Proteins in the Nutrient-Sensing and DNA damage checkpoint pathways cooperate to restrain mitotic progression following DNA damage

PLoS Genetics

Volumn 7, Issue 7, 2011, Pages

  Searle, Jennifer S ^a,b   Wood, Matthew D ^a   Kaur, Mandeep ^a   Tobin, David V ^a   Sanchez, Yolanda ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; HEXOKINASE; HEXOKINASE 2; PROTEIN; PROTEIN MCK 1; PROTEIN ZDS 1; PROTEIN ZDS 2; UNCLASSIFIED DRUG; CYCLIC AMP; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CARBON SOURCE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL GROWTH; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVITY; GENE LOCATION; MOLECULAR INTERACTION; NUTRIENT CYCLE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANAPHASE; BIOLOGICAL MODEL; CYTOLOGY; FOOD; GENETICS; METABOLISM; MITOSIS; MUTATION; PHOSPHORYLATION; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

ANAPHASE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA DAMAGE; FOOD; MITOSIS; MODELS, BIOLOGICAL; MUTATION; PHOSPHORYLATION; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 79960968062     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002176     Document Type: Article

References (64)

1. Cohen-Fix O, Peters JM, Kirschner MW, Koshland D, (1996) Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10: 3081-3093.
2. Visintin R, Prinz S, Amon A, (1997) CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278: 460-463.
3. Irniger S, Piatti S, Michaelis C, Nasmyth K, (1995) Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81: 269-278.
4. Ciosk R, Zachariae W, Michaelis C, Shevchenko A, Mann M, et al. (1998) An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93: 1067-1076.
5. Uhlmann F, Lottspeich F, Nasmyth K, (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400: 37-42.
6. Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, et al. (1997) Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278: 455-460.
7. Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, et al. (1998) The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2: 709-718.
8. Shou W, Seol JH, Shevchenko A, Baskerville C, Moazed D, et al. (1999) Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 97: 233-244.
9. Jaspersen SL, Charles JF, Tinker-Kulberg RL, Morgan DO, (1998) A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol Biol Cell 9: 2803-2817.
10. Visintin R, Hwang ES, Amon A, (1999) Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus [see comments]. Nature 398: 818-823.
11. Shou W, Azzam R, Chen SL, Huddleston MJ, Baskerville C, et al. (2002) Cdc5 influences phosphorylation of Net1 and disassembly of the RENT complex. BMC Mol Biol 3: 3.
12. Stegmeier F, Amon A, (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38: 203-232.
13. Queralt E, Lehane C, Novak B, Uhlmann F, (2006) Downregulation of PP2A(Cdc55) phosphatase by separase initiates mitotic exit in budding yeast. Cell 125: 719-732.
14. Queralt E, Uhlmann F, (2008) Cdk-counteracting phosphatases unlock mitotic exit. Curr Opin Cell Biol 20: 661-668.
15. Jin F, Liu H, Liang F, Rizkallah R, Hurt MM, et al. (2008) Temporal control of the dephosphorylation of Cdk substrates by mitotic exit pathways in budding yeast. Proc Natl Acad Sci U S A 105: 16177-16182.
16. Lim HH, Goh PY, Surana U, (1998) Cdc20 is essential for the cyclosome-mediated proteolysis of both Pds1 and Clb2 during M phase in budding yeast. Curr Biol 8: 231-234.
17. Baumer M, Braus GH, Irniger S, (2000) Two different modes of cyclin clb2 proteolysis during mitosis in Saccharomyces cerevisiae. FEBS Lett 468: 142-148.
18. Wasch R, Cross FR, (2002) APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 418: 556-562.
19. 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.
20. Wang Y, Hu F, Elledge SJ, (2000) The Bfa1/Bub2 GAP complex comprises a universal checkpoint required to prevent mitotic exit. Curr Biol 10: 1379-1382.
21. 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.
22. Alexandru G, Zachariae W, Schleiffer A, Nasmyth K, (1999) Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage. Embo J 18: 2707-2721.
23. Li R, (1999) Bifurcation of the mitotic checkpoint pathway in budding yeast. Proc Natl Acad Sci U S A 96: 4989-4994.
24. Elledge SJ, (1996) Cell cycle checkpoints: preventing an identity crisis. Science 274: 1664-1672.
25. Clarke DJ, Gimenez-Abian JF, (2000) Checkpoints controlling mitosis. Bioessays 22: 351-363.
26. Yamada H, Kumada K, Yanagida M, (1997) Distinct subunit functions and cell cycle regulated phosphorylation of 20S APC/cyclosome required for anaphase in fission yeast. J Cell Sci 110 (Pt 15): 1793-1804.
27. Anghileri P, Branduardi P, Sternieri F, Monti P, Visintin R, et al. (1999) Chromosome separation and exit from mitosis in budding yeast: dependence on growth revealed by cAMP-mediated inhibition. Exp Cell Res 250: 510-523.
28. Heo SJ, Tatebayashi K, Ikeda H, (1999) The budding yeast cohesin gene SCC1/MCD1/RHC21 genetically interacts with PKA, CDK and APC. Curr Genet 36: 329-338.
29. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA, (2002) TOWARD MAINTAINING THE GENOME: DNA Damage and Replication Checkpoints. Annu Rev Genet 36: 617-656.
30. Wang H, Liu D, Wang Y, Qin J, Elledge SJ, (2001) Pds1 phosphorylation in response to DNA damage is essential for its DNA damage checkpoint function. Genes Dev 15: 1361-1372.
31. 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.
32. Agarwal R, Tang Z, Yu H, Cohen-Fix O, (2003) Two distinct pathways for inhibiting pds1 ubiquitination in response to DNA damage. J Biol Chem 278: 45027-45033.
33. Zhang T, Nirantar S, Lim HH, Sinha I, Surana U, (2009) DNA damage checkpoint maintains CDH1 in an active state to inhibit anaphase progression. Dev Cell 17: 541-551.
34. Searle JS, Schollaert KL, Wilkins BJ, Sanchez Y, (2004) The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat Cell Biol 6: 138-145.
35. Cannon JF, Tatchell K, (1987) Characterization of Saccharomyces cerevisiae genes encoding subunits of cyclic AMP-dependent protein kinase. Mol Cell Biol 7: 2653-2663.
36. Toda T, Cameron S, Sass P, Zoller M, Scott JD, et al. (1987) Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol Cell Biol 7: 1371-1377.
37. Toda T, Cameron S, Sass P, Zoller M, Wigler M, (1987) Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 50: 277-287.
38. Thevelein JM, de Winde JH, (1999) Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33: 904-918.
39. Rolland F, Wanke V, Cauwenberg L, Ma P, Boles E, et al. (2001) The role of hexose transport and phosphorylation in cAMP signalling in the yeast Saccharomyces cerevisiae. FEM Yeast Res 1: 33-45.
40. Colledge M, Scott JD, (1999) AKAPs: from structure to function. Trends Cell Biol 9: 216-221.
41. Griffioen G, Branduardi P, Ballarini A, Anghileri P, Norbeck J, et al. (2001) Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain. Mol Cell Biol 21: 511-523.
42. Griffioen G, Swinnen S, Thevelein JM, (2003) Feedback inhibition of cell wall integrity signaling by Zds1 involves Gsk3 phosphorylation of a cAMP-dependent protein kinase regulatory subunit. J Biol Chem 18: 18.
43. Griffioen G, Thevelein JM, (2002) Molecular mechanisms controlling the localisation of protein kinase A. Curr Genet 41: 199-207.
44. Weinert TA, Kiser GL, Hartwell LH, (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev 8: 652-665.
45. Garvik B, Carson M, Hartwell L, (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.
46. Desany BA, Alcasabas AA, Bachant JB, Elledge SJ, (1998) Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev 12: 2956-2970.
47. Mizunuma M, Hirata D, Miyaoka R, Miyakawa T, (2001) GSK-3 kinase Mck1 and calcineurin coordinately mediate Hsl1 down-regulation by Ca2+ in budding yeast. Embo J 20: 1074-1085.
48. Boutelet F, Petitjean A, Hilger F, (1985) Yeast cdc35 mutants are defective in adenylate cyclase and are allelic with cyr1 mutants while CAS1, a new gene, is involved in the regulation of adenylate cyclase. Embo J 4: 2635-2641.
49. Dubacq C, Guerois R, Courbeyrette R, Kitagawa K, Mann C, (2002) Sgt1p contributes to cyclic AMP pathway activity and physically interacts with the adenylyl cyclase Cyr1p/Cdc35p in budding yeast. Eukaryot Cell 1: 568-582.
50. Gorner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, et al. (1998) Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12: 586-597.
51. Thevelein JM, (1994) Signal transduction in yeast. Yeast 10: 1753-1790.
52. Shero JH, Hieter P, (1991) A suppressor of a centromere DNA mutation encodes a putative protein kinase (MCK1). Genes Dev 5: 549-560.
53. Wood MD, Sanchez Y, (2010) Deregulated Ras signaling compromises DNA damage checkpoint recovery in S. cerevisiae. Cell Cycle 9: 3353-3363.
54. Queralt E, Uhlmann F, (2008) Separase cooperates with Zds1 and Zds2 to activate Cdc14 phosphatase in early anaphase. J Cell Biol 182: 873-883.
55. Bi E, Pringle JR, (1996) ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol Cell Biol 16: 5264-5275.
56. Fraschini R, D'Ambrosio C, Venturetti M, Lucchini G, Piatti S, (2006) Disappearance of the budding yeast Bub2-Bfa1 complex from the mother-bound spindle pole contributes to mitotic exit. J Cell Biol 172: 335-346.
57. Maekawa H, Priest C, Lechner J, Pereira G, Schiebel E, (2007) The yeast centrosome translates the positional information of the anaphase spindle into a cell cycle signal. J Cell Biol 179: 423-436.
58. Pereira G, Schiebel E, (2005) Kin4 kinase delays mitotic exit in response to spindle alignment defects. Mol Cell 19: 209-221.
59. Gentry MS, Hallberg RL, (2002) Localization of Saccharomyces cerevisiae protein phosphatase 2A subunits throughout mitotic cell cycle. Mol Biol Cell 13: 3477-3492.
60. Matyakhina L, Lenherr SM, Stratakis CA, (2002) Protein kinase A and chromosomal stability. Ann N Y Acad Sci 968: 148-157.
61. Pan X, Heitman J, (1999) Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19: 4874-4887.
62. Foiani M, Marini F, Gamba D, Lucchini G, Plevani P, (1994) The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol Cell Biol 14: 923-933.
63. Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ, (1994) The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev 8: 2401-2415.
64. 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.