Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks

Genes and Development

Volumn 22, Issue 13, 2008, Pages 1816-1827

  Segurado, Monica ^a   Diffley, John F X ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Checkpoints; Chk1; DNA replication fork stabilization; Exo1; Mec1; Rad53

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; FUNGAL DNA;

ARTICLE; DNA DAMAGE; DNA REPLICATION; EXO1 GENE; FUNGAL GENE; NONHUMAN; PRIORITY JOURNAL; YEAST;

ANTINEOPLASTIC AGENTS, ALKYLATING; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPLICATION; EXODEOXYRIBONUCLEASES; METHYL METHANESULFONATE; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 46249122812     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.477208     Document Type: Article

References (56)

1. Allen, J.B., Zhou, Z., Siede, W., Friedberg, E.C., and Elledge, S.J. 1994. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes & Dev. 8: 2401-2415.
2. Andreassen, P.R., Ho, G.P., and D'Andrea, A.D. 2006. DNA damage responses and their many interactions with the replication fork. Carcinogenesis 27: 883-892.
3. Bjergbaek, L., Cobb, J.A., Tsai-Pflugfelder, M., and Gasser, S.M. 2005. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 24: 405-417.
4. Branzei, D. and Foiani, M. 2006. The Rad53 signal transduction pathway: Replication fork stabilization, DNA repair, and adaptation. Exp. Cell Res. 312: 2654-2659.
5. Brondello, J.M., Boddy, M.N., Furnari, B., and Russell, P. 1999. Basis for the checkpoint signal specificity that regulates Chk1 and Cds1 protein kinases. Mol. Cell. Biol. 19: 4262-4269.
6. Chan, C.S. and Tye, B.K. 1983. Organization of DNA sequences and replication origins at yeast telomeres. Cell 33: 563-573.
7. Cobb, J.A., Bjergbaek, L., Shimada, K., Frei, C., and Gasser, S.M. 2003. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22: 4325-4336.
8. Cobb, J.A., Schleker, T., Rojas, V., Bjergbaek, L., Tercero, J.A., and Gasser, S.M. 2005. Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes & Dev. 19: 3055-3069.
9. Cotta-Ramusino, C., Fachinetti, D., Lucca, C., Doksani, Y., Lopes, M., Sogo, J., and Foiani, M. 2005. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17: 153-159.
10. Desany, B.A., Alcasabas, A.A., Bachant, J.B., and Elledge, S.J. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes & Dev. 12: 2956-2970.
11. Diffley, J.F., Cocker, J.H., Dowell, S.J., and Rowley, A. 1994. Two steps in the assembly of complexes at yeast replication origins in vivo. Cell 78: 303-316.
12. Digilio, F.A., Pannuti, A., Lucchesi, J.C., Furia, M., and Polito, L.C. 1996. Tosca: A Drosophila gene encoding a nuclease specifically expressed in the female germline. Dev. Biol. 178: 90-100.
13. Donovan, S., Harwood, J., Drury, L.S., and Diffley, J.F. 1997. Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Natl. Acad. Sci. 94: 5611-5616.
14. Feng, W., Collingwood, D., Boeck, M.E., Fox, L.A., Alvino, G.M., Fangman, W.L., Raghuraman, M.K., and Brewer, B.J. 2006. Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat. Cell Biol. 8: 148-155.
15. Fiorentini, P., Huang, K.N., Tishkoff, D.X., Kolodner, R.D., and Symington, L.S. 1997. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol. Cell. Biol. 17: 2764-2773.
16. Foiani, M., Pellicioli, A., Lopes, M., Lucca, C., Ferrari, M., Liberi, G., Muzi Falconi, M., and Plevani, P. 2000. DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae. Mutat. Res. 451: 187-196.
17. Friedman, K.L., Brewer, B.J., and Fangman, W.L. 1997. Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 667-678.
18. Gardner, R., Putnam, C.W., and Weinert, T. 1999. RAD53, DUN1 and PDS1 define two parallel G2/M checkpoint pathways in budding yeast. EMBO J. 18: 3173-3185.
19. Hartwell, L.H. and Kastan, M.B. 1994. Cell cycle control and cancer. Science 266: 1821-1828.
20. Jia, X., Weinert, T., and Lydall, D. 2004. Mec1 and Rad53 inhibit formation of single-stranded DNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 166: 753-764.
21. Kolodner, R.D., Putnam, C.D., and Myung, K. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297: 552-557.
22. Labib, K., Diffley, J.F., and Kearsey, S.E. 1999. G1-phase and B-type cyclins exclude the DNA-replication factor Mcm4 from the nucleus. Nat. Cell Biol. 1: 415-422.
23. Labib, K., Tercero, J.A., and Diffley, J.F. 2000. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288: 1643-1647.
24. Lieber, M.R. 1997. The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Bioessays 19: 233-240.
25. Lindsay, H.D., Griffiths, D.J., Edwards, R.J., Christensen, P.U., Murray, J.M., Osman, F., Walworth, N., and Carr, A.M. 1998. S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes & Dev. 12: 382-395.
26. Liu, Y., Vidanes, G., Lin, Y.C., Mori, S., and Siede, W. 2000. Characterization of a Saccharomyces cerevisiae homologue of Schizosaccharomyces pombe Chk1 involved in DNA-damage-induced M-phase arrest. Mol. Gen. Genet. 262: 1132-1146.
27. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C.S., and Foiani, M. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
28. Lowndes, N.F. and Murguia, J.R. 2000. Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10: 17-25.
29. Lucca, C., Vanoli, F., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Haber, J., and Foiani, M. 2004. Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23: 1206-1213.
30. Martinho, R.G., Lindsay, H.D., Flaggs, G., DeMaggio, A.J., Hoekstra, M.F., Carr, A.M., and Bentley, N.J. 1998. Analysis of Rad3 and Chk1 protein kinases defines different checkpoint responses. EMBO J. 17: 7239-7249.
31. Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald III, E.R., Hurov, K.E., Luo, J., Bakalarski, C.E., Zhao, Z., Solimini, N., Lerenthal, Y., et al. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166.
32. Moreau, S., Morgan, E.A., and Symington, L.S. 2001. Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159: 1423-1433.
33. Nyberg, K.A., Michelson, R.J., Putnam, C.W., and Weinert, T.A. 2002. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36: 617-656.
34. O'Connell, M.J., Walworth, N.C., and Carr, A.M. 2000. The G2-phase DNA-damage checkpoint. Trends Cell Biol. 10: 296-303.
35. Paulovich, A.G. and Hartwell, L.H. 1995. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82: 841-847.
36. Reynolds, A.E., McCarroll, R.M., Newlon, C.S., and Fangman, W.L. 1989. Time of replication of ARS elements along yeast chromosome III. Mol. Cell. Biol. 9: 4488-4494.
37. Rhind, N. and Russell, P. 2000. Chk1 and Cds1: Linchpins of the DNA damage and replication checkpoint pathways. J. Cell Sci. 113: 3889-3896.
38. Sanchez, Y., Bachant, J., Wang, H., Hu, F., Liu, D., Tetzlaff, M., and Elledge, S.J. 1999. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286: 1166-1171.
39. Santocanale, C. and Diffley, J.F. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395: 615-618.
40. Shirahige, K., Hori, Y., Shiraishi, K., Yamashita, M., Takahashi, K., Obuse, C., Tsurimoto, T., and Yoshikawa, H. 1998. Regulation of DNA-replication origins during cell-cycle progression. Nature 395: 618-621.
41. Smolka, M.B., Albuquerque, C.P., Chen, S.H., and Zhou, H. 2007. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. 104: 10364-10369.
42. Sogo, J.M., Lopes, M., and Foiani, M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
43. Szankasi, P. and Smith, G.R. 1992. A single-stranded DNA exonuclease from Schizosaccharomyces pombe. Biochemistry 31: 6769-6773.
44. Szankasi, P. and Smith, G.R. 1995. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267: 1166-1169.
45. Tercero, J.A. and Diffley, J.F. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412: 553-557.
46. Tercero, J.A., Labib, K., and Diffley, J.F. 2000. DNA synthesis at individual replication forks requires the essential initiation factor Cdc45p. EMBO J. 19: 2082-2093.
47. Tercero, J.A., Longhese, M.P., and Diffley, J.F. 2003. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11: 1323-1336.
48. Tishkoff, D.X., Boerger, A.L., Bertrand, P., Filosi, N., Gaida, G.M., Kane, M.F., and Kolodner, R.D. 1997. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. 94: 7487-7492.
49. Tishkoff, D.X., Amin, N.S., Viars, C.S., Arden, K.C., and Kolodner, R.D. 1998. Identification of a human gene encoding a homologue of Saccharomyces cerevisiae EXO1, an exonuclease implicated in mismatch repair and recombination. Cancer Res. 58: 5027-5031.
50. Tran, P.T., Erdeniz, N., Dudley, S., and Liskay, R.M. 2002. Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amst.) 1: 895-912.
51. Tsubouchi, H. and Ogawa, H. 2000. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11: 2221-2233.
52. Vernis, L., Piskur, J., and Diffley, J.F. 2003. Reconstitution of an efficient thymidine salvage pathway in Saccharomyces cerevisiae. Nucleic Acids Res. 31: e120. doi: 10.1093/nar/gng121.
53. Walworth, N.C. and Bernards, R. 1996. rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint. Science 271: 353-356.
54. Yamamoto, A., Guacci, V., and Koshland, D. 1996. Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae. J. Cell Biol. 133: 85-97.
55. Yamashita, M., Hori, Y., Shinomiya, T., Obuse, C., Tsurimoto, T., Yoshikawa, H., and Shirahige, K. 1997. The efficiency and timing of initiation of replication of multiple replicons of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 655-665.
56. Zhou, B.B. and Elledge, S.J. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.