Direct kinase-to-kinase signaling mediated by the FHA phosphoprotein recognition domain of the Dun1 DNA damage checkpoint kinase

Molecular and Cellular Biology

Volumn 23, Issue 4, 2003, Pages 1441-1452

  Bashkirov, Vladimir I ^a,b   Bashkirova, Elena V ^a,c   Haghnazari, Edwin ^a   Heyer, Wolf Dietrich ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^c Novozymes Biotech Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HYDROXYUREA; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE DUN1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME PHOSPHORYLATION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; YEAST;

CELL CYCLE; CELL CYCLE PROTEINS; DNA DAMAGE; METHYL METHANESULFONATE; MUTATION; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 0037312919     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.4.1441-1452.2003     Document Type: Article

References (61)

1. Aboussekhra, A., J. E. Vialard, D. E. Morrison, M. A. Delatorreruiz, L. Cernakova, F. Fabre, and N. F. Lowndes. 1996. A novel role for the budding yeast RAD9 checkpoint gene in DNA damage-dependent transcription. EMBO J. 15:3912-3922.
2. Ahn, J.-Y., X. Li, H. L. Davis, and C. E. Canman. 2002. Phosphorylation of threonine 68 promotes oligomerization and autophosphorylation of the Chk2 protein kinase via the forkhead-associated domain. J. Biol. Chem. 277:19389-19395.
3. Alcasabas, A. A., A. J. Osborn, J. Bachant, F. H. Hu, P. J. H. Werler, K. Bousset, K. Furuya, J. F. X. Diffley, A. M. Carr, and S. J. Elledge. 2001. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3:958-965.
4. Allen, J. B., Z. Zhou, W. Siede, E. C. Friedberg, and S. J. Elledge. 1994. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev. 8:2401-2415.
5. Bashkirov, V. I., J. S. King, E. V. Bashkirova, J. Schmuckli-Maurer, and W. D. Heyer. 2000. DNA repair protein Rad55 is a terminal substrate of the DNA damage checkpoints. Mol. Cell. Biol. 20:4393-4404.
6. Bell, D. W., J. M. Varley, T. E. Szydlo, D. H. Kang, D. C. R. Wahrer, K. E. Shannon, M. Lubratovich, S. J. Verselis, K. J. Isselbacher, J. F. Fraumeni, J. M. Birch, F. P. Li, J. E. Garber, and D. A. Haber. 1999. Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science 286:2528-2531.
7. Boddy, M. N., A. Lopez-Girona, P. Shanahan, H. Interthal, W. D. Heyer, and P. Russell. 2000. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20:8758-8766.
8. Craven, R. J., and T. D. Petes. 2000. Involvement of the checkpoint protein Mec1p in silencing of gene expression at telomeres in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:2378-2384.
9. Desany, B., 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. Genes0 Dev. 12:2956-2970.
10. Dohlman, H. G., and J. W. Thorner. 2001. Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu. Rev. Biochem. 70:703-754.
11. Durocher, D., J. Henckel, A. R. Fersht, and S. P. Jackson. 1999. The FHA domain is a modular phosphopeptide recognition motif. Mol. Cell 4:387-394.
12. Durocher, D., I. A. Taylor, D. Sarbassova, L. F. Haire, S. L. Westcott, S. P. Jackson, S. J. Smerdon, and M. B. Yaffe. 2000. The molecular basis of FHA domain-phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol. Cell 6:1169-1182.
13. Emili, A. 1998. MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol. Cell 2:183-189.
14. Ferrell, J. E. 1996. Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem. Sci. 21:460-466.
15. Fikus, M. U., P. A. Mieczkowski, P. Koprowski, J. Rytka, E. Sledziewska-Gojska, and Z. Ciesla. 2000. The product of the DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, specifically functions in mitochondria. Genetics 154:73-81.
16. 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. 11:3173-3185.
17. Garvik, B., M. Carson, and L. Hartwell. 1995. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 15:6128-6138.
18. Gilbert, C. S., C. M. Green, and N. F. Lowndes. 2001. Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell 8:129-136.
19. Gyuris, J., E. Golemis, H. Chertkov, and R. Brent. 1993. Cdi1, a human G1-phase and S-phase protein phosphatase that associates with Cdk2. Cell 75:791-803.
20. Haber, J. E. 1999. Sir-Ku-itous routes to make ends meet. Cell 97:829-832.
21. Hammet, A., B. L. Pike, and J. Heierhorst. 2002. Posttranscriptional regulation of the RAD5 DNA repair gene by the Dun1 kinase and the Pan2-Pan3 poly(A)-nuclease complex contributes to survival of replication blocks. J. Biol. Chem. 277:22469-22474.
22. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
23. Ho, Y., A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. Y. Yang, C. Wolting, I. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano, D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sorensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. V. Hogue, D. Figeys, and M. Tyers. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
24. Hofmann, K., and P. Bucher. 1995. The FHA domain: a putative nuclear signalling domain found in protein kinases and transcription factors. Trends. Biochem. Sci. 20:347-349.
25. Huang, M., and S. J. Elledge. 2000. The FHA domain, a phosphoamino acid binding domain involved in the DNA damage response pathway. CSHSQB 65:413-421.
26. Huang, M., Z. Zhou, and S. J. Elledge. 1998. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 94:595-605.
27. Huang, M. X., and S. J. Elledge. 1997. Identification of RNR4, encoding a second essential small subunit of ribonucleotide reductase in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:6105-6113.
28. Huse, M., and J. Kuriyan. 2002. The conformational plasticity of protein kinases. Cell 109:275-282.
29. Li, J., G.-I. Lee, S. R. Van Doren, and J. C. Walker. 2000. The FHA domain mediates phosphoprotein interactions. J. Cell Sci. 113:4143-4149.
30. Li, J. J., B. L. Williams, L. F. Haire, M. Goldberg, E. Walker, D. Durocher, M. B. Yaffe, S. P. Jackson, and S. J. Smerdon. 2002. Structural and functional versatility of the FHA domain in DNA-damage signaling by the tumor suppressor kinase Chk2. Mol. Cell 9:1045-1054.
31. Lowndes, N. F., and J. R. Murguia. 2000. Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10:17-25.
32. Madhani, H. D., and G. R. Fink. 1998. The riddle of MAP kinase signaling specificity. Trends Genet. 14:151-155.
33. Mallory, J. C., and T. D. Petes. 2000. Protein kinase activity of Tel1p and Mec1p, two Saccharomyces cerevisiae proteins related to the human ATM protein kinase. Proc. Natl. Acad. Sci. USA 97:13749-13754.
34. Matsuoka, S., G. Rotman, A. Ogawa, Y. Shiloh, K. Tamai, and S. J. Elledge. 2000. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. USA 97:10389-10394.
35. Myung, K., A. Datta, and R. D. Kolodner. 2001. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104:397-408.
36. Paciotti, V., M. Clerici, M. Scotti, G. Lucchini, and M. P. Longhese. 2001. Characterization of mec1 kinase-deficient mutants and of new hypomorphic mec1 alleles impairing subsets of the DNA damage response pathway. Mol. Cell. Biol. 21:3913-3925.
37. Pellicioli, A., S. B. Lee, C. Lucca, M. Foiani, and J. E. Haber. 2001. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell 7:293-300.
38. Pellicioli, A., C. Lucca, G. Liberi, F. Marini, M. Lopes, P. Plevani, A. Romano, P. P. Di Fiore, and M. Foiani. 1999. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18:6561-6572.
39. Pike, B. L., A. Hammet, and J. Heierhorst. 2001. Role of the N-terminal forkhead-associated domain in the cell cycle checkpoint function of the Rad53 kinase. J. Biol. Chem. 276:14019-14026.
40. Rhind, N., and P. Russell. 1998. Mitotic DNA damage and replication checkpoints in yeast. Curr. Opin. Cell Biol. 10:749-758.
41. Sanchez, Y., J. Bachant, H. Wang, F. H. Hu, D. Liu, M. Tetzlaff, and S. J. Elledge. 1999. Control of the DNA damage checkpoint by Chk1 and Rad53 protein kinases through distinct mechanisms. Science 286:1166-1171.
42. Sanchez, Y., B. A. Desany, W. J. Jones, Q. H. 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.
43. Sanchez, Y., Z. Zhou, M. X. Huang, B. E. Kemp, and S. J. Elledge. 1997. Analysis of budding yeast kinases controlled by DNA damage. Methods Enzymol. 283:398-410.
44. Scherer, S., and R. W. Davis. 1979. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc. Natl. Acad. Sci. USA 76:4951-4955.
45. Schwartz, M. F., J. K. Duong, Z. X. Sun, J. S. Morrow, D. Pradhan, and D. F. Stern. 2002. Rad9 phosphorylation sites couple Rad53 to the Saccharomyces cerevisiae DNA damage checkpoint. Mol. Cell 9:1055-1065.
46. Solinger, J. A., G. Lutz, T. Sugiyama, S. C. Kowalczykowski, and W.-D. Heyer. 2001. Rad54 protein stimulates heteroduplex DNA formation in the synaptic phase of DNA strand exchange via specific interactions with the presynaptic Rad51 nucleoprotein filament. J. Mol. Biol. 307:1207-1221.
47. Stavridi, E. S., Y. Huyen, I. R. Loreto, D. M. Scolnick, T. D. Halazonetis, N. P. Pavletich, and P. D. Jeffrey. 2002. Crystal structure of the FHA domain of the Chfr mitotic checkpoint protein and its complex with tungstate. Structure 10:891-899.
48. Sun, Z. X., D. S. Fay, F. Marini, M. Foiani, and D. F. Stern. 1996. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev. 10:395-406.
49. Sun, Z. X., J. Hsiao, D. S. Fay, and D. F. Stern. 1998. Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science 281:272-274.
50. Tanaka, K., M. N. Boddy, X. B. Chen, C. H. McGowan, and P. Russell. 2001. Threonine-11, phosphorylated by Rad3 and ATM in vitro, is required for activation of fission yeast checkpoint kinase Cdsl. Mol. Cell. Biol. 21:3398-3404.
51. Tsai, M.-D. 2002. FHA: a signal transduction domain with diverse specificity and function. Structure 10:887-889.
52. Usui, T., H. Ogawa, and J. H. J. Petrini. 2001. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell 7:1255-1266.
53. Vialard, J. E., C. S. Gilbert, C. M. Green, and N. F. Lowndes. 1998. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J. 17:5679-5688.
54. Wang, P., I. J. L. Byeon, H. Liao, K. D. Beebe, S. Yongkiettrakul, D. Pei, and M. D. Tsai. 2000. Structure and specificity of the interaction between the FHA2 domain of Rad53 and phosphotyrosyl peptides. J. Mol. Biol. 302:927-940.
55. Weinert, T. 1998. DNA damage checkpoints update: getting molecular. Curr. Opin. Genet. Dev. 8:185-193.
56. Wolter, R., W. Siede, and M. Brendel. 1996. Regulation of SNM1, an inducible Saccharomyces cerevisiae gene required for repair of DNA cross-links. Mol. Gen. Genet. 250:162-168.
57. Xu, X., L. M. Tsvetkov, and D. F. Stern. 2002. Chk2 activation and phosphorylation-dependent oligomerization. Mol. Cell. Biol. 22:4419-4432.
58. Zhao, X. L., E. G. D. Muller, and R. Rothstein. 1998. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2:329-340.
59. Zheng, P., D. S. Fay, J. Burton, H. Xiao, J. L. Pinkham, and D. F. Stern. 1993. SPK1 is an essential S-phase-specific gene of Saccharomyces cerevisiae that encodes a nuclear serine/threonine/tyrosine kinase. Mol. Cell. Biol. 13:5829-5842.
60. Zhou, B. B. S., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
61. Zhou, Z., and S. J. Elledge. 1993. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75:1119-1127.