Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance

EMBO Journal

Volumn 24, Issue 2, 2005, Pages 405-417

  Bjergbaek, Lotte ^a   Cobb, Jennifer A ^a   Tsai Pflugfelder, Monica ^a   Gasser, Susan M ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

DNA polymerase stabilisation; Rad53 activation; S phase checkpoint; Sgs1p; Top3

Indexed keywords

CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; DNA POLYMERASE; DNA TOPOISOMERASE; HELICASE; HYDROXYUREA; REPLICATION FACTOR C; REPLISOME; RESOLVASE; S PHASE KINASE ASSOCIATED PROTEIN; TRANSCRIPTION FACTOR SGS1P; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; COMPLEX FORMATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; EPISTASIS; GENE MUTATION; GENETIC STABILITY; GENOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF;

CELL CYCLE; CELL CYCLE PROTEINS; DNA HELICASES; DNA REPLICATION; DNA TOPOISOMERASES, TYPE I; HYDROXYUREA; IMMUNOPRECIPITATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 13444283383     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600511     Document Type: Article

References (50)

1. Aboussekhra A, Chanet R, Adjiri A, Fahre F (1992) Semidominant suppressors of Srs2 helicase mutations of S. cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol Cell Biol 12: 3224-3234
2. Adams A, Gottschling DE, Kaiser CA, Stearns T (1997) Methods in Yeast Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press
3. Alcasabas AA, Osborn AJ, Bachant J, Hu F, Weder PJ, Bousset K, Furuya K, Diffley JF, Carr AM, Elledge SJ (2001) Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol 3: 958-965
4. Aparicio OM, Stout AM, Bell SP (1999) Differential assembly of Cdc45p and DNA polymerases at early and late origins of DNA replication. Proc Natl Acad Sci USA 96: 9130-9135
5. Aushubel FM, Brent R, Kinston R, Moore D, Seidman JJ, Smith J, Struhl K (1994) Current Protocols in Molecular Biology. New York: John Wiley and Sons
6. Chakraverty RK, Kearsey JM, Oakley TJ, Grenon M, de La Torre Ruiz MA, Lowndes NF, Hickson ID (2001) Topoisomerase III acts upstream of Rad53p in the S-phase DNA damage checkpoint. Mol Cell Biol 21: 7150-7162
7. Cobb JA, Bjergbaek L, Shimada K, Frei C, Gasser SM (2003) DNA polymerase stabilisation at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J 22: 4325-4336
8. Fabre F, Chan A, Heyer WD, Gangloff S (2002) Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc Natl Acad Sci USA 99: 16887-16892
9. Frei C, Gasser SM (2000) The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev 14: 81-96
10. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391-8398
11. Goodwin A, Wang SW, Toda T, Norbury C, Hickson ID (1999) Topoisomerase III is essential for accurate nuclear division in S. pombe. Nucleic Acids Res 27: 4050-4058
12. Ira G, Malkova A, Liberi G, Foiani M, Haber JE (2003) Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401-411
13. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, Sugimoto K, Shirahige K (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083
14. Khakhar RR, Cobb JA, Bjergbaek L, Hickson ID, Gasser SM (2003) RecQ helicases: multiple roles in genome maintenance. Trends Cell Biol 13: 493-501
15. Kolodner RD, Putnam CD, Myung K (2002) Maintenance of genome stability in S. cerevisiae. Science 297: 552-557
16. Kumagai A, Dunphy WG (2000) Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol Cell 6: 839-849
17. Lee J, Kumagai A, Dunphy WG (2003) Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol Cell 11: 329-340
18. Li W, Kim SM, Lee J, Dunphy WG (2004) Absence of BLM leads to accumulation of chromosomal DNA breaks during both unperturbed and disrupted S phases. J Cell Biol 165: 801-812
19. Li W, Wang JC (1998) Mammalian DNA topoisomerase IIIα is essential in early embryogenesis. Proc Natl Acad Sci USA 95: 1010-1013
20. Liberi G, Chiolo I, Pellicioli A, Lopes M, Plevani P, Muzi-Falconi M, Foiani M (2000) Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J 19: 5027-5038
21. Lomonosov M, Anand S, Sangrithi M, Davies R, Venkitaraman AR (2003) Stabilisation of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev 17: 3017-3022
22. Longtine MS, McKenzie III A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in S. cerevisiae. Yeast 14: 953-961
23. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, Muzi-Falconi M, Newlon CS, Foiani M (2001) The DNA replication checkpoint response stabilises stalled replication forks. Nature 412: 557-561
24. Lu JA, Mullen JR, Brill SJ, Kleff S, Romeo AM, Sternglanz R (1996) Human homologues of yeast helicase. Nature 383: 678-679
25. Marchetti MA, Kumar S, Hartsuiker E, Maftahi M, Carr AM, Freyer GA, Burhans WC, Huberman JA (2002) A single unbranched S-phase DNA damage and replication fork blockage checkpoint pathway. Proc Natl Acad Sci USA 99: 7472-7477
26. McGlynn P, Lloyd RG (2001) Rescue of stalled replication forks by RecG: simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation. Proc Natl Acad Sci USA 98: 8227-8234
27. Merrill BJ, Holm C (1999) A requirement for recombinational repair in S. cerevisiae is caused by DNA replication defects of mec1 mutants. Genetics 153: 595-605
28. Michel B, Flores MJ, Viguera E, Grompone G, Seigneur M, Bidnenko V (2001) Rescue of arrested replication forks by homologous recombination. Proc Natl Acad Sci USA 98: 8181-8188
29. Mohaghegh P, Hickson ID (2001) DNA helicase deficiencies associated with cancer predisposition and premature ageing disorders. Hum Mol Genet 10: 741-746
30. Mullen JR, Kaliraman V, Brill SJ (2000) Bipartite structure of the SGS1 DNA helicase in S. cerevisiae. Genetics 154: 1101-1114
31. Murray JM, Lindsay HD, Munday CA, Carr AM (1997) Role of S. pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol Cell Biol 17: 6868-6875
32. Myung K, Datta A, Chen C, Kolodner RD (2001) SGS1, the S. cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat Genet 27: 113-116
33. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA (2002) Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 36: 617-656
34. Osborn AJ, Elledge SJ (2003) Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev 17: 1755-1767
35. Paulovich AG, Margulies RU, Garvik BM, Hartwell LH (1997) RAD9, RAD17, and RAD24 are required for S phase regulation in S. cerevisiae in response to DNA damage. Genetics 145: 45-62
36. Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, Plevani P, Romano A, Di Fiore PP, Foiani M (1999) Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J 18: 6561-6572
37. Robu ME, Inman RB, Cox MM (2001) RecA protein promotes the regression of stalled replication forks in vitro. Proc Natl Acad Sci USA 98: 8211-8218
38. Schollaert KL, Poisson JM, Searle JS, Schwanekamp JA, Tomlinson CR, Sanchez Y (2004) A role for S. cerevisiae Chk1p in the response to replication blocks. Mol Biol Cell 15: 4051-4063
39. Schwartz MF, Lee SJ, Duong JK, Eminaga S, Stern DF (2003) FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2: 384-396
40. Shimada K, Pasero P, Gasser SM (2002) ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phase. Genes Dev 16: 3236-3252
41. Sinclair DA, Mills K, Guarente L (1997) Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science 277: 1313-1316
42. Sogo JM, Lopes M, Foiani M (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602
43. Stewart E, Chapman CR, Al-Khodairy F, Carr AM, Enoch T (1997) rqh1+, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J 16: 2682-2692
44. Tercero JA, Diffley JF (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412: 553-557
45. Tercero JA, Longhese MP, Diffley JF (2003) A central role for DNA replication forks in checkpoint activation and response. Mol Cell 11: 1323-1336
46. Wallis JW, Chrebet G, Brodsky G, Rolfe M, Rothstein R (1989) A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409-419
47. Watt PM, Hickson ID, Borts RH, Louis EJ (1996) Sgs1, a homologue of the Blooms and Werners syndrome genes, is required for maintenance of genome stability in S. cerevisiae. Genetics 144: 935-945
48. Wu L, Davies SL, Levitt NC, Hickson ID (2001) Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J Biol Chem 276: 19375-19381
49. Wu L, Davies SL, North PS, Goulaouic H, Riou JF, Turley H, Gatter KC, Hickson ID (2000) The Bloom's syndrome gene product interacts with topoisomerase III. J Biol Chem 275: 9636-9644
50. Wu L, Hickson ID (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874