Nutrient sensing kinases PKA and sch9 phosphorylate the catalytic domain of the ubiquitin-conjugating enzyme Cdc34

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Cocklin, Ross ^a   Goebl, Mark ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN CDC34; PROTEIN SCH9; UBIQUITIN CONJUGATING ENZYME; UNCLASSIFIED DRUG; ANAPHASE PROMOTING COMPLEX; ANAPHASE-PROMOTING COMPLEX; PROTEIN KINASE; SCH9 PROTEIN KINASE; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL GROWTH; CELL SIZE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; UBIQUITINATION; WESTERN BLOTTING; YEAST CELL; ANIMAL; CELL CYCLE; CELL DIVISION; CHEMISTRY; ENZYME ACTIVE SITE; FOOD; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; CATALYTIC DOMAIN; CELL CYCLE; CELL DIVISION; CELL SIZE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FOOD; HUMANS; PHOSPHORYLATION; PROTEIN KINASES; SPECIES SPECIFICITY; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 80455174489     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027099     Document Type: Article

References (69)

1. Glickman MH, Ciechanover A, (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82: 373-428.
2. Goebl MG, Yochem J, Jentsch S, McGrath JP, Varshavsky A, et al. (1988) The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme. Science 241: 1331-1335.
3. Mathias N, Steussy CN, Goebl MG, (1998) An essential domain within Cdc34p is required for binding to a complex containing Cdc4p and Cdc53p in Saccharomyces cerevisiae. J Biol Chem 273: 4040-4045.
4. Deshaies RJ, (1999) SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15: 435-467.
5. Henchoz S, Chi Y, Catarin B, Herskowitz I, Deshaies RJ, et al. (1997) Phosphorylation- and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast. Genes Dev 11: 3046-3060.
6. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW, (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91: 209-219.
7. Verma R, Feldman RM, Deshaies RJ, (1997) SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34, and cyclin/CDK activities. Mol Biol Cell 8: 1427-1437.
8. Skowyra D, Koepp DM, Kamura T, Conrad MN, Conaway RC, et al. (1999) Reconstitution of G1 cyclin ubiquitination with complexes containing SCFGrr1 and Rbx1. Science 284: 662-665.
9. Petroski MD, Deshaies RJ, (2005) Mechanism of lysine 48-linked ubiquitin-chain synthesis by the cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 123: 1107-1120.
10. Gazdoiu S, Yamoah K, Wu K, Escalante CR, Tappin I, et al. (2005) Proximity-induced activation of human Cdc34 through heterologous dimerization. Proc Natl Acad Sci U S A 102: 15053-15058.
11. Varelas X, Ptak C, Ellison MJ, (2003) Cdc34 self-association is facilitated by ubiquitin thiolester formation and is required for its catalytic activity. Mol Cell Biol 23: 5388-5400.
12. Pitluk ZW, McDonough M, Sangan P, Gonda DK, (1995) Novel CDC34 (UBC3) ubiquitin-conjugating enzyme mutants obtained by charge-to-alanine scanning mutagenesis. Mol Cell Biol 15: 1210-1219.
13. Liu Y, Mathias N, Steussy CN, Goebl MG, (1995) Intragenic suppression among CDC34 (UBC3) mutations defines a class of ubiquitin-conjugating catalytic domains. Mol Cell Biol 15: 5635-5644.
14. Lass A, Cocklin R, Scaglione KM, Skowyra M, Korolev S, et al. (2011) The loop-less tmCdc34 E2 mutant defective in polyubiquitination in vitro and in vivo supports yeast growth in a manner dependent on Ubp14 and Cka2. Cell Div 6: 7.
15. Cocklin R, Heyen J, Larry T, Tyers M, Goebl M, (2011) New insight into the role of the Cdc34 ubiquitin-conjugating enzyme in cell cycle regulation via Ace2 and Sic1. Genetics 187: 701-715.
16. Goebl MG, Goetsch L, Byers B, (1994) The Ubc3 (Cdc34) ubiquitin-conjugating enzyme is ubiquitinated and phosphorylated in vivo. Mol Cell Biol 14: 3022-3029.
17. Coccetti P, Tripodi F, Tedeschi G, Nonnis S, Marin O, et al. (2008) The CK2 phosphorylation of catalytic domain of Cdc34 modulates its activity at the G1 to S transition in Saccharomyces cerevisiae. Cell Cycle 7: 1391-1401.
18. Sadowski M, Mawson A, Baker R, Sarcevic B, (2007) Cdc34 C-terminal tail phosphorylation regulates Skp1/cullin/F-box (SCF)-mediated ubiquitination and cell cycle progression. Biochem J 405: 569-581.
19. Horvath A, Riezman H, (1994) Rapid protein extraction from Saccharomyces cerevisiae. Yeast 10: 1305-1310.
20. Martzen MR, McCraith SM, Spinelli SL, Torres FM, Fields S, et al. (1999) A biochemical genomics approach for identifying genes by the activity of their products. Science 286: 1153-1155.
21. Backer JM, (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 410: 1-17.
22. Irniger S, Baumer M, Braus GH, (2000) Glucose and ras activity influence the ubiquitin ligases APC/C and SCF in Saccharomyces cerevisiae. Genetics 154: 1509-1521.
23. Santangelo GM, (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 253-282.
24. Hixson CS, Krebs EG, (1980) Characterization of a cyclic AMP-binding protein from bakers' yeast. Identification as a regulatory subunit of cyclic AMP-dependent protein kinase. J Biol Chem 255: 2137-2145.
25. 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.
26. 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.
27. Cameron S, Levin L, Zoller M, Wigler M, (1988) cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae. Cell 53: 555-566.
28. Tegge W, Frank R, Hofmann F, Dostmann WR, (1995) Determination of cyclic nucleotide-dependent protein kinase substrate specificity by the use of peptide libraries on cellulose paper. Biochemistry 34: 10569-10577.
29. Songyang Z, Blechner S, Hoagland N, Hoekstra MF, Piwnica-Worms H, et al. (1994) Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 4: 973-982.
30. Denis CL, Kemp BE, Zoller MJ, (1991) Substrate specificities for yeast and mammalian cAMP-dependent protein kinases are similar but not identical. J Biol Chem 266: 17932-17935.
31. Smith CM, Radzio-Andzelm E, Madhusudan, Akamine P, Taylor SS, (1999) The catalytic subunit of cAMP-dependent protein kinase: prototype for an extended network of communication. Prog Biophys Mol Biol 71: 313-341.
32. Jacinto E, Lorberg A, (2008) TOR regulation of AGC kinases in yeast and mammals. Biochem J 410: 19-37.
33. Chang F, Herskowitz I, (1990) Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell 63: 999-1011.
34. Oehlen LJ, Cross FR, (1994) G1 cyclins CLN1 and CLN2 repress the mating factor response pathway at Start in the yeast cell cycle. Genes Dev 8: 1058-1070.
35. Weinberger M, Feng L, Paul A, Smith DL Jr, Hontz RD, et al. (2007) DNA replication stress is a determinant of chronological lifespan in budding yeast. PLoS ONE 2: e748.
36. 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.
37. Lindstrom DL, Gottschling DE, (2009) The mother enrichment program: a genetic system for facile replicative life span analysis in Saccharomyces cerevisiae. Genetics 183: 413-422 411SI-413SI.
38. Longo VD, Fabrizio P, (2002) Regulation of longevity and stress resistance: a molecular strategy conserved from yeast to humans? Cell Mol Life Sci 59: 903-908.
39. Bitterman KJ, Medvedik O, Sinclair DA, (2003) Longevity regulation in Saccharomyces cerevisiae: linking metabolism, genome stability, and heterochromatin. Microbiol Mol Biol Rev 67: 376-399 table of contents.
40. Pesin JA, Orr-Weaver TL, (2008) Regulation of APC/C activators in mitosis and meiosis. Annu Rev Cell Dev Biol 24: 475-499.
41. Duda DM, Scott DC, Calabrese MF, Zimmerman ES, Zheng N, et al. (2011) Structural regulation of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 21: 257-264.
42. Vodermaier HC, (2004) APC/C and SCF: controlling each other and the cell cycle. Curr Biol 14: R787-796.
43. Tripodi F, Zinzalla V, Vanoni M, Alberghina L, Coccetti P, (2007) In CK2 inactivated cells the cyclin dependent kinase inhibitor Sic1 is involved in cell-cycle arrest before the onset of S phase. Biochem Biophys Res Commun 359: 921-927.
44. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A, (2005) The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol Cell 20: 589-599.
45. Mbonyi K, van Aelst L, Arguelles JC, Jans AW, Thevelein JM, (1990) Glucose-induced hyperaccumulation of cyclic AMP and defective glucose repression in yeast strains with reduced activity of cyclic AMP-dependent protein kinase. Mol Cell Biol 10: 4518-4523.
46. Byfield MP, Murray JT, Backer JM, (2005) hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082.
47. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, et al. (2005) Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci U S A 102: 14238-14243.
48. Sonenberg N, Hinnebusch AG, (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
49. Wilson WA, Hawley SA, Hardie DG, (1996) Glucose repression/derepression in budding yeast: SNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP:ATP ratio. Curr Biol 6: 1426-1434.
50. Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D, et al. (2007) Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell 26: 663-674.
51. Lu JY, Lin YY, Sheu JC, Wu JT, Lee FJ, et al. (2011) Acetylation of Yeast AMPK Controls Intrinsic Aging Independently of Caloric Restriction. Cell 146: 969-979.
52. Griffioen G, Swinnen S, Thevelein JM, (2003) Feedback inhibition on cell wall integrity signaling by Zds1 involves Gsk3 phosphorylation of a cAMP-dependent protein kinase regulatory subunit. J Biol Chem 278: 23460-23471.
53. 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.
54. Toda T, Cameron S, Sass P, Wigler M, (1988) SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits. Genes Dev 2: 517-527.
55. Yorimitsu T, Zaman S, Broach JR, Klionsky DJ, (2007) Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol Biol Cell 18: 4180-4189.
56. Wu K, Kovacev J, Pan ZQ, (2010) Priming and extending: a UbcH5/Cdc34 E2 handoff mechanism for polyubiquitination on a SCF substrate. Mol Cell 37: 784-796.
57. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292: 107-110.
58. Johnson TE, (1990) Increased life-span of age-1 mutants in Caenorhabditis elegans and lower Gompertz rate of aging. Science 249: 908-912.
59. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, et al. (2001) Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292: 104-106.
60. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R, (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
61. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A, (1996) Dwarf mice and the ageing process. Nature 384: 33.
62. Hsieh CC, DeFord JH, Flurkey K, Harrison DE, Papaconstantinou J, (2002) Implications for the insulin signaling pathway in Snell dwarf mouse longevity: a similarity with the C. elegans longevity paradigm. Mech Ageing Dev 123: 1229-1244.
63. Flurkey K, Papaconstantinou J, Harrison DE, (2002) The Snell dwarf mutation Pit1(dw) can increase life span in mice. Mech Ageing Dev 123: 121-130.
64. Colombo S, Ronchetti D, Thevelein JM, Winderickx J, Martegani E, (2004) Activation state of the Ras2 protein and glucose-induced signaling in Saccharomyces cerevisiae. J Biol Chem 279: 46715-46722.
65. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
66. Harlow E, Lane D, (1999) Using Antibodies: A Laboratory Manual Plainview Cold Spring Harbor Laboratory Press.
67. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
68. Schweitzer K, Cocklin R, Garrett L, Desai F, Goebl M, (2005) The ubiquitin ligase SCFGrr1 is necessary for pheromone sensitivity in Saccharomyces cerevisiae. Yeast 22: 553-564.
69. Zaremberg V, Moreno S, (1996) Analysis of the mechanism of activation of cAMP-dependent protein kinase through the study of mutants of the yeast regulatory subunit. Eur J Biochem 237: 136-142.