Rad53 phosphorylation site clusters are important for Rad53 regulation and signaling

Molecular and Cellular Biology

Volumn 23, Issue 17, 2003, Pages 6300-6314

  Lee, Soo Jung ^a   Schwartz, Marc F ^a,b   Duong, Jimmy K ^a   Stern, David F ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; DNA; PROTEIN DUN1; PROTEIN KINASE; PROTEIN MEC1; PROTEIN TEL1; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; FUNGAL CELL; GENE ACTIVATION; GENE CONTROL; GENE FUNCTION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; YEAST;

ALANINE; AMINO ACID SUBSTITUTION; BINDING SITES; CELL CYCLE PROTEINS; DNA DAMAGE; FUNGAL PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MUTATION; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION;

SACCHAROMYCETALES;

EID: 0042470439     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.17.6300-6314.2003     Document Type: Article

References (76)

1. Ahn, J., and C. Prives. 2002. Checkpoint kinase 2 (Chk2) monomers or dimers phosphorylate Cdc25C after DNA damage regardless of threonine 68 phosphorylation. J. Biol. Chem. 277:48418-48426.
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. Ahn, J. Y., J. K. Schwarz, H. Piwnica-Worms, and C. E. Canman. 2000. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 60:5934-5936.
4. Aleasabas, A. A., A. J. Osborn, J. Bachant, F. Hu, P. J. Werler, K. Bousset, K. Furuya, J. F. 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.
5. 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.
6. Anderson, L., C. Henderson, and Y. Adachi. 2001. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol. Cell. Biol. 21:1719-1729.
7. Bashkirov, V. I., E. V. Bashkirova, E. Haghnazari, and W. D. Heyer. 2003. Direct kinase-to-kinase signaling mediated by the FHA phosphoprotein recognition domain of the Dun1 DNA damage checkpoint kinase. Mol. Cell. Biol. 23:1441-1452.
8. Bell, D. W., J. M. Varley, T. E. Szydlo, D. H. Kang, D. C. 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.
9. Byeon, I. J., S. Yongkiettrakul, and M. D. Tsai. 2001. Solution structure of the yeast Rad53 FHA2 complexed with a phosphothreonine peptide pTXXL: comparison with the structures of FHA2-pYXL and FHA1-pTXXD complexes. J. Mol. Biol. 314:577-588.
10. de la Torre Ruiz, M. A., and N. F. Lowndes. 2000. DUN1 defines one branch downstream of RAD53 for transcription and DNA damage repair in Saccharomyces cerevisiae. FEBS Lett. 485:205-206.
11. de la Torre-Ruiz, M. A., C. M. Green, and N. F. Lowndes. 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.
12. DiTullio, R. A., Jr., T. A. Mochan, M. Venere, J. Bartkova, M. Sehested, J. Bartek, and T. D. Halazonetis. 2002. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 4:998-1002.
13. Dohrmann, P. R., G. Oshiro, M. Tecklenburg, and R. A. Selafani. 1999. RAD53 regulates DBF4 independently of checkpoint function in Saccharomyces cerevisiae. Genetics 151:965-977.
14. 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.
15. Durocher, D., I. A. Taylor, D. Sarbassova, L. F. Haire, S. L. Westeott, S. P. Jackson, S. J. Smerdon, and M. B. Yaffe. 2000. The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phosphodependent signaling mechanisms. Mol. Cell 6:1169-1182.
16. Emili, A. 1998. MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol. Cell 2:183-189.
17. Emili, A., D. M. Schieltz, J. R. Yates III, and L. H. Hartwell. 2001. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell 7:13-20.
18. Fay, D. S., Z. Sun, and D. F. Stern. 1997. Mutations in SPRI/RAD53 that specifically abolish checkpoint but not growth-related functions. Curr. Genet. 31:97-105.
19. 2/M checkpoint pathways in budding yeast. EMBO J. 18:3173-3185.
20. 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.
21. Goldberg, M., M. Stucki, J. Falck, D. D'Amours, D. Rahman, D. Pappin, J. Bartek, and S. P. Jackson. 2003. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421:952-956.
22. Guo, Z., A. Kumagai, S. X. Wang, and W. G. Dunphy. 2000. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14:2745-2756.
23. Hammet, A.,B. L. Pike, K. I. Mitchelhill, T. Teh, B. Kobe, C. M. House, B. E. Kemp, and J. Heierhorst. 2006. FHA domain boundaries of the dun1p and rad53p cell cycle checkpoint kinases. FEBS Lett. 471:141-146.
24. Ho, Y., A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. 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. Matthlesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. Hogue, D. Figeys, and M. Tyers. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
25. Hu, F., A. A. Alcasabas, and S. J. Elledge. 2001. Asf1 links Rad53 to control of chromatin assembly. Genes Dev. 15:1061-1066.
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. Kihara, M., W. Nakai, S. Asano, A. Suzuki, K. Kitada, Y. Kawasaki, L. H. Johnston, and A. Sugino. 2000. Characterization of the yeast Cdc7p/Dbf4p complex purified from insect cells. Its protein kinase activity is regulated by Rad53p. J. Biol. Chem. 275:35051-35062.
28. Kondo, T., T. Wakayama, T. Naiki, K. Matsumoto, and K. Sugimoto. 2001. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294:867-870.
29. Lee, C. H., and J. H. Chung. 2001. The hCds1 (Chk2)-FHA domain is essential for a chain of phosphorylation events on hCds1 that is induced by ionizing radiation. J. Biol. Chem. 276:30537-30541.
30. Leroy, C., S. E. Lee, M. B. Vaze, F. Ochsenbien, R. Guerois, J. E. Haber, and M. C. Marsolier-Kergoat. 2003. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol. Cell 11:827-835.
31. 2/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
32. Lopes, M., C. Cotta-Ramusino, A. Pellicioli, G. Liberi, P. Plevani, M. Muzi-Falconi, C. S. Newlon, and M. Foiani. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412:557-561.
33. Lou, Z., K. Minter-Dykhouse, X. Wu, and J. Chen. 2003. MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421:957-961.
34. Lydall, D., and T. Weinert. 1997. Use of cdc13-1-induced DNA damage to study effects of checkpoint genes on DNA damage processing. Methods Enzymol. 283:410-424.
35. Malkin, D., F. P. Li, L. C. Strong, J. F. Fraumeni, Jr., C. E. Nelson, D. H. Kim, J. Kassel, M. A. Gryka, F. Z. Bischoff, M. A. Tainsky, et al. 1990. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 250:1233-1238.
36. Martinho, R. G., H. D. Lindsay, G. Flaggs, A. J. DeMaggio, M. F. Hoekstra, A. M. Carr, and N. J. Bentley. 1998. Analysis of Rad3 and Chk1 protein kinases defines different checkpoint responses. EMBO J. 17:7239-7249.
37. Massague, J. 2000. How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 1:169-178.
38. 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.
39. Melchionna, R., X. B. Chen, A. Blasina, and C. H. McGowan. 2000. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat. Cell Biol. 2:762-765.
40. Melo, J., and D. Toczyski. 2002. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14:237-245.
41. Melo, J. A., J. Cohen, and D. P. Toczyski. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15:2809-2821.
42. Navas, T. A., Y. Sanchez, and S. J. Elledge. 1996. RAD9 and DNA polymerase epsilon form parallel sensory branches for transducing the DNA damage checkpoint signal in Saccharomyces cerevisiae. Genes Dev. 10:2632-2643.
43. Nyberg, K. A., R. J. Michelson, C. W. Putnam, and T. A. Weinert. 2002. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36:617-656.
44. Paciotti, V., M. Clerici, G. Lucchini, and M. P. Longhese, 2000. The checkpoint protein Ddc2, functionally related to S. pombe Rad26, interacts with Mecl and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14:2046-2059.
45. Pellicioli, A., C. Lucca, G. Liberi, F. Marini, M. Lopes, P. Plevani, A. Romano, P. P. Di Fiore, and M. Folani. 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.
46. Peng, A., and P. L. Chen. 2003. NFBD1, like 53BP1, is an early and redundant transducer mediating Chk2 phosphorylation in response to DNA damage. J. Biol. Chem. 278:8873-8876.
47. Sanchez, Y., J. Bachant, H. Wang, F. 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.
48. Sanchez, Y., B. A. Desany, W. J. Jones, Q. 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.
49. Santocanale, C., and J. F. Diffley. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395:615-618.
50. Santocanale, C., K. Sharma, and J. F. Diffley. 1999. Activation of dormant origins of DNA replication in budding yeast. Genes Dev. 13:2360-2364.
51. Savitsky, K., A. Bar-Shira, S. Gilad, G. Rotman, Y. Ziv, L. Vanagaite, D. A. Tagle, S. Smith, T. Uziel, S. Sfez, et al. 1995. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749-1753.
52. Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103: 211-225.
53. Schwartz, M. F., J. K. Duong, Z. 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.
54. Schwartz, M. F., S.-J. Lee, J. K. Duong, and D. F. Stern. 2003. FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2:384-396.
55. Shang, Y. L., A. J. Bodero, and P. L. Chen. 2003. NFBD1, a novel nuclear protein with signature motifs of FHA and BRCT, and an internal 41 amino acid repeat sequence, is an early participant in DNA damage response. J. Biol. Chem. 278:6323-6329.
56. Stewart, G. S., B. Wang, C. R. Bignell, A. M. Taylor, and S. J. Elledge. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961-966.
57. Sugimoto, K., S. Ando, T. Shimomura, and K. Matsumoto. 1997. Rfc5, a replication factor C component, is required for regulation of Rad53 protein kinase in the yeast checkpoint pathway. Mol. Cell. Biol. 17:5905-5914.
58. Sun, Z., 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.
59. Sun, Z., 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.
60. 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 Cds1. Mol. Cell. Biol. 21:3398-3404.
61. 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.
62. 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.
63. Wakayama, T., T. Kondo, S. Ando, K. Matsumoto, and K. Sugimoto. 2001. Pie1, a protein interacting with Mec1, controls cell growth and checkpoint responses in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:755-764.
64. Wang, B., S. Matsuoka, P. B. Carpenter, and S. J. Elledge. 2002. 53BP1, a mediator of the DNA damage checkpoint. Science 298:1435-1438.
65. Wang, H., and S. J. Elledge. 1999. DRC1, DNA replication and checkpoint protein 1, functions with DPB11 to control DNA replication and the S-phase checkpoint in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 96:3824-3829.
66. Wang, P., I. J. Byeon, H. Liao, K. D. Beebe, S. Yongkiettrakul, D. Pet, and M. D. Tsai. 2000. II. Structure and specificity of the interaction between the FHA2 domain of Rad53 and phosphotyrosyl peptides. J. Mol. Biol. 302:927-940.
67. 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.
68. Xu, X., and D. F. Stern. 2003. NFBD1/KIAA0170 is a chromatin-associated protein involved in DNA damage signaling pathways. J. Biol. Chem. 278: 8795-8803.
69. Xu, X., L. M. Tsvetkov, and D. F. Stern. 2002. Chk2 activation and phosphorylation-dependent oligomerization. Mol. Cell. Biol. 22:4419-4432.
70. 2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet. 30:285-289.
71. Zhao, X., A. Chabes, V. Domkin, L. Thelander, and R. Rothstein. 2001. The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage. EMBO J. 20:3544-3553.
72. Zhao, X., B. Georgieva, A. Chabes, V. Domkin, J. H. Ippel, J. Schleucher, S. Wijmenga, L. Thelander, and R. Rothstein. 2000. Mutational and structural analyses of the ribonucleotide reductase inhibitor Sml1 define its Rnr1 interaction domain whose inactivation allows suppression of mec1 and rad53 lethality. Mol. Cell. Biol. 20:9076-9083.
73. Zhao, X., E. G. 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.
74. Zhao, X., and R. Rothstein. 2002. The Dun1 checkpoint kinase phosphorylates and regulates the ribonucleotide reductase inhibitor Sml1. Proc. Natl. Acad. Sci. USA 99:3746-3751.
75. 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.
76. Zhou, Z., and S. J. Elledge. 1993. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75:1119-1127.