Checkpoint-dependent regulation of origin firing and replication fork movement in response to DNA damage in fission yeast

Molecular and Cellular Biology

Volumn 29, Issue 2, 2009, Pages 602-611

  Kumart, Sanjay ^a,b   Huberman, Joel A ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; CDC10 GENE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CENTROMERE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TELOMERE; YEAST;

CDC25 PHOSPHATASES; CELL CYCLE PROTEINS; DNA DAMAGE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; METHYL METHANESULFONATE; PROTEIN-SERINE-THREONINE KINASES; REPLICATION ORIGIN; S PHASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TELOMERE; TRANSCRIPTION FACTORS;

SCHIZOSACCHAROMYCETACEAE;

EID: 58249107984     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01319-08     Document Type: Article

References (55)

1. Alcasabas, A. A., A. J. Osborn, J. Bacchant, F. Hu, P. J. H. Werler, K. Bousset, K. Furuya, J. F. X. Diffley, A. M. Carr, and S. J. Elledge. 2001. Mrcl transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3:958-965.
2. Alexandrow, M. G., and J. L. Hamlin. 2005. Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J. Cell Biol. 168:875-886.
3. Andreassen, P. R., G. P. H. Ho, and A. D. D'Andrea. 2006. DNA damage responses and their many interactions with the replication fork. Carcinogenesis 27:883-892.
4. Boddy, M. N., and P. Russell. 2001. DNA replication checkpoint. Curr. Biol. 11:R953-R956.
5. Brewer, B. J., and W. L. Fangman. 1987. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51:463-471.
6. Chahwan, C., T. M. Nakamura, S. Sivakumar, P. Russell, and N. Rhind. 2003. The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol. 23:6564-6573.
7. Costanzo, V., D. Shechter, P. J. Lupardus, K. A. Cimprich, M. Gottesman, and J. Gautier. 2003. An ATR- and Cdc7-dependent DNA damage check-point that inhibits initiation of DNA replication. Mol. Cell 11:203-213.
8. Duncker, B. P., K. Shimada, M. Tsai-Pflugfelder, P. Pasero, and S. M. Gasser. 2002. An N-terminal domain of Dbf4p mediates interaction with both origin recognition complex (ORC) and Rad53p and can deregulate late origin firing. Proc. Natl. Acad. Sci. USA 99:16087-16092.
9. Falck, J., N. Mailand, R. G. Syljuasen, J. Bartek, and J. Lukas. 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410:842-847.
10. Feng, W., D. Collingwood, M. E. Boeck, L. A. Fox, G. M. Alvino, W. L. Fangman, M. K. Raghuraman, and B. J. Brewer. 2006. Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat. Cell Biol. 8:148-155.
11. Furnari, B., A. Blasina, M. N. Boddy, C. H. McGowan, and P. Russell. 1999. Cdc25 inhibited in vivo and in vitro by checkpoint kinases Cds1 and Chk1. Mol. Biol. Cell 10:833-845.
12. cdc25, by a human protein-tyrosine phosphatase. Science 250:1573-1576.
13. Hayashi, M., Y. Katou, T. Itoh, M. Tazumi, Y. Yamada, T. Takahashi, T. Nakagawa, K. Shirahige, and H. Masukata. 2007. Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO J. 26:1327-1339.
14. Heffernan, T. P., K. Unsal-Kacmaz, A. N. Heinloth, D. A. Simpson, R. S. Paules, A. Sancar, M. Cordeiro-Stone, and W. K. Kaufmann. 2007. Cdc7- Dbf4 and the human checkpoint response to UVC. J. Biol. Chem. 282:9458-9468.
15. Heichinger, C., C. J. Penkett, J. Bähler, and P. Nurse. 2006. Genome-wide characterization of fission yeast DNA replication origins. EMBO J. 25:5171-5179.
16. Huberman, J. A., L. D. Spotila, K. A. Nawotka, S. M. El-Assouli, and L. R. Davis. 1987. The in vivo replication origin of the yeast 2μm plasmid. Cell 51:473-481.
17. Hyrien, O., and M. Mechali. 1992. Plasmid replication in Xenopus eggs and egg extracts: a 2D gel electrophoretic analysis. Nucleic Acids Res. 20:1463-1469.
18. Kalejta, R. F., and J. L. Hamlin. 1996. Composite patterns in neutral/neutral two-dimensional gels demonstrate inefficient replication origin usage. Mol. Cell. Biol. 16:4915-4922.
19. Katou, Y., Y. Kanoh, M. Bando, H. Noguchi, H. Tanaka, T. Ashikari, K. Sugimoto, and K. Shirahige. 2003. S-phase checkpoint proteins Tofl and Mrcl form a stable replication-pausing complex. Nature 424:1078-1083.
20. Kim, S.-M., D. D. Dubey, and J. A. Huberman. 2003. Early-replicating heterochromatin. Genes Dev. 17:330-335.
21. Kim, S. M., and J. A. Huberman. 2001. Regulation of replication timing in fission yeast. EMBO J. 20:6115-6126.
22. Kommajosyula, N., and N. Rhind. 2006. Cdc2 tyrosine phosphorylation is not required for the S-phase DNA damage checkpoint in fission yeast. Cell Cycle 5:2495-2500.
23. Kumar, S., and J. A. Huberman. 2004. On the slowing of S phase in response to DNA damage in fission yeast. J. Biol. Chem. 279:43574-43580.
24. Lambert, S., and A. M. Carr. 2005. Checkpoint responses to replicationfork barriers. Biochimie 87:591-602.
25. Larner, J. M., H. Lee, and J. L. Hamlin. 1994. Radiation effects on DNA synthesis in a defined chromosomal replicon. Mol. Cell. Biol. 14:1901-1908.
26. Lindsay, H. D., D. J. Griffiths, R. J. Edwards, P. U. Christensen, J. M. Murray, F. Osman, N. Walworth, and A. M. Carr. 1998. S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes Dev. 12:382-395.
27. Mailand, N., J. Falck, C. Lukas, R. G. Syljuasen, M. Welcker, J. Bartek, and J. Lukas. 2000. Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425-1429.
28. Marchetti, M. A., S. Kumar, E. Hartsuiker, M. Maftahi, A. M. Carr, G. A. Freyer, W. C. Burhans, and J. A. Huberman. 2002. A single unbranched S-phase DNA damage and replication fork blockage checkpoint pathway. Proc. Natl. Acad. Sci. USA 99:7472-7477.
29. Masai, H., E. Matsui, Z. You, Y. Ishimi, K. Tamai, and K. Arai. 2000. Human Cdc7-related kinase complex. In vitro phosphorylation of MCM by concerted actions of Cdks and Cdc7 and that of a critical threonine residue of Cdc7 by Cdks J. Biol. Chem. 275:29042-29052.
30. Matsumoto, S., K. Ogino, E. Noguchi, P. Russell, and H. Masai. 2005. Hsk1-Dfp1/Him1, the Cdc7-Dbf4 kinase in Schizosaccharomyces pombe, associates with Swi1, a component of the replication fork protection complex. J. Biol. Chem. 280:42536-42542.
31. Merrick, C. J., D. Jackson, and J. F. X. Diffley. 2004. Visualization of altered replication dynamics after DNA damage in human cells. J. Biol. Chem. 279:20067-20075.
32. Mickle, K. L., S. Ramanathan, A. Rosebrock, A. Oliva, A. Chaudari, C. Yompakdee, D. Scott, J. Leatherwood, and J. A. Huberman. 2007. Check-point-independence of most DNA replication origins in fission yeast. BMC Mol. Biol. 8:112.
33. Noguchi, E., C. Noguchi, W. H. McDonald, J. R. Yates III, and P. Russell. 2004. Swi1 and Swi3 are components of a replication fork protection complex in fission yeast. Mol. Cell. Biol. 24:8342-8355.
34. Olson, E., C. J. Nievera, A. Y. L. Lee, L. Chen, and X. Wu. 2007. The Mre11-Rad50-Nbs1 complex acts both upstream and downstream of ataxia telangectasia mutated and Rad3-related protein (ATR) to regulate the S-phase checkpoint following UV treatment. J. Biol. Chem. 282:22939-22952.
35. Patel, P. K., B. Arcangioli, S. P. Baker, A. Bensimon, and N. Rhind. 2006. DNA replication origins fire stochastically in fission yeast. Mol. Biol. Cell 17:308-316.
36. 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.
37. 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.
38. Raghuraman, M. K., E. A. Winzeler, D. Collingwood, S. Hunt, L. Wodicka, A. Conway, D. J. Lockhart, R. W. Davis, B. J. Brewer, and W. L. Fangman. 2001. Replication dynamics of the yeast genome. Science 294:115-121.
39. Rhind, N., and P. Russell. 2000. Checkpoints: it takes more than time to heal some wounds. Curr. Biol. 10:R908-R911.
40. Rhind, N., and P. Russell. 1998. Tyrosine phosphorylation of Cdc2 is required for the replication checkpoint in Schizosaccharomyces pombe. Mol. Cell. Biol. 18:3782-3787.
41. Santocanale, C., and J. F. Diffley. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395:615-618.
42. Seiler, J. A., C. Conti, A. Syed, M. I. Aladjem, and Y. Pommier. 2007. The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol. Cell. Biol. 27:5806-5818.
43. Shikata, M., F. Ishikawa, and J. Kanoh. 2007. Tel2 Is required for activation of the Mrc1-mediated replication checkpoint. J. Biol. Chem. 282:5346-5355.
44. Shimura, T., M. M. Martin, M. J. Torres, C. Gu, J. M. Pluth, M. A. DiBernardi, J. S. McDonald, and M. I. Aladjem. 2007. DNA-PK is involved in repairing a transient surge of DNA breaks induced by deceleration of DNA replication. J. Mol. Biol. 367:665-680.
45. Shirahige, K., Y. Hori, K. Shiraishi, M. Yamashita, K. Takahashi, C. Obuse, T. Tsurimoto, and H. Yoshikawa. 1998. Regulation of DNA-replication origins during cell-cycle progression. Nature 395:618-621.
46. Snaith, H. A., G. W. Brown, and S. L. Forsburg. 2000. Schizosaccharomyces pombe Hsk1p is a potential Cds1p target required for genome integrity. Mol. Cell. Biol. 20:7922-7932.
47. Sommariva, E., T. K. Pellney, N. Karahan, S. Kumar, J. A. Huberman, and J. Z. Dalgaard. 2005. Schizosaccharomyces pombe Swi1, Swi3, and Hsk1 are components of a novel S-phase response pathway to alkylation damage. Mol. Cell. Biol. 25:2770-2784.
48. Stracker, T. H., J. W. Theunissen, M. Morales, and J. H. Petrini. 2004. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair 3:845-854.
49. Szyjka, S. J., J. G. Aparicio, C. J. Viggiani, S. Knott, W. Xu, S. Tavaré, and O. M. Aparicio. 2008. Rad53 regulates replication fork restart after DNA damage in Saccharomyces cerevisiae. Genes Dev. 22:1906-1920.
50. +, encoding a regulatory subunit for Hsk1 kinase, plays essential roles in S-phase initiation as well as in S-phase checkpoint control and recovery from DNA damage. Mol. Cell. Biol. 19:5535-5547.
51. Takeda, T., K. Ogino, K. Tatebayashi, H. Ikeda, K.-I. Arai, and H. Masai. 2001. Regulation of initiation of S phase, replication checkpoint signaling, and maintenance of mitotic chromosome structures during S phase by Hsk1 kinase in the fission yeast. Mol. Biol. Cell 12:1257-1274.
52. Tanaka, K., and P. Russell. 2001. Mrc1 channels the DNAreplicationarrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3:966-972.
53. Tercero, J. A., and J. F. Diffley. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412:553-557.
54. Unsal-Kacmaz, K., P. D. Chastain, P. P. Qu, P. Minoo, M. Cordeiro-Stone, A. Sancar, and W. K. Kaufmann. 2007. The human Tim/Tipin complex coordinates an intra-S checkpoint response to UV that slows replication fork displacement. Mol. Cell. Biol. 27:3131-3142.
55. Weinreich, M., and B. Stillman. 1999. Cdc7p-Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway. EMBO J. 18:5334-5346.