The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci

Genes and Development

Volumn 14, Issue 1, 2000, Pages 81-96

  Frei, Christian ^a   Gasser, Susan M ^a  

^a SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

Bloom's syndrome; Checkpoint; DNA damage; DNA replication; Sgs1p helicase; Werner's syndrome

Indexed keywords

HELICASE;

ARTICLE; BLOOM SYNDROME; CELL CYCLE S PHASE; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; NONHUMAN; PRIORITY JOURNAL; WERNER SYNDROME; YEAST;

CELL CYCLE PROTEINS; DNA HELICASES; DNA REPLICATION; FUNGAL PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 0033957793     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Aparicio, O.M., D.M. Weinstein, and S.P. Bell. 1997. Components and dynamics of DNA replication complexes in S. cerevisiae: Redistribution of MCM proteins and Cdc45p during S phase. Cell 91: 59-69.
2. Araki, H., S.H. Leem, A. Phongdara, and A. Sugino, 1995. Dpb11, which interacts with DNA polymerase II(e) in S. cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc. Natl. Acad. Sci. 92: 11791-11795.
3. Auerbach, A.D. and P.C. Verlander. 1997. Disorders of DNA replication and repair. Curr. Opin. Pediatr. 9: 600-616.
4. Bierne, H. and B. Michel, 1994. When replication forks stop. Mol. Microbiol. 13: 17-23.
5. Budd, M.E. and J.L. Campbell, 1993. DNA polymerases δ and ε are required for chromosomal replication in S. cerevisiae. Mol. Cell. Biol. 13: 496-505.
6. _. 1997. A yeast replicative helicase, Dna2 helicase, interacts with yeast Fen-1 nuclease in carrying out its essential function. Mol. Cell. Biol. 17: 2136-2142.
7. Chakraverty, R.K. and I.D. Hickson. 1999. Defending genome integrity during DNA replication: A proposed role for RecQ family helicases. BioEssays 21: 286-294.
8. Chester, N., F. Kuo, C. Kozak, C.D. O'Hara, and P. Leder. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes & Dev. 12: 3382-3393.
9. Cho, R.J., M.J. Campbell, E.A. Winzeler, L. Steinmetz, A. Conway, L. Wodicka, T.G. Wolfsberg, A.E. Gabrielian, D. Landsman, D.J. Lockhart et al. 1998. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol. Cell 2: 65-73.
10. Cohen-Fix, O. and D. Koshland. 1997. The anaphase inhibitor of S. cerevisiae Pdslp is a target of the DNA damage checkpoint pathway. Proc. Natl Acad. Sci. 94: 14361-14366.
11. Coverley, D. and R.A. Laskey. 1994. Regulation of eukaryotic DNA replication. Annu. Rev. Biochem. 63: 745-776.
12. Davey, S., C.S. Han, S.A. Ramer, J.C. Klassen, A. Jacobson, A. Eisenberger, K.M. Hopkins, H.B. Lieberman, and G.A. Freyer. 1998. Fission yeast rad12+ regulates cell cycle checkpoint control and is homologous to the Bloom's syndrome disease gene. Mol. Cell. Biol. 18: 2721-2728.
13. de la Torre-Ruiz, M.A., C.M. Green, and N.F. Lowndes. 1998. RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation. EMBO J. 17: 2687-2698.
14. Desany, B.A., A.A. Alcasabas, J.B. Bachant, and S.J. Elledge. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes & Dev. 12: 2956-2970.
15. Elledge, S.J. 1996. Cell cycle checkpoints - preventing an identity crisis. Science 274: 1664-1672.
16. Ellis, N.A., J. Groden, T.Z. Ye, J. Straughen, D.J. Lennon, S. Ciocci, M. Proytcheva, and J. German. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83: 655-666.
17. Epstein, C.J., G.M. Martin, A.L. Schultz, and A.G. Motulsky. 1966. Werner's syndrome a review of its symptomatology, natural history, pathologic features, genetics and relationship to the natural aging process. Medicine 45: 177-221.
18. Gangloff, S., J.P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein. 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.
19. Gardner, R., C.W. Putnam, and T. Weinert. 1999. RAD53, DUN1, and PDS1 define two parallel G2/M checkpoint pathways in budding yeast. EMBO J. 18: 3173-3185.
20. German, J. 1993. Bloom syndrome: A mendelian prototype of somatic mutational disease. Medicine 72: 393-406.
21. Gotta, M., T. Laroche, A. Formenton, L. Maillet, H. Scherthan, and S.M. Gasser. 1996. The clustering of telomeres and co-localization with Rap1, Sir3, and Sir4 proteins in wild-type S. cerevisiae. J. Cell Biol. 134: 1349-1363.
22. Gotta, M., S. Strahl-Bolsinger, H. Renauld, T. Laroche, B.K. Kennedy, M. Grunstein, and S.M. Gasser. 1997. Localization of Sir2p: The nucleolus as a compartment for silent information regulators. EMBO J. 16: 3243-3255.
23. Gotta, M., T. Laroche, and S.M. Gasser. 1999. Analysis of nuclear organization in Saccharomyces cerevisiae. Methods Enzymol. 304: 663-672.
24. Hand, R. and J. German. 1975. A retarded rate of DNA chain growth in Bloom's syndrome. Proc. Natl. Acad. Sci 72: 758-762.
25. Kastan, M.B. 1997. Checkpoint controls and cancer. Cancer Surv. 29: 1-6.
26. Klein, F., T. Laroche, M.E. Cardenas, J.F. Hofmann, D. Schweizer, and S.M. Gasser. 1992. Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast. J. Cell Biol. 117: 935-948.
27. Kusano, K., M.E. Berres, and W.R. Engels. 1999. Evolution of the RECQ family of helicases. A Drosophila homolog, DmBLM, is similar to the human Bloom's syndrome gene. Genetics 151: 1027-1039.
28. Kuzminov, A. 1995. Instability of inhibited replication forks in E. coli. BioEssays 17: 733-741.
29. Li, J.J. 1995. DNA replication. Once, and only once. Curr. Biol. 5: 472-475.
30. Longhese, M.P., H. Neecke, V. Paciotti, G. Lucchini, and P. Plevani. 1996. The 70 kDa subunit of replication protein A is required for the G1/S and intra-S DNA damage checkpoints in budding yeast. Nucleic Acids Res. 24: 3533-3537.
31. Longhese, M.P., V. Paciotti, R. Fraschini, R. Zaccarini, P. Plevani, and G. Lucchini. 1997. The novel DNA damage checkpoint protein Ddclp is phosphorylated periodically during the cell cycle and in response to DNA damage in budding yeast. EMBO J. 16: 5216-5226.
32. Longtine, M.S., A. McKenzie, 3rd, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J.R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in S. cerevisiae. Yeast 14: 953-961.
33. Lonn, U., S. Lonn, U. Nylen, G. Winblad, and J. German. 1990. An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancel Res. 50: 3141-3145.
34. Lu, J.A., J.R. Mullen, S.J. Brill, S. Kleff, A.M. Romeo, and R. Stemglanz. 1996. Human homologues of yeast helicase. Nature 383: 678-679.
35. Lydall, D. and T. Weinert. 1997. G2/M checkpoint genes of S. cerevisiae: Further evidence for roles in DNA replication and/or repair. Mol. & Gen. Genet. 256: 638-651.
36. Marciniak, R.A., D.B. Lombard, F.B. Johnson, and L. Guarente. 1998. Nucleolar localization of the Werner syndrome protein in human cells. Proc. Natl. Acad. Sci. 95: 6887-6892.
37. Marini, F., A. Pellicioli, V. Paciotti, G. Lucchini, P. Plevani, D.F. Stern, and M. Foiani. 1997. A role for DNA primase in coupling DNA replication to DNA damage response. EMBO J. 16: 639-650.
38. Morozov, V., A.R. Mushegian, E.V. Koonin, and P. Bork. 1997. A putative nucleic acid-binding domain in Bloom's and Werner's syndrome helicases. Trends Biochem. Sci. 22: 417-418.
39. Murray, J.M., H.D. Lindsay, C.A. Munday, and A.M. Carr. 1997. Role of S. pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol. Cell. Biol. 17: 6868-6875.
40. Nakamura, H., T. Morita, and C. Sato. 1986. Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165: 291-297.
41. Navas, T.A., Z. Zhou, and SJ. Elledge. 1995. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint. Cell 80: 29-39.
42. Navas, T.A., Y. Sanchez, and S.J. Elledge. 1996. RAD9 and DNA polymerase ε form parallel sensory branches for transducing the DNA damage checkpoint signal in S. cerevisiae. Genes & Dev. 10: 2632-2643.
43. Pasero, P. and S.M. Gasser. 1998. New systems for replicating DNA in vitro. Cun. Opin. Cell Biol. 10: 304-310.
44. Pasero, P., D. Braguglia, and S.M. Gasser. 1997. ORC-dependent and origin-specific initiation of DNA replication at defined foci in isolated yeast nuclei. Genes & Dev. 11: 1504-1518.
45. Pasero, P., B.P. Duncker, E. Schwob, and S.M. Gasser. 1999. A role for the Cdc7 kinase regulatory subunit Dbf4p in the formation of initiation-competent origins of replication. Genes & Dev. 13: 2159-2176.
46. Paulovich, A.G. and L.H. Hartwell. 1995. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82: 841-847.
47. Paulovich, A.G., R.U. Margulies, B.M. Garvik, and L.H. Hartwell. 1997. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics 145: 45-62.
48. Plug, A.W., A.H. Peters, Y. Xu, K.S. Keegan, M.F. Hoekstra, D. Baltimore, P. de Boer, and T. Ashley. 1997. ATM and RPA in meiotic chromosome synapsis and recombination. Nat. Genet. 17: 457-461.
49. Plug, A.W., A.H. Peters, K.S. Keegan, M.F. Hoekstra, P. de Boer, and T. Ashley. 1998. Changes in protein composition of meiotic nodules during mammalian meiosis. J. Cell Sci. 111: 413-423.
50. Poot, M., H. Hoehn, T.M. Runger, and G.M. Martin. 1992. Impaired S-phase transit of Werner syndrome cells expressed in lymphoblastoid cell lines. Exp. Cell Res. 202: 267-273.
51. Puranam, K.L. and P.J. Blackshear. 1994. Cloning and characterization of RECQL, a potential human homologue of the Escherichia coli DNA helicase RecQ. J. Biol. Chem. 269: 29838-29845.
52. Salk, D., E. Bryant, H. Hoehn, P. Johnston, and G.M. Martin. 1985. Growth characteristics of Werner syndrome cells in vitro. Adv. Exp. Med. Biol. 190: 305-311.
53. Sanchez, Y., B.A. Desany, W.J. Jones, Q. Liu, B. Wang, and S.J. Elledge. 1996. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360.
54. Shiratori, M., S. Sakamoto, N. Suzuki, Y. Tokutake, Y. Kawabe, T. Enomoto, M. Sugimoto, M. Goto, T. Matsumoto, and Y. Furuichi. 1999. Detection by epitope-defined monoclonal antibodies of Werner DNA helicases in the nucleoplasm and their upregulation by cell transformation and immortalization. J. Cell Biol. 144: 1-9.
55. Sidorova, J.M. and L.L. Breeden. 1997. Rad53-dependent phosphorylation of Swi6 and down-regulation of CLN1 and CLN2 transcription occur in response to DNA damage in Saccharomyces cerevisiae. Genes & Dev. 11: 3032-3045.
56. Sinclair, D.A. and L. Guarente. 1997. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91: 1033-1042.
57. Sinclair, D.A., K. Mills, and L. Guarente. 1997. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science 277: 1313-1316.
58. Stewart, E., C.R. Chapman, F. Al-Khodairy, A.M. Carr, and T. Enoch. 1997. rqhl+, 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.
59. Sun, Z., D.S. Fay, F. Marini, M. Foiani, and D.F. Stern. 1996. Spkl/Rad53 is regulated by Mecl-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes & Dev. 10: 395-406.
60. Walpita, D., A.W. Plug, N.F. Neff, J. German, and T. Ashley. 1999. Bloom's syndrome protein, BLM, colocalizes with replication protein A in meiotic prophase nuclei of mammalian spermatocytes. Proc. Natl. Acad. Sci. 96: 5622-5627.
61. Wang, H. and S.J. Elledge. 1999. DRC1, DNA replication and checkpoint protein 1, functions with DPB11 to control DNA replication and the S-phase checkpoint in Saccharomyces ceievisiae. Proc. Natl. Acad. Sci. 96: 3824-3829.
62. Watt, P.M. and I.D. Hickson. 1996. Genome stability - failure to unwind causes cancer. Curr. Biol. 6: 265-267.
63. Watt, P.M., E.J. Louis, R.H. Borts, and I.D. Hickson. 1995. Sgs1: A eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81: 253-260.
64. Watt, P.M., I.D. Hickson, R.H. Borts, and E.J. Louis. 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.
65. Weinert, T. 1998. DNA damage checkpoints update: Getting molecular. Curr. Opin. Genet. Dev. 8: 185-193.
66. Xu, Z. and D. Norris. 1998. The SFP1 gene product of S. cerevisiae regulates G2/M transitions during the mitotic cell cycle and DMA-damage response. Genetics 150: 1419-1428.
67. Yamagata, K., J. Kato, A. Shimamoto, M. Goto, Y. Furuichi, and H. Ikeda. 1998. Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: Implication for genomic instability in human diseases. Proc. Natl. Acad. Sci. 95: 8733-8738.
68. Yan, H. and J. Newport. 1995. FFA-1, a protein that promotes the formation of replication centers within nuclei. Science 269: 1883-1885.
69. Yan, H., C.Y. Chen, R. Kobayashi, and J. Newport. 1998. Replication focus-forming activity 1 and the Werner syndrome gene product. Nat. Genet. 19: 375-378.
70. Yu, C.E., J. Oshima, Y.H. Fu, E.M. Wijsman, F. Hisama, R. Alisch, S. Matthews, J. Nakura, T. Miki, S. Ouais et al. 1996. Positional cloning of the Werner's syndrome gene. Science 272: 258-262.