJ, Bhaskara V, Ghirlando R, Paull TT, (2007) Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol Cell 28: 638-651
30. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, (2009) The sequence alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079
31. Lisby M, Barlow JH, Burgess RC, Rothstein R, (2004) Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713
32. Makharashvili N, Tubbs AT, Yang S-H, Wang H, Barton O, Zhou Y, Deshpande RA, Lee J-H, Lobrich M, Sleckman BP, Wu X, Paull TT, (2014) Catalytic and noncatalytic roles of the CtIP endonuclease in double-strand break end resection. Mol Cell 54: 1022-1033
33. Mantiero D, Clerici M, Lucchini G, Longhese MP, (2007) Dual role for Saccharomyces cerevisiae Tel1 in the checkpoint response to double-strand breaks. EMBO Rep 8: 380-387
34. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F, (2010) Deriving the consequences of genomic variants with the Ensembl API and SNP effect predictor. Bioinformatics 26: 2069-2070
35. Mimitou EP, Symington LS, (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774
36. Mimitou EP, Symington LS, (2010) Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J 29: 3358-3369
37. 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
38. Moreau S, Morgan EAA, Symington LSS, (2001) Overlapping functions of the Saccharomyces cerevisiae mre11, exo1 and rad27 nucleases in DNA metabolism. Genetics 159: 1423
39. Nairz K, Klein F, (1997) mre11S - a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11: 2272-2290
40. Prinz S, Amon A, Klein F, (1997) Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146: 781-795
41. Sali A, Blundell TL, (1990) Definition of general topological equivalence in protein structures. A procedure involving comparison of properties and relationships through simulated annealing and dynamic programming. J Mol Biol 212: 403-428
42. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815
43. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, Elledge SJ, (1996) Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360
44. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP, (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514
45. Schiller CB, Lammens K, Guerini I, Coordes B, Feldmann H, Schlauderer F, Möckel C, Schele A, Strässer K, Jackson SP, Hopfner K-P, (2012) Structure of Mre11-Nbs1 complex yields insights into ataxia-telangiectasia-like disease mutations and DNA damage signaling. Nat Struct Mol Biol 19: 693-700
46. Stracker TH, Petrini JHJ, (2011) The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 12: 90-103
47. Symington LS, Gautier J, (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247-271
48. Usui T, Ogawa H, Petrini JH, (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7: 1255-1266
49. Vaze MB, Pellicioli A, Lee SE, Ira G, Liberi G, Arbel-Eden A, Foiani M, Haber JE, (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol Cell 10: 373-385
50. Wang H, Li Y, Truong LN, Shi LZ, Hwang PY-H, He J, Do J, Cho MJ, Li H, Negrete A, Shiloach J, Berns MW, Shen B, Chen L, Wu X, (2014) CtIP maintains stability at common fragile sites and inverted repeats by end resection-independent endonuclease activity. Mol Cell 54: 1012-1021
51. 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-strand-break repair. Cell 135: 97-109
52. You Z, Shi LZ, Zhu Q, Wu P, Zhang Y-W, Basilio A, Tonnu N, Verma IM, Berns MW, Hunter T, (2009) CtIP links DNA double-strand break sensing to resection. Mol Cell 36: 954-969
53. Zhu Z, Chung W-H, Shim EY, Lee SE, Ira G, (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994