Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase

EMBO Journal

Volumn 18, Issue 22, 1999, Pages 6561-6572

  Pellicioli, Achille ^a   Lucca, Chiara ^a   Liberi, Giordano ^a   Marini, Federica ^a,b   Lopes, Massimo ^a   Plevani, Paolo ^a   Romano, Alfredo ^c   Di Fiore, Pier Paolo ^c   Foiani, Marco ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

Checkpoints; DNA damage; DNA polymerase primase; DNA replication; Rad53

Indexed keywords

DNA POLYMERASE; PROTEIN KINASE; PROTEIN RAD 53 KINASE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

CELL CYCLE; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; ENZYME ACTIVATION; FUNGAL PROTEINS; G1 PHASE; GENOTYPE; MODELS, GENETIC; MUTAGENESIS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 0033570894     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.22.6561     Document Type: Article

References (51)

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, 2416-2428.
2. Brush, G., Morrow, D.M., Heiter, P. and Kelly, T.J. (1996) The ATM homolog MECI is required for phosphorylation of replication protein A in yeast. Proc. Natl Acad. Sci. USA, 93, 15075-15080.
3. Burke, D.J. and Church, D. (1991) Protein synthesis requirements for nuclear division, cytokinesis,and cell separation in Saccharomyces cerevisiae. Mol. Cell. Biol., 11, 3691-3698.
4. Carr, A. and Hoekstra, M.F. (1995) The cellular response to DNA damage. Trends Cell Biol., 5, 32-40.
5. Cheng, L., Collyer, T. and Hardy, C.F.J. (1999) Cell cycle regulation of DNA replication initiator factor Dbf4p. Mol. Cell. Biol., 19, 4270-4278.
6. Desdouets, C., Santocanale, C., Drury, L.S., Perkins, G., Foiani, M., Plevani, P. and Diffley, J.F.X. (1998) Evidence for a Cdc6-independent mitotic resetting event involving DNA polymerase α. EMBO J., 17, 4139-4146.
7. Din, S.U., Brill, S.J., Fairman, M.P. and Stillman, B. (1990) Cell cycle regulated phosphorylation of DNA replication factor A from human and yeast cells. Genes Dev., 4, 968-977.
8. Dohrmann, P.R., Oshiro, G., Tecklenburg, M. and Sclafani, R.A. (1999) RAD53 regulates DBF4 independently of checkpoint function in Saccharomyces cerevisiae. Genetics, 151, 965-977.
9. Dorneiter, I., Erdile, L.F., Gilbert, U., von Winkler, D., Kelly, T.J. and Fanning,E. (1992) Interactions of DNA polymerase α-primase with replication protein A and SV40 T antigen. EMBO J., 11, 769-776.
10. Elledge, S.J. (1996) Cell cycle checkpoints: preventing an identity crisis. Science, 274, 1664-1672.
11. Ferrari, M., Lucchini, G., Plevani, P. and Foiani, M. (1996) Phosphorylation of the DNA polymerase α-primase B subunit is dependent on its association with the p180 polypeptide. J. Biol. Chem., 15, 8661-8666.
12. Ferrell, J.E., Jr and Martin, G.S. (1991) Assessing activities of blotted protein kinases. Methods Enzymol., 200, 430-435.
13. Foiani, M., Liberi, G., Lucchini, G. and Plevani, P. (1995) Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase α-primase B subunit. Mol. Cell. Biol., 15, 883-891.
14. Foiani, M., Lucchini, G. and Plevani, P. (1997) The DNA polymerase α-primase complex couples DNA replication, cell cycle progression and DNA-damage response. Trends Biochem. Sci., 22, 424-427.
15. Foiani, M., Ferrari, M., Liberi, G., Lopes, M., Lucca, C., Marini, F., Pellicioli, A., Muzi-Falconi, M. and Plevani, P. (1998) S-phase DNA damage checkpoint in budding yeast. Biol. Chem., 379, 1019-1023.
16. Foiani, M., Liberi, G., Piatti, S. and Plevani, P. (1999) Saccharomyces cerevisiae as a model system to study DNA replication. In Cotterill, S. (ed.), Eukaryotic DNA. Replication. A Practical Approach. Oxford University Press, Oxford, UK, pp. 185-200.
17. 2 cell cycle arrested yeast cells. Mutat. Res., 354, 69-75.
18. Gietz, R.D. and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six base-pair restriction sites. Gene, 74, 527-534.
19. Hartwell, L.H. and Kastan, M.B. (1994) Cell cycle controls and cancer. Science, 266, 1821-1828.
20. Hereford, L.M. and Hartwell, L.H. (1974) Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J. Mol. Biol., 84, 445-461.
21. Holmes, A.M. and Haber,J.E. (1999) Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell, 96, 415-424.
22. Kesti, T., Flick, K., Keranen, S., Syvaoja, J.E. and Wittenberg, C. (1999) DNA polymerase ε catalytic domains are dispensable for DNA replication, DNA repair and cell viability. Mol Cell, 3, 679-685.
23. Kogoma, T. (1997) Stable DNA replication: interplay between DNA replication, homologous recombination and transcription. Microbiol. Rev., 61, 212-238.
24. 1/S and intra-S DNA damage checkpoints in budding yeast. Nucleic Acids Res., 24, 3533-3537.
25. Longhese, M.P., Paciotti, V., Fraschini, R., Plevani, P. and Lucchini, G. (1997) The novel DNA damage checkpoint protein Ddc1p is phosphorylated periodically during the cell cycle and in response to DNA damage in budding yeast. EMBO J., 16, 5216-5226.
26. Longhese, M.P., Foiani, M., Muzi-Falconi, M., Lucchini, G. and Plevani, P. (1998) DNA damage checkpoint in budding yeast. EMBO J., 17, 5525-5528.
27. 2TM checkpoint genes of Saccharomyces cerevisiae: further evidence for roles in DNA replication and/or repair. Mol. Gen. Genet., 256, 638-651.
28. Malkova, A., Ivanov, E.L. and Haber, J.E. (1996) Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl Acad. Sci. USA, 93, 7131-7136.
29. Marini, F., Pellicioli, A., Paciotti, V., Lucchini, G., Plevani, P., Stern, D.F. and Foiani, M. (1997) A role for DNA primase in coupling DNA replication to DNA damage response. EMBO J., 16, 639-650.
30. Murray, A.W. and Hunt, T. (1993) The Cell Cycle. W.H.Freeman & Co., New York, NY.
31. Navas, T.A., Zhou, Z. and Elledge, S. (1995) DNA polymerase E links the DNA replication machinery to the S phase checkpoint. Cell, 80, 29-39.
32. Navas, T.A., Sanchez, Y. and Elledge, S.J. (1996) RAD9 and DNA polymerase ε form parallel sensory branches for transducing the DNA damage checkpont signal in Saccharomyces cerevisiae. Genes Dev., 10, 2632-2643.
33. Nelson, W.G. and Kastan, M.B. (1994) DNA strand-breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol., 14, 1815-1823.
34. Paciotti, V., Lucchini, G., Plevani, P. and Longhese, M.P. (1998) Mec1p is essential for phosphorylation of the yeast DNA damage checkpoint protein Ddc1p, which physically interacts with Mec3p. EMBO J., 17, 4199-4209.
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. Paulovich, A.G., Toczyski, D.P. and Hartwell, L.H. (1997) When checkpoints fail. Cell, 88, 315-321.
37. Sanchez, Y., Desany, B.A., Jones, W.J., Liu, Q., Wang, B. and Elledge, S.J. (1996) Regulation of RAD53 by the ATM-like kinases MECI and TELI in yeast cell cycle checkpoint pathways. Science, 271, 357-360.
38. Santocanale, C. and Diffley, J.F.X. (1998) A Mec1- and Rad53-dependent checkpoint controls late-origin firing origins of DNA replication. Nature, 395, 615-618.
39. 1 to S transition in S.cerevisiae. Cell, 79, 233-244.
40. Seigneur, M., Bidnenko, V., Ehrlich, S.D. and Michel, B. (1998) RuvAB acts at arrested replication forks. Cell, 95, 419-430.
41. Shiraige, 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.
42. Smith, G.C.M. and Jackson, S. (1999) The DNA-dependent protein kinase. Genes Dev., 13, 916-934.
43. Sun, Z., Fay, D.S., Marini, F., Foiani, M. and Stern, D.F. (1996)Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and DNA damage checkpoint pathway. Genes Dev., 10, 395-406.
44. Sun, Z., Hsiao, J., Fay, D.S. and Stern, D.F. (1998) Rad53 FHA domain is associated with phosphorylated Rad9 in the DNA damage checkpoint. Science, 281, 272-274.
45. Thelen, M.P, Venclovas, C. and Fidelis, K. (1999) A sliding clamp model for the Rad1 family of cell cycle checkpoint proteins. Cell, 96, 769-770.
46. Vialard, J.E., Gilbert, C.S., Green, C.M. and Lowndes, N.F. (1998) The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tell-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J., 17, 5679-5688.
47. Waga, S. and Stillman, B. (1998) The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem., 67, 721-751.
48. Weinert, T. (1997) Yeast checkpoints controls and relevance to cancer. Cancer Surv., 29, 109-132.
49. Weinert, T. (1998) DNA damage checkpoints update: getting molecular Curr. Opin. Genet. Dev., 8, 185-193.
50. Weinert, J.A., Kiser, G.L. and Hartwell, L.H. (1994) Mitotic checkpoints in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev., 8, 652-665.
51. Wold, M.S. (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding potein required for eukaryotic DNA metabolism. Annu. Rev. Biochem., 66, 61-92.