CDC5 inhibits the hyperphosphorylation of the checkpoint kinase Rad53, leading to checkpoint adaptation

PLoS Biology

Volumn 8, Issue 1, 2010, Pages

  Vidanes, Genevieve M ^a,c   Sweeney, Frédéric D ^b   Galicia, Sarah ^b   Cheung, Stephanie ^a   Doyle, John P ^a   Durocher, Daniel ^b   Toczyski, David P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 5; CHECKPOINT KINASE 2; PHOSPHOPROTEIN PHOSPHATASE 2; PHOSPHOPROTEIN PHOSPHATASE 2C; PHOSPHOPROTEIN PHOSPHATASE 3C; PHOSPHOPROTEIN PHOSPHATASE CDC14; PROTEIN DDC2; PROTEIN MEC1; PROTEIN RAD9; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GAL1; UNCLASSIFIED DRUG; CDC5 PROTEIN, S CEREVISIAE; MEC1 PROTEIN, S CEREVISIAE; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; RAD53 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE;

ARTICLE; CELL CYCLE; CELL CYCLE ARREST; COMPLEX FORMATION; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; NONHUMAN; ADAPTATION; BIOLOGICAL MODEL; CYTOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE; VERTEBRATA;

ADAPTATION, BIOLOGICAL; CELL CYCLE; CELL CYCLE PROTEINS; DNA DAMAGE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 75749156256     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000286     Document Type: Article

References (68)

1. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432: 316-323.
2. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745.
3. Cimprich KA, Cortez D (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9: 616-627.
4. Sugawara N, Haber JE (1992) Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol Cell Biol 12: 563-575.
5. Maringele L, Lydall D (2002) EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Delta mutants. Genes Dev 16: 1919-1933.
6. Melo JA, Cohen J, Toczyski DP (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev 15: 2809-2821.
7. Kondo T, Wakayama T, Naiki T, Matsumoto K, Sugimoto K (2001) Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294: 867-870.
8. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
9. Lisby M, Barlow JH, Burgess RC, Rothstein R (2004) Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713.
10. Majka J, Burgers PM (2003) Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc Natl Acad Sci U S A 100: 2249-2254.
11. Bermudez VP, Lindsey-Boltz LA, Cesare AJ, Maniwa Y, Griffith JD, et al. (2003) Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc Natl Acad Sci U S A 100: 1633-1638.
12. Ellison V, Stillman B (2003) Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol 1: E33. doi:10.1371/journal.pbio.0000033.
13. Zou L, Liu D, Elledge SJ (2003) Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc Natl Acad Sci U S A 100: 13827-13832.
14. Melo J, Toczyski D (2002) A unified view of the DNA-damage checkpoint. Curr Opin Cell Biol 14: 237-245.
15. Usui T, Ogawa H, Petrini JH (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7: 1255-1266.
16. Bonilla CY, Melo JA, Toczyski DP (2008) Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol Cell 30: 267-276.
17. Alcasabas AA, Osborn AJ, Bachant J, Hu F, Werler PJ, et al. (2001) Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol 3: 958-965.
18. Emili A (1998) MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol Cell 2: 183-189.
19. Sun Z, Hsiao J, Fay DS, Stern DF (1998) Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science 281: 272-274.
20. Sanchez Y, Bachant J, Wang H, Hu F, Liu D, et al. (1999) Control of the DNA damage checkpoint by Chk1 and Rad53 protein kinases through distinct mechanisms. Science 286: 1166-1171.
21. Blankley RT, Lydall D (2004) A domain of Rad9 specifically required for activation of Chk1 in budding yeast. J Cell Sci 117: 601-608.
22. Sweeney FD, Yang F, Chi A, Shabanowitz J, Hunt DF, et al. (2005) Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr Biol 15: 1364-1375.
23. Vialard JE, Gilbert CS, Green CM, Lowndes NF (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.
24. Xu YJ, Davenport M, Kelly TJ (2006) Two-stage mechanism for activation of the DNA replication checkpoint kinase Cds1 in fission yeast. Genes Dev 20: 990-1003.
25. Tanaka K, Russell P (2004) Cds1 phosphorylation by Rad3-Rad26 kinase is mediated by forkhead-associated domain interaction with Mrc1. J Biol Chem 279: 32079-32086.
26. Toczyski DP, Galgoczy DJ, Hartwell LH (1997) CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90: 1097-1106.
27. Charles JF, Jaspersen SL, Tinker-Kulberg RL, Hwang L, Szidon A, et al. (1998) The Polo-related kinase Cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae. Curr Biol 8: 497-507.
28. Pellicioli A, Lee SE, Lucca C, Foiani M, Haber JE (2001) Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol Cell 7: 293-300.
29. Yoo HY, Kumagai A, Shevchenko A, Dunphy WG (2004) Adaptation of a DNA replication checkpoint response depends upon inactivation of Claspin by the Polo-like kinase. Cell 117: 575-588.
30. Mailand N, Bekker-Jensen S, Bartek J, Lukas J (2006) Destruction of Claspin by SCFbetaTrCP restrains Chk1 activation and facilitates recovery from genotoxic stress. Mol Cell 23: 307-318.
31. Peschiaroli A, Dorrello NV, Guardavaccaro D, Venere M, Halazonetis T, et al. (2006) SCFbetaTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol Cell 23: 319-329.
32. Mamely I, van Vugt MA, Smits VA, Semple JI, Lemmens B, et al. (2006) Polo-like kinase-1 controls proteasome-dependent degradation of Claspin during checkpoint recovery. Curr Biol 16: 1950-1955.
33. Toczyski DP (2006) Methods for studying adaptation to the DNA damage checkpoint in yeast. Methods Enzymol 409: 150-165.
34. Soulier J, Lowndes NF (1999) The BRCT domain of the S. cerevisiae checkpoint protein Rad9 mediates a Rad9-Rad9 interaction after DNA damage. Curr Biol 9: 551-554.
35. Leroy C, Lee SE, Vaze MB, Ochsenbien F, Guerois R, et al. (2003) PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol Cell 11: 827-835.
36. Guillemain G, Ma E, Mauger S, Miron S, Thai R, et al. (2007) Mechanisms of checkpoint kinase Rad53 inactivation after a double-strand break in Saccharomyces cerevisiae. Mol Cell Biol 27: 3378-3389.
37. Snead JL, Sullivan M, Lowery DM, Cohen MS, Zhang C, et al. (2007) A coupled chemical-genetic and bioinformatic approach to Polo-like kinase pathway exploration. Chem Biol 14: 1261-1272.
38. Asano S, Park JE, Sakchaisri K, Yu LR, Song S, et al. (2005) Concerted mechanism of Swe1/Wee1 regulation by multiple kinases in budding yeast. EMBO J 24: 2194-2204.
39. Bartholomew CR, Woo SH, Chung YS, Jones C, Hardy CF (2001) Cdc5 interacts with the Wee1 kinase in budding yeast. Mol Cell Biol 21: 4949-4959.
40. Visintin R, Stegmeier F, Amon A (2003) The role of the polo kinase Cdc5 in controlling Cdc14 localization. Mol Biol Cell 14: 4486-4498.
41. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, et al. (2004) DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431: 1011-1017.
42. Clerici M, Baldo V, Mantiero D, Lottersberger F, Lucchini G, et al. (2004) A Tel1/MRX-dependent checkpoint inhibits the metaphase-to-anaphase transition after UV irradiation in the absence of Mec1. Mol Cell Biol 24: 10126-10144.
43. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, et al. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8: 37-45.
44. Vodenicharov MD, Wellinger RJ (2006) DNA degradation at unprotected telomeres in yeast is regulated by the CDK1 (Cdc28/Clb) cell-cycle kinase. Mol Cell 24: 127-137.
45. Lee SJ, Duong JK, Stern DF (2004) A Ddc2-Rad53 fusion protein can bypass the requirements for RAD9 and MRC1 in Rad53 activation. Mol Biol Cell 15: 5443-5455.
46. Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, et al. (2003) The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115: 83-95.
47. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, et al. (1996) Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360.
48. Sun Z, Fay DS, Marini F, Foiani M, Stern DF (1996) Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev 10: 395-406.
49. Tsvetkov L, Xu X, Li J, Stern DF (2003) Polo-like kinase 1 and Chk2 interact and co-localize to centrosomes and the midbody. J Biol Chem 278: 8468-8475.
50. Tsvetkov LM, Tsekova RT, Xu X, Stern DF (2005) The Plk1 Polo box domain mediates a cell cycle and DNA damage regulated interaction with Chk2. Cell Cycle 4: 609-617.
51. Durocher D, Henckel J, Fersht AR, Jackson SP (1999) The FHA domain is a modular phosphopeptide recognition motif. Mol Cell 4: 387-394.
52. Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J (2003) Diverse but overlapping functions of the two forkhead-associated (FHA) domains in Rad53 checkpoint kinase activation. J Biol Chem 278: 30421-30424.
53. Petronczki M, Lenart P, Peters JM (2008) Polo on the rise-from mitotic entry to cytokinesis with Plk1. Dev Cell 14: 646-659.
54. Alexandru G, Uhlmann F, Mechtler K, Poupart MA, Nasmyth K (2001) Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105: 459-472.
55. Barr FA, Sillje HH, Nigg EA (2004) Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5: 429-440.
56. Usui T, Foster SS, Petrini JH (2009) Maintenance of the DNA-damage checkpoint requires DNA-damage-induced mediator protein oligomerization. Mol Cell 33: 147-159.
57. Gilbert CS, Green CM, Lowndes NF (2001) Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol Cell 8: 129-136.
58. Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, et al. (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.
59. Lowery DM, Mohammad DH, Elia AE, Yaffe MB (2004) The Polo-box domain: a molecular integrator of mitotic kinase cascades and Polo-like kinase function. Cell Cycle 3: 128-131.
60. Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J (2004) Mdt1, a novel Rad53 FHA1 domain-interacting protein, modulates DNA damage tolerance and G(2)/M cell cycle progression in Saccharomyces cerevisiae. Mol Cell Biol 24: 2779-2788.
61. Schwartz MF, Lee SJ, Duong JK, Eminaga S, Stern DF (2003) FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2: 384-396.
62. Durocher D, Taylor IA, Sarbassova D, Haire LF, Westcott SL, et al. (2000) The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol Cell 6: 1169-1182.
63. Duncker BP, Shimada K, Tsai-Pflugfelder M, Pasero P, Gasser SM (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 U S A 99: 16087-16092.
64. van Vugt MA, Smits VA, Klompmaker R, Medema RH (2001) Inhibition of Polo-like kinase-1 by DNA damage occurs in an ATM- or ATR-dependent fashion. J Biol Chem 276: 41656-41660.
65. Smits VA, Klompmaker R, Arnaud L, Rijksen G, Nigg EA, et al. (2000) Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat Cell Biol 2: 672-676.
66. Galgoczy DJ, Toczyski DP (2001) Checkpoint adaptation precedes spontaneous and damage-induced genomic instability in yeast. Mol Cell Biol 21: 1710-1718.
67. Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I (2005) Polo-like kinases (Plks) and cancer. Oncogene 24: 287-291.
68. Strebhardt K, Ullrich A (2006) Targeting polo-like kinase 1 for cancer therapy. Nat Rev Cancer 6: 321-330.