Cell cycle-dependent phosphorylation of Rad53 kinase by Cdc5 and Cdc28 modulates checkpoint adaptation

Cell Cycle

Volumn 9, Issue 2, 2010, Pages 350-363

  Schleker, Thomas ^a,b   Shimada, Kenji ^a   Sack, Ragna ^a   Pike, Brietta L ^a   Gasser, Susan M ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

Adaptation; Cdc28; Cdc5; CDK; Cell cycle; Checkpoint; Chk2; DNA damage; Polo like kinase; Rad53

Indexed keywords

CDC5 PROTEIN; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; FUNGAL PROTEIN; POLO LIKE KINASE; SERINE; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; DNA DAMAGE; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

SACCHAROMYCETALES;

EID: 74949131810     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.2.10448     Document Type: Article

References (76)

1. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434:864-70.
2. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434:907-13.
3. Hartwell LH, Weinert TA. Checkpoints: controls that ensure the order of cell cycle events. Science 1989; 246:629-34.
4. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 1995; 268:1749-53.
5. Nevanlinna H, Bartek J. The CHEK2 gene and inherited breast cancer susceptibility. Oncogene 2006; 25:5912-9.
6. Stern DF, Zheng P, Beidler DR, Zerillo C. Spk1, a new kinase from Saccharomyces cerevisiae, phosphorylates proteins on serine, threonine and tyrosine. Mol Cell Biol 1991; 11:987-1001.
7. Zheng P, Fay DS, Burton J, Xiao H, Pinkham JL, Stern DF. SPK1 is an essential S-phase-specific gene of Saccharomyces cerevisiae that encodes a nuclear serine/threonine/tyrosine kinase. Mol Cell Biol 1993; 13:5829-42.
8. Branzei D, Foiani M. The Rad53 signal transduction pathway: Replication fork stabilization, DNA repair, and adaptation. Exp Cell Res 2006; 312:2654-9.
9. Elledge SJ, Zhou Z, Allen JB, Navas TA. DNA damage and cell cycle regulation of ribonucleotide reductase. Bioessays 1993; 15:333-9.
10. Chen SH, Smolka MB, Zhou H. Mechanism of Dun1 activation by Rad53 phosphorylation in Saccharomyces cerevisiae. J Biol Chem 2007; 282:986-95.
11. Sun Z, Fay DS, Marini F, Foiani M, Stern DF. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev 1996; 10:395-406.
12. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, Elledge SJ. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 1996; 271:357-60.
13. Zhao X, Muller EG, Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 1998; 2:329-40.
14. Carr AM. DNA structure dependent checkpoints as regulators of DNA repair. DNA Repair (Amst) 2002; 1:983-94.
15. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39-85.
16. Pellicioli A, Foiani M. Signal transduction: how rad53 kinase is activated. Curr Biol 2005; 15:769-71.
17. Lowndes NF, Murguia JR. Sensing and responding to DNA damage. Curr Opin Genet Dev 2000; 10:17-25.
18. Harrison JC, Haber JE. Surviving the breakup: the DNA damage checkpoint. Annu Rev Genet 2006; 40:209-35.
19. Mantiero D, Clerici M, Lucchini G, Longhese MP. Dual role for Saccharomyces cerevisiae Tel1 in the checkpoint response to double-strand breaks. EMBO Rep 2007; 8:380-7.
20. Baldo V, Testoni V, Lucchini G, Longhese MP. Dominant TEL1-hy mutations compensate for Mec1 lack of functions in the DNA damage response. Mol Cell Biol 2008; 28:358-75.
21. Nakada D, Shimomura T, Matsumoto K, Sugimoto K. The ATM-related Tel1 protein of Saccharomyces cerevisiae controls a checkpoint response following phleomycin treatment. Nucleic Acids Res 2003; 31:1715-24.
22. Weinert TA, Kiser GL, Hartwell LH. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev 1994; 8:652-65.
23. Paciotti V, Clerici M, Scotti M, Lucchini G, Longhese MP. Characterization of mec1 kinase-deficient mutants and of new hypomorphic mec1 alleles impairing subsets of the DNA damage response pathway. Mol Cell Biol 2001; 21:3913-25.
24. Toh GW, Lowndes NF. Role of the Saccharomyces cerevisiae Rad9 protein in sensing and responding to DNA damage. Biochem Soc Trans 2003; 31:242-6.
25. Ubersax JA, Ferrell JE Jr. Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 2007; 8:530-41.
26. Nash P, Tang X, Orlicky S, Chen Q, Gertler FB, Mendenhall MD, et al. Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 2001; 414:514-21.
27. Sweeney FD, Yang F, Chi A, Shabanowitz J, Hunt DF, Durocher D. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr Biol 2005; 15:1364-75.
28. Smolka MB, Albuquerque CP, Chen SH, Schmidt KH, Wei XX, Kolodner RD, et al. Dynamic changes in protein-protein interaction and protein phosphorylation probed with amine reactive isotope tag. Mol Cell Proteomics 2005.
29. Kim ST, Lim DS, Canman CE, Kastan MB. Substrate specificities and identification of putative substrates of ATM kinase family members. J Biol Chem 1999; 274:37538-43.
30. Lee SJ, Schwartz MF, Duong JK, Stern DF. Rad53 phosphorylation site clusters are important for Rad53 regulation and signaling. Mol Cell Biol 2003; 23:6300-14.
31. Traven A, Heierhorst J. SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays 2005; 27:397-407.
32. Durocher D, Henckel J, Fersht AR, Jackson SP. The FHA domain is a modular phosphopeptide recognition motif. Mol Cell 1999; 4:387-94.
33. Durocher D, Taylor IA, Sarbassova D, Haire LF, Westcott SL, Jackson SP, et al. The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol Cell 2000; 6:1169-82.
34. Liao H, Yuan C, Su MI, Yongkiettrakul S, Qin D, Li H, et al. Structure of the FHA1 domain of yeast Rad53 and identification of binding sites for both FHA1 and its target protein Rad9. J Mol Biol 2000; 304:941-51.
35. Liao H, Byeon IJ, Tsai MD. Structure and function of a new phosphopeptide-binding domain containing the FHA2 of Rad53. J Mol Biol 1999; 294:1041-9.
36. Sun Z, Hsiao J, Fay DS, Stern DF. Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science 1998; 281:272-4.
37. Vialard JE, Gilbert CS, Green CM, Lowndes NF. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J 1998; 17:5679-88.
38. Smolka MB, Chen SH, Maddox PS, Enserink JM, Albuquerque CP, Wei XX, et al. An FHA domain-mediated protein interaction network of Rad53 reveals its role in polarized cell growth. J Cell Biol 2006; 175:743-53.
39. Bjergbaek L, Cobb JA, Tsai-Pflugfelder M, Gasser SM. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J 2005; 24:405-17.
40. Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J. 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 2004; 24:2779-88.
41. Diani L, Colombelli C, Tamilselvan Nachimuthu B, Donnianni RA, Plevani P, Muzi-Falconi M, et al. Saccharomyces CDK1 phosphorylates Rad53 kinase in metaphase influencing cellular morphogenesis. J Biol Chem 2009.
42. Shimada K, Pasero P, Gasser SM. ORC and the intra-Sphase checkpoint: a threshold regulates Rad53p activation in S phase. Genes Dev 2002; 16:3236-52.
43. Tercero JA, Longhese MP, Diffley JF. A central role for DNA replication forks in checkpoint activation and response. Mol Cell 2003; 11:1323-36.
44. 2/M arrest. Mol Cell 2001; 7:293-300.
45. Sandell LL, Zakian VA. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 1993; 75:729-39.
46. Wang W, Malcolm BA. Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange Site-Directed Mutagenesis. Biotechniques 1999; 26:680-2.
47. Sugimoto K, Ando S, Shimomura T, Matsumoto K. Rfc5, a replication factor C component, is required for regulation of Rad53 protein kinase in the yeast checkpoint pathway. Mol Cell Biol 1997; 17:5905-14.
48. Longtine MS, McKenzie A, 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998; 14:953-61.
49. Braguglia D, Heun P, Pasero P, Duncker BP, Gasser SM. Semi-conservative replication in yeast nuclear extracts requires Dna2 helicase and supercoiled template. J Mol Biol 1998; 281:631-49.
50. Frei C, Gasser SM. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev 2000; 14:81-96.
51. Jaquenoud M, van Drogen F, Peter M. Cell cycle-dependent nuclear export of Cdh1p may contribute to the inactivation of APC/C(Cdh1). EMBO J 2002; 21:6515-26.
52. Yaffe MP, Schatz G. Two nuclear mutations that block mitochondrial protein import in yeast. Proc Natl Acad Sci USA 1984; 81:4819-23.
53. Cobb JA, Bjergbaek L, Shimada K, Frei C, Gasser SM. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J 2003; 22:4325-36.
54. Yamaguchi T, Goto H, Yokoyama T, Sillje H, Hanisch A, Uldschmid A, et al. Phosphorylation by Cdk1 induces Plk1-mediated vimentin phosphorylation during mitosis. J Cell Biol 2005; 171:431-6.
55. Choi KS, Eom YW, Kang Y, Ha MJ, Rhee H, Yoon JW, et al. Cdc2 and Cdk2 kinase activated by transforming growth factor-beta1 trigger apoptosis through the phosphorylation of retinoblastoma protein in FaO hepatoma cells. J Biol Chem 1999; 274:31775-83.
56. Clemenson C, Marsolier-Kergoat MC. The spindle assembly checkpoint regulates the phosphorylation state of a subset of DNA checkpoint proteins in Saccharomyces cerevisiae. Molecular and cellular biology 2006; 26:9149-61.
57. Lee H, Yuan C, Hammet A, Mahajan A, Chen ES, Wu MR, et al. Diphosphothreonine-specific interaction between an SQ/TQ cluster and an FHA domain in the Rad53-Dun1 kinase cascade. Mol Cell 2008; 30:767-78.
58. Nigg EA. Polo-like kinases: positive regulators of cell division from start to finish. Curr Opin Cell Biol 1998; 10:776-83.
59. Tsvetkov L, Xu X, Li J, Stern DF. Polo-like kinase 1 and Chk2 interact and co-localize to centrosomes and the midbody. J Biol Chem 2003; 278:8468-75.
60. Benjamin KR, Zhang C, Shokat KM, Herskowitz I. Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 2003; 17:1524-39.
61. Heichman KA, Roberts JM. The yeast CDC16 and CDC27 genes restrict DNA replication to once per cell cycle. Cell 1996; 85:39-48.
62. Sanchez Y, Bachant J, Wang H, Hu F, Liu D, Tetzlaff M, et al. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 1999; 286:1166-71.
63. Leroy C, Lee SE, Vaze MB, Ochsenbien F, Guerois R, Haber JE, et al. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol Cell 2003; 11:827-35.
64. 2/M arrest after DNA damage. Cell 1998; 94:399-409.
65. Toczyski DP, Galgoczy DJ, Hartwell LH. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 1997; 90:1097-106.
66. Galgoczy DJ, Toczyski DP. Checkpoint adaptation precedes spontaneous and damage-induced genomic instability in yeast. Mol Cell Biol 2001; 21:1710-8.
67. Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J. Diverse but overlapping functions of the two forkhead-associated (FHA) domains in Rad53 checkpoint kinase activation. J Biol Chem 2003; 278:30421-4.
68. Schwartz MF, Lee SJ, Duong JK, Eminaga S, Stern DF. FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2003; 2:384-96.
69. Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, Hoepker K, et al. The molecular basis for phospho-dependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 2003; 115:83-95.
70. Lee SE, Pellicioli A, Vaze MB, Sugawara N, Malkova A, Foiani M, et al. Yeast Rad52 and Rad51 recombination proteins define a second pathway of DNA damage assessment in response to a single double-strand break. Mol Cell Biol 2003; 23:8913-23.
71. Ahn J, Urist M, Prives C. The Chk2 protein kinase. DNA Repair (Amst) 2004; 3:1039-47.
72. Bahassi el M, Conn CW, Myer DL, Hennigan RF, McGowan CH, Sanchez Y, et al. Mammalian Polo-like kinase 3 (Plk3) is a multifunctional protein involved in stress response pathways. Oncogene 2002; 21:6633-40.
73. Ouyang B, Pan H, Lu L, Li J, Stambrook P, Li B, et al. Human Prk is a conserved protein serine/threonine kinase involved in regulating M phase functions. J Biol Chem 1997; 272:28646-51.
74. Lee KS, Erikson RL. Plk is a functional homolog of Saccharomyces cerevisiae Cdc5, and elevated Plk activity induces multiple septation structures. Mol Cell Biol 1997; 17:3408-17.
75. Cheng L, Hunke L, Hardy CF. Cell cycle regulation of the Saccharomyces cerevisiae polo-like kinase cdc5p. Mol Cell Biol 1998; 18:7360-70.
76. Bonilla CY, Melo JA, Toczyski DP. Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol Cell 2008; 30:267-76.