Elevated levels of the polo kinase Cdc5 override the Mec1/ATR checkpoint in budding yeast by acting at different steps of the signaling pathway

PLoS Genetics

Volumn 6, Issue 1, 2010, Pages

  Donnianni, Roberto Antonio ^a   Ferrari, Matteo ^a   Lazzaro, Federico ^a   Clerici, Michela ^b   Nachimuthu, Benjamin Tamilselvan ^a   Plevani, Paolo ^a   Muzi Falconi, Marco ^a   Pellicioli, Achille ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 2; POLO KINASE CDC5; POLO LIKE KINASE; PROTEIN RAD9; UNCLASSIFIED DRUG; CDC5 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; MEC1 PROTEIN, S CEREVISIAE; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; RAD53 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE;

ARTICLE; BUDDING; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; NONHUMAN; PROCESSING; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; YEAST; AMINO ACID SEQUENCE; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEAR DIVISION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCETALES;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CELL NUCLEUS DIVISION; DNA BREAKS, DOUBLE-STRANDED; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 76749116250     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000763     Document Type: Article

References (84)

1. Harrison JC, Haber JE (2006) Surviving the breakup: the DNA damage checkpoint. Annu Rev Genet 40: 209-235.
2. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745.
3. Branzei D, Foiani M (2008) Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 9: 297-308.
4. Lazzaro F, Giannattasio M, Puddu F, Granata M, Pellicioli A, et al. (2009) Checkpoint mechanisms at the intersection between DNA damage and repair. DNA Repair (Amst) 8: 1055-1067.
5. Mimitou EP, Symington LS (2009) Nucleases and helicases take center stage in homologous recombination. Trends Biochem Sci 34: 264-272.
6. Bartek J, Lukas J (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19: 238-245.
7. Clemenson C, Marsolier-Kergoat MC (2009) DNA damage checkpoint inactivation: adaptation and recovery. DNA Repair (Amst) 8: 1101-1109.
8. Lee SE, Pellicioli A, Demeter J, Vaze MP, Gasch AP, et al. (2000) Arrest, adaptation, and recovery following a chromosome double-strand break in Saccharomyces cerevisiae. Cold Spring Harb Symp Quant Biol 65: 303-314.
9. Galgoczy DJ, Toczyski DP (2001) Checkpoint adaptation precedes spontaneous and damage-induced genomic instability in yeast. Mol Cell Biol 21: 1710-1718.
10. van Vugt MA, Medema RH (2004) Checkpoint adaptation and recovery: back with Polo after the break. Cell Cycle 3: 1383-1386.
11. van de Weerdt BC, Medema RH (2006) Polo-like kinases: a team in control of the division. Cell Cycle 5: 853-864.
12. 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.
13. Toczyski DP, Galgoczy DJ, Hartwell LH (1997) CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90: 1097-1106.
14. Vaze MB, Pellicioli A, Lee SE, Ira G, Liberi G, et al. (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol Cell 10: 373-385.
15. van Vugt MA, Bras A, Medema RH (2004) Polo-like kinase-1 controls recovery from a G2 DNA damage-induced arrest in mammalian cells. Mol Cell 15: 799-811.
16. Syljuasen RG, Jensen S, Bartek J, Lukas J (2006) Adaptation to the ionizing radiation-induced G2 checkpoint occurs in human cells and depends on checkpoint kinase 1 and Polo-like kinase 1 kinases. Cancer Res 66: 10253-10257.
17. Liu X, Lei M, Erikson RL (2006) Normal cells, but not cancer cells, survive severe Plk1 depletion. Mol Cell Biol 26: 2093-2108.
18. Lane HA, Nigg EA (1996) Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J Cell Biol 135: 1701-1713.
19. 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.
20. 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.
21. 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.
22. Mamely I, van Vugt MA, Smits VA, Semple JI, Lemmens B, et al. (2006) Pololike kinase-1 controls proteasome-dependent degradation of Claspin during checkpoint recovery. Curr Biol 16: 1950-1955.
23. 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.
24. 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.
25. Kee Y, Kim JM, D'Andrea AD (2009) Regulated degradation of FANCM in the Fanconi anemia pathway during mitosis. Genes Dev 23: 555-560.
26. Bahassi el M, Conn CW, Myer DL, Hennigan RF, McGowan CH, et al. (2002) Mammalian Polo-like kinase 3 (Plk3) is a multifunctional protein involved in stress response pathways. Oncogene 21: 6633-6640.
27. 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.
28. Petrinac S, Ganuelas ML, Bonni S, Nantais J, Hudson JW (2009) Polo-like kinase 4 phosphorylates Chk2. Cell Cycle 8: 327-329.
29. Cheng L, Hunke L, Hardy CF (1998) Cell cycle regulation of the Saccharomyces cerevisiae polo-like kinase cdc5p. Mol Cell Biol 18: 7360-7370.
30. 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.
31. 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.
32. Ando K, Ozaki T, Yamamoto H, Furuya K, Hosoda M, et al. (2004) Polo-like kinase 1 (Plk1) inhibits p53 function by physical interaction and phosphorylation. J Biol Chem 279: 25549-25561.
33. Tsvetkov L, Stern DF (2005) Phosphorylation of Plk1 at S137 and T210 is inhibited in response to DNA damage. Cell Cycle 4: 166-171.
34. Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, et al. (2008) The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 134: 256-267.
35. Macurek L, Lindqvist A, Lim D, Lampson MA, Klompmaker R, et al. (2008) Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455: 119-123.
36. Lu LY, Yu X (2009) The balance of Polo-like kinase 1 in tumorigenesis. Cell Div 4: 4.
37. Eckerdt F, Yuan J, Strebhardt K (2005) Polo-like kinases and oncogenesis. Oncogene 24: 267-276.
38. Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I (2005) Polo-like kinases (Plks) and cancer. Oncogene 24: 287-291.
39. Smith MR, Wilson ML, Hamanaka R, Chase D, Kung H, et al. (1997) Malignant transformation of mammalian cells initiated by constitutive expression of the polo-like kinase. Biochem Biophys Res Commun 234: 397-405.
40. Weichert W, Denkert C, Schmidt M, Gekeler V, Wolf G, et al. (2004) Polo-like kinase isoform expression is a prognostic factor in ovarian carcinoma. Br J Cancer 90: 815-821.
41. Tokumitsu Y, Mori M, Tanaka S, Akazawa K, Nakano S, et al. (1999) Prognostic significance of polo-like kinase expression in esophageal carcinoma. Int J Oncol 15: 687-692.
42. Knecht R, Oberhauser C, Strebhardt K (2000) PLK (polo-like kinase), a new prognostic marker for oropharyngeal carcinomas. Int J Cancer 89: 535-536.
43. Kneisel L, Strebhardt K, Bernd A, Wolter M, Binder A, et al. (2002) Expression of polo-like kinase (PLK1) in thin melanomas: a novel marker of metastatic disease. J Cutan Pathol 29: 354-358.
44. Yamada S, Ohira M, Horie H, Ando K, Takayasu H, et al. (2004) Expression profiling and differential screening between hepatoblastomas and the corresponding normal livers: identification of high expression of the PLK1 oncogene as a poor-prognostic indicator of hepatoblastomas. Oncogene 23: 5901-5911.
45. Bartek J, Lukas J, Bartkova J (2007) DNA damage response as an anti-cancer barrier: damage threshold and the concept of 'conditional haploinsufficiency'. Cell Cycle 6: 2344-2347.
46. 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.
47. Hu F, Wang Y, Liu D, Li Y, Qin J, et al. (2001) Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints. Cell 107: 655-665.
48. Song S, Grenfell TZ, Garfield S, Erikson RL, Lee KS (2000) Essential function of the polo box of Cdc5 in subcellular localization and induction of cytokinetic structures. Mol Cell Biol 20: 286-298.
49. Song S, Lee KS (2001) A novel function of Saccharomyces cerevisiae CDC5 in cytokinesis. J Cell Biol 152: 451-469.
50. 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.
51. 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.
52. 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.
53. Pellicioli A, Foiani M (2005) Signal transduction: how rad53 kinase is activated. Curr Biol 15: R769-771.
54. Fiorani S, Mimun G, Caleca L, Piccini D, Pellicioli A (2008) Characterization of the activation domain of the Rad53 checkpoint kinase. Cell Cycle 7: 493-499.
55. Mantiero D, Clerici M, Lucchini G, Longhese MP (2007) Dual role for Saccharomyces cerevisiae Tel1 in the checkpoint response to double-strand breaks. EMBO Rep 8: 380-387.
56. Toh GW, Lowndes NF (2003) Role of the Saccharomyces cerevisiae Rad9 protein in sensing and responding to DNA damage. Biochem Soc Trans 31: 242-246.
57. 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.
58. Lazzaro F, Sapountzi V, Granata M, Pellicioli A, Vaze M, et al. (2008) Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J 27: 1502-1512.
59. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, et al. (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425: 859-864.
60. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455: 689-692.
61. 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.
62. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
63. 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.
64. Navadgi-Patil VM, Burgers PM (2009) A tale of two tails: Activation of DNA damage checkpoint kinase Mec1/ATR by the 9-1-1 clamp and by Dpb11/ TopBP1. DNA Repair (Amst).
65. Baroni E, Viscardi V, Cartagena-Lirola H, Lucchini G, Longhese MP (2004) The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol Cell Biol 24: 4151-4165.
66. Clerici M, Mantiero D, Lucchini G, Longhese MP (2006) The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep 7: 212-218.
67. Kim HS, Vijayakumar S, Reger M, Harrison JC, Haber JE, et al. (2008) Functional interactions between Sae2 and the Mre11 complex. Genetics 178: 711-723.
68. Yu X, Fu S, Lai M, Baer R, Chen J (2006) BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev 20: 1721-1726.
69. Limbo O, Chahwan C, Yamada Y, de Bruin RA, Wittenberg C, et al. (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol Cell 28: 134-146.
70. Yuan J, Chen J (2009) N terminus of CtIP is critical for homologous recombination mediated double-strand break repair. J Biol Chem.
71. Lloyd J, Chapman JR, Clapperton JA, Haire LF, Hartsuiker E, et al. (2009) A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 139: 100-111.
72. Williams RS, Dodson GE, Limbo O, Yamada Y, Williams JS, et al. (2009) Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139: 87-99.
73. Chen L, Nievera CJ, Lee AY, Wu X (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 283: 7713-7720.
74. Yu X, Chen J (2004) DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol 24: 9478-9486.
75. Huertas P, Jackson SP (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284: 9558-9565.
76. Trenz K, Errico A, Costanzo V (2008) Plx1 is required for chromosomal DNA replication under stressful conditions. EMBO J 27: 876-885.
77. Tsvetkov L, Stern DF (2005) Interaction of chromatin-associated Plk1 and Mcm7. J Biol Chem 280: 11943-11947.
78. Longtine MS, McKenzie A, 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
79. Gyuris J, Golemis E, Chertkov H, Brent R (1993) Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75: 791-803.
80. Miller CT, Gabrielse C, Chen YC, Weinreich M (2009) Cdc7p-dbf4p regulates mitotic exit by inhibiting Polo kinase. PLoS Genet 5: e1000498. doi:10.1371/journal.pgen.1000498.
81. Lee SE, Moore JK, Holmes A, Umezu K, Kolodner RD, et al. (1998) Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94: 399-409.
82. Clerici M, Mantiero D, Lucchini G, Longhese MP (2005) The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280: 38631-38638.
83. Viscardi V, Bonetti D, Cartagena-Lirola H, Lucchini G, Longhese MP (2007) MRX-dependent DNA damage response to short telomeres. Mol Biol Cell 18: 3047-3058.
84. Clerici M, Mantiero D, Guerini I, Lucchini G, Longhese MP (2008) The Yku70-Yku80 complex contributes to regulate double-strand break processing and checkpoint activation during the cell cycle. EMBO Rep 9: 810-818.