Phosphate-activated cyclin-dependent kinase stabilizes G1 cyclin to trigger cell cycle entry

Molecular and Cellular Biology

Volumn 33, Issue 7, 2013, Pages 1273-1284

  Menoyo, S ^a   Ricco, N ^a   Bru, S ^a   Hernandez Ortega S ^a   Escote X ^b   Aldea, M ^c   Cloteta, J ^a  

^a UNIVERSITAT INTERNACIONAL DE CATALUNYA   (Spain)

^b HOSPITAL UNIVERSITARI JOAN XXIII   (Spain)

^c INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CYCLIN DEPENDENT KINASE; CYCLIN G1; PHOSPHATE; PHOSPHATE 85; PROTEIN CLN 3; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CELL CYCLE REGULATION; ENVIRONMENTAL CHANGE; G1 PHASE CELL CYCLE CHECKPOINT; NONHUMAN; NUTRIENT AVAILABILITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE;

AUTOPHAGY; CDC28 PROTEIN KINASE, S CEREVISIAE; CELL CYCLE; CELL CYCLE CHECKPOINTS; CYCLIN G1; CYCLIN-DEPENDENT KINASES; CYCLINS; DOWN-REGULATION; G0 PHASE; G1 PHASE; PHOSPHATES; PHOSPHORYLATION; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN;

EID: 84875262072     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01556-12     Document Type: Article

References (50)

1. De Virgilio C. 2012. The essence of yeast quiescence. FEMS Microbiol. Rev. 36:306-339.
2. Wittenberg C, Reed SI.2005. Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes.Oncogene24: 2746-2755.
3. Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabrielian AE, Landsman D, Lockhart DJ, Davis RW.1998. A genome-wide transcriptional analysis of the mitotic cell cycle.Mol.Cell 2:65-73.
4. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B.1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.Mol. Biol. Cell9:3273-3297.
5. Koch C, Nasmyth K.1994. Cell cycle regulated transcription in yeast.Curr. Opin. Cell Biol--. 6:451-459.
6. Cosma MP, Panizza S, Nasmyth K.2001. Cdk1 triggers association of RNA polymerase to cell cycle promoters only after recruitment of the mediator by SBF.Mol. Cell7:1213-1220.
7. Koch C, Schleiffer A, Ammerer G, Nasmyth K.1996. Switching transcription on and off during the yeast cell cycle: Cln/Cdc28 kinases activate bound transcription factor SBF (Swi4/Swi6) at start, whereas Clb/Cdc28 kinases displace it from the promoter in G2.Genes Dev.10:129-141.
8. Cross FR, Blake CM.1993. The yeast Cln3 protein is an unstable activator of Cdc28.Mol. Cell. Biol.13:3266-3271.
9. Yaglom J, Linskens MH, Sadis S, Rubin DM, Futcher B, Finley D.1995. p34Cdc28-mediated control of Cln3 cyclin degradation.Mol. Cell. Biol. 15:731-741.
10. Costanzo M, Nishikawa JL, Tang X, Millman JS, Schub O, Breitkreuz K, Dewar D, Rupes I, Andrews B, Tyers M.2004. CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast.Cell117:899-913.
11. de Bruin RA, McDonald WH, Kalashnikova TI, Yates J, III, Wittenberg C.2004. Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5.Cell117:887-898.
12. Wagner MV, Smolka MB, de Bruin RA, Zhou H, Wittenberg C, Dowdy SF.2009. Whi5 regulation by site specific CDK-phosphorylation in Saccharomyces cerevisiae.PLoS One 4:e4300.doi:10.1371/journal.pone.0004300.
13. Wang H, Carey LB, Cai Y, Wijnen H, Futcher B.2009. Recruitment of Cln3 cyclin to promoters controls cell cycle entry via histone deacetylase and other targets.PLoS Biol.7:e1000189. doi:10.1371/journal.pbio .1000189.
14. Skotheim JM, Di Talia S, Siggia ED, Cross FR.2008. Positive feedback of G1 cyclins ensures coherent cell cycle entry.Nature454:291-296.
15. Cross FR, Schroeder L, Bean JM.2007. Phosphorylation of the Sic1 inhibitor of B-type cyclins in Saccharomyces cerevisiae is not essential but contributes to cell cycle robustness.Genetics176:1541-1555.
16. Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M.2004. "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol.Mol. Biol. Rev.68:187-206.
17. Martin DE, Hall MN.2005. The expanding TOR signaling network.Curr. Opin. Cell Biol.17:158-166.
18. Gallego C, Gari E, Colomina N, Herrero E, Aldea M.1997. The Cln3 cyclin is down-regulated by translational repression and degradation during the G1 arrest caused by nitrogen deprivation in budding yeast.EMBO J.16:7196-7206.
19. Lee YS, Huang K, Quiocho FA, O'Shea EK.2008. Molecular basis of cyclin-CDK-CKI regulation by reversible binding of an inositol pyrophosphate.Nat. Chem. Biol.4:25-32.
20. Huang D, Friesen H, Andrews B.2007. Pho85, a multifunctional cyclindependent protein kinase in budding yeast.Mol. Microbiol.66:303-314.
21. Schneider KR, Smith RL, O'Shea EK.1994. Phosphate-regulated inactivation of the kinase PHO80-PHO85 by the CDK inhibitor PHO81.Science266:122-126.
22. Lee YS, Mulugu S, York JD, O'Shea EK.2007. Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates.Science316: 109-112.
23. Nishizawa M, Komai T, Katou Y, Shirahige K, Ito T, Toh-E A.2008. Nutrient-regulated antisense and intragenic RNAs modulate a signal transduction pathway in yeast.PLoS Biol.6:2817-2830.
24. O'Neill EM, Kaffman A, Jolly ER, O'Shea EK.1996. Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex.Science271: 209-212.
25. Wanke V, Pedruzzi I, Cameroni E, Dubouloz F, De Virgilio C.2005. Regulation of G0 entry by the Pho80-Pho85 cyclin-CDK complex.EMBO J.24: 4271-4278.
26. Wysocki R, Javaheri A, Kristjansdottir K, Sha F, Kron SJ.2006. CDK Pho85 targets CDK inhibitor Sic1 to relieve yeast G1 checkpoint arrest after DNA damage.Nat. Struct. Mol. Biol.13: 908-914.
27. Carroll AS, Bishop AC, DeRisi JL, Shokat KM, O'Shea EK.2001. Chemical inhibition of the Pho85 cyclin-dependent kinase reveals a role in the environmental stress response.Proc. Natl. Acad. Sci. U. S. A.98: 12578-12583.
28. Gietz RD, Sugino A.1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.Gene74:527-534.
29. Clotet J, Escote X, Adrover MA, Yaakov G, Gari E, Aldea M, de Nadal E, Posas F.2006. Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity.EMBO J.25:2338-2346.
30. Haase SB, Reed SI.2002. Improved flow cytometric analysis of the budding yeast cell cycle.Cell Cycle1:132-136.
31. Hernandez-Ortega S, Bru S, Ricco N, Ramirez S, Casals N, Jimenez J, Isasa M, Crosas B, Clotet J. 21 December2012. Defective in mitotic arrest 1 (Dma1) ubiquitin ligase controls G1 cyclin degradation.J. Biol. Chem.[Epub ahead of print.] doi:10.1074/jbc.M112.426593.
32. Fabrizio P, Longo VD.2007. The chronological life span of Saccharomyces cerevisiae.Methods Mol. Biol.371:89-95.
33. Schneider BL, Yang QH, Futcher AB.1996. Linkage of replication to start by the Cdk inhibitor Sic1.Science272:560-562.
34. Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, Winderickx J.2010. Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae.Curr. Genet.56:1-32.
35. Johnston GC, Pringle JR, Hartwell LH.1977. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae.Exp. Cell Res.105:79-98.
36. Yang Z, Geng J, Yen WL, Wang K, Klionsky DJ.2010. Positive or negative roles of different cyclin-dependent kinase Pho85-cyclin complexes orchestrate induction of autophagy in Saccharomyces cerevisiae.Mol. Cell38:250-264.
37. Verges E, Colomina N, Gari E, Gallego C, Aldea M.2007. Cyclin Cln3 is retained at the ER and released by the J chaperone Ydj1 in late G1 to trigger cell cycle entry.Mol. Cell26:649-662.
38. Weinberger M, Feng L, Paul A, Smith DL, Jr, Hontz RD, Smith JS, Vujcic M, Singh KK, Huberman JA, Burhans WC.2007. DNA replication stress is a determinant of chronological lifespan in budding yeast.PLoS One2:e748. doi:10.1371/journal.pone.0000748.
39. Zinzalla V, Graziola M, Mastriani A, Vanoni M, Alberghina L.2007. Rapamycin-mediated G1 arrest involves regulation of the Cdk inhibitor Sic1 in Saccharomyces cerevisiae.Mol. Microbiol.63:1482-1494.
40. Boer VM, Crutchfield CA, Bradley PH, Botstein D, Rabinowitz JD.2010. Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations.Mol. Biol. Cell21:198-211.
41. Thomas MR, O'Shea EK.--2005. An intracellular phosphate buffer filters transient fluctuations in extracellular phosphate levels.Proc. Natl. Acad. Sci. U. S. A.102:9565-9570.
42. Hall DD, Markwardt DD, Parviz F, Heideman W.1998. Regulation of the Cln3-Cdc28 kinase by cAMP in Saccharomyces cerevisiae.EMBO J.17:4370-4378.
43. Polymenis M, Schmidt EV.1997. Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast.Genes Dev.11: 2522-2531.
44. Truman AW, Kristjansdottir K, Wolfgeher D, Hasin N, Polier S, Zhang H, Perrett S, Prodromou C, Jones GW, Kron SJ.2012. CDK-dependent Hsp70 phosphorylation controls G1 cyclin abundance and cell-cycle progression.Cell151:1308-1318.
45. Escote X, Zapater M, Clotet J, Posas F.2004. Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1.Nat. Cell Biol.6:997-1002.
46. Holmes JK, Solomon MJ.1996. A predictive scale for evaluating cyclindependent kinase substrates. A comparison of p34cdc2 and p33cdk2.J. Biol. Chem.271:25240-25246.
47. Songyang Z, Lu KP, Kwon YT, Tsai LH, Filhol O, Cochet C, Brickey DA, Soderling TR, Bartleson C, Graves DJ, DeMaggio AJ, Hoekstra MF, Blenis J, Hunter T, Cantley LC.1996. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulindependent kinase II, CDK5, and Erk1.Mol. Cell. Biol.16:6486-6493.
48. Huang K, Ferrin-O'Connell I, Zhang W, Leonard GA, O'Shea EK, Quiocho FA.2007. Structure of the Pho85-Pho80 CDK-cyclin complex of the phosphate-responsive signal transduction pathway.Mol. Cell28:614-623.
49. Nash R, Tokiwa G, Anand S, Erickson K, Futcher AB.1988. The WHI1 gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog.EMBO J.7:4335-4346.
50. Igual JC, Johnson AL, Johnston LH.1996. Coordinated regulation of gene expression by the cell cycle transcription factor Swi4 and the protein kinase C MAP kinase pathway for yeast cell integrity.EMBO J.15:5001-5013.