The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage

EMBO Journal

Volumn 17, Issue 19, 1998, Pages 5679-5688

  Vialard, Jorge E ^a,b   Gilbert, Christopher S ^a   Green, Catherine M ^a   Lowndes, Noel F ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b JANSSEN RESEARCH FOUNDATION   (Belgium)

Author keywords

Checkpoint; DNA damage; MEC1; Phosphorylation; RAD9

Indexed keywords

MESYLIC ACID METHYL ESTER; PHOSPHATASE; POLYCLONAL ANTIBODY; PROTEIN;

ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENETIC TRANSCRIPTION; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; ULTRAVIOLET RADIATION;

CELL CYCLE PROTEINS; DNA DAMAGE; FUNGAL PROTEINS; G2 PHASE; GAMMA RAYS; HYDROXYUREA; METHYL METHANESULFONATE; MITOSIS; MUTAGENS; MUTATION; NOCODAZOLE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; ULTRAVIOLET RAYS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0032189952     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.19.5679     Document Type: Article

References (47)

1. Aboussekhra, A., Vialard, J.E., Morrison, D.E., de la Torre-Ruiz, M.A., Cernakova, L., Fabre, F. and Lowndes, N.F. (1996) A novel role for the budding yeast RAD9 checkpoint gene in DNA damage-dependent transcription. EMBO J., 15, 3912-3922.
2. 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.
3. Bentley, N.J., Holtzman, D.A., Flaggs, G., Keegan, K.S., DeMaggio, A., Ford, J.C., Hoekstra, M. and Carr, A.M. (1996) The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J., 15, 6641-6651.
4. Bork, P., Hofmann, K., Bucher, P., Neuwald, A.F., Altschul, S.F. and Koonin, E.V. (1997) A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J., 11, 68-76.
5. Brush, G.S., Morrow, D.M., Hieter, P. and Kelly, T.J. (1996) The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proc. Natl Acad. Sci. USA, 93, 15075-15080.
6. Cahill, D.P., Lengauer, C., Yu, J., Riggins, G.J., Willson, J.K.V., Markowitz, S.D., Kinzler, K.W. and Vogelstein, B. (1998) Mutation of mitotic checkpoint genes in human cancers. Nature, 392, 300-303.
7. Callebaut, I. and Mornon, J.P. (1997) From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett., 400, 25-30.
8. Cohen-Fix, O. and Koshland, D. (1997) The anaphase inhibitor of Saccharomyces cerevisiae Pds1 is a target of the DNA damage checkpoint pathway. Proc. Natl Acad. Sci. USA, 94, 14361-14366.
9. Critchlow, S.E., Bowater, R.P. and Jackson, S.P. (1997) Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA lisase IV. Curr. Biol., 7, 588-598.
10. de la Torre-Ruiz, M.-A., Green, C.M. and Lowndes, N.F. (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.
11. Elledge, S.J. (1996) Cell cycle checkpoints: preventing an identity crisis. Science, 274, 1664-1672.
12. Futreal, P.A. et al. (1994) BRCA1 mutations in primary breast and ovarian carcinomas. Science, 266, 120-122.
13. Greenwell, P.W., Kronmal, S.L., Porter, S.E., Gassenhuber, J., Obermaier, B. and Petes, T.D. (1995) TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell, 82, 823-829.
14. Griffiths, D.J., Barbet, N.C. McCready, S., Lehmann, A.R. and Carr, A.M. (1995) Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO J., 14, 5812-5823.
15. Hartwell, L.H. and Kastan, M.B. (1994) Cell cycle control and cancer. Science, 266, 1821-1828.
16. Hunter, T. (1995) When is a lipid kinase not a lipid kinase? When it is a protein kinase. Cell, 83, 1-4.
17. Jung, M., Kondratyev, A., Lee, S.A., Dimtchev, A. and Dritschilo, A. (1997) ATM gene product phosphorylates I kappa B-alpha. Cancer Res., 57, 24-27.
18. Keegan, K.S. et al. (1990) The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev., 10, 2423-2437.
19. Kiser, G.L. and Weinert, T.A. (1996) Distinct roles of yeast MEC and RAD checkpoint genes in transcriptional induction after DNA damage and implications for function. Mol. Biol. Cell, 7, 703-718.
20. Koonin, E.V., Altschul, S.F. and Bork, P. (1996) BRCA1 protein products: Functional motifs. Nature Genet., 13, 266-268.
21. Longhese, M.P., Paciotti, V. Fraschini, R., Zaccarini, 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.
22. Lydall, D. and Weinert, T. (1995) Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science, 270, 1488-1491.
23. Miki, Y. et al. (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science, 266, 66-71.
24. Morgan, S.E. and Kastan, M.B. (1997) p53 and ATM: cell cycle, cell death and cancer. Adv. Cancer Res., 71, 1-25.
25. Morrow, D.M., Tagle, D.A.. Shiloh, Y. Collins, F. and Hieter, P. (1995) TEL1, an S.cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell, 82, 831-840.
26. Nash, R.A., Caldecott, K.W., Barnes, D.E. and Lindahl, T. (1997) XRCC1 protein interacts with one of two distinct forms of DNA ligase III. Biochemistry, 36, 5207-5211.
27. Navas, T.A., Sanchez, Y and Elledge, S.J. (1996) RAD9 and DNA polymerase epsilon form parallel sensory branches tor transducing the DNA damage checkpoint signal in Saccharomyces cerevisiae. Genes Dev., 10, 2632-2643.
28. Pati, D., Keller, C., Groudine, M. and Plon, S.E. (1997) Reconstitution of a MEC1-independent checkpoint in yeast by expression of a novel human fork head cDNA. Mol. Cell. Biol., 17, 3037-3046.
29. 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.
30. Paulovich, A.G., Margulies, R.U., Garvik, B.M. and Hartwell, L.H. (1997a) RAD9, RAD17 and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics, 145, 45-62.
31. Paulovich, A.G., Toczyski, D.P. and Hartwell, L.H. (1997b) When checkpoints fail. Cell, 88, 315-321.
32. Rudner, A.D. and Murray, A.W. (1996) The spindle assembly checkpoint. Curr. Opin. Cell Biol., 8. 773-780.
33. Ruffner, H. and Verma, I.M. (1997) BRCA1 is a cell cycle-regulated nuclear phosphoprotein. Proc. Natl Acad. Sci. USA, 94, 7138-7143.
34. Saka, Y., Esashi, F. Matsusaka, T., Mochida, S. and Yanagida, M. (1998) Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chkl. Genes Dev., 11, 3387-3400.
35. Sanchez, Y. Desany, B.A., Jones, W.J., Liu, Q., Wang, B. and Elledge, S.J. (1996) Resulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science, 271, 357-360.
36. Scully, R., Chen, J., Ochs, R.L., Keegan, K., Hoekstra, M., Feunteun, J. and Livingston, D.M. (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell, 90, 425-435.
37. 1 arrest defines a second checkpoint for damaged DNA in the cell cycle of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 90, 7985-7989.
38. Sun, Z., Fay, D.S., Marini, F., Foiani, M. and Stern, D.F. (1996) Spk1/Rad53 is regulated bv Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev., 10, 395-406.
39. Sun, Z., Hsiao, J., Fay, D.S. and Stern, D.F. (1998) Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science, 281, 272-274
40. Thelen, M.P., Onel, K. and Holloman, W.K. (1994) The REC1 gene of Ustilago maydis involved in the cellular response to DNA damage encodes an exonuclease. J. Biol. Chem., 269, 747-754.
41. Weinert, T.A. and Hartwell, L.H. (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science, 241, 317-322.
42. Weinert, T.A. and Hartwell, L.H. (1990) Characterization of RAD9 of Saccharomyces cerevisiae and evidence that its function acts posttranslationally in cell cycle arrest after DNA damage. Mol. Cell. Biol., 10, 6554-6564.
43. Weinert, T.A., Kiser, G.L. and Hartwell, L.H. (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev., 8, 652-665.
44. Willson, J., Wilson, S., Warr, N. and Watts, F.Z. (1997) Isolation and characterization of the Schizosaccharomyces pombe rhp9 gene: a gene required for the DNA damage checkpoint but not the replication checkpoint. Nucleic Acids Res., 25, 2138-2146.
45. Yamamoto, A., Guacci, V. and Koshland, D. (1996) Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J. Cell Biol., 133, 99-110.
46. Yang, S.S.. Yeh, E., Salmon, E.D. and Bloom, K. (1997) Identification of a mid-anaphase checkpoint in budding yeast. J. Cell Biol., 136, 345-354.
47. Zhou, Z. and Elledge, S.J. (1993) DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell, 75, 1119-1127.