Regulation of Hxt3 and Hxt7 Turnover Converges on the Vid30 Complex and Requires Inactivation of the Ras/cAMP/PKA Pathway in Saccharomyces cerevisiae

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Snowdon, Chris ^a   van der Merwe, George ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL PROTEIN; GLUCOSE TRANSPORTER; HXT3 PROTEIN; HXT7 PROTEIN; RAS PROTEIN; RAS2 PROTEIN; RIM15 PROTEIN; RSP5 PROTEIN; TORC1 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VID30 COMPLEX;

ARTICLE; ENDOCYTOSIS; ENZYME INACTIVATION; ENZYME INHIBITION; NONHUMAN; NUTRIENT; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; UBIQUITINATION;

BLOTTING, WESTERN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ETHANOL; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; MICROSCOPY, FLUORESCENCE; MONOSACCHARIDE TRANSPORT PROTEINS; RAS PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION; VESICULAR TRANSPORT PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84870828146     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050458     Document Type: Article

References (66)

1. Barbet NC, Schneider U, Helliwell SB, Stansfield I, Tuite MF, et al. (1996) TOR controls translation initiation and early G1 progression in yeast. Mol Biol Cell 7: 25-42.
2. 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.
3. Smith A, Ward MP, Garrett S, (1998) Yeast PKA represses Msn2p/Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J 17: 3556-3564.
4. Beck T, Hall MN, (1999) The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402: 689-692.
5. Cardenas ME, Cutler NS, Lorenz MC, Di Como CJ, Heitman J, (1999) The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev 13: 3271-3279.
6. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, et al. (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150: 1507-1513.
7. Kamada Y, Sekito T, Ohsumi Y, (2004) Autophagy in yeast: a TOR-mediated response to nutrient starvation. Curr Top Microbiol Immunol 279: 73-84.
8. Powers T, Dilova I, Chen CY, Wedaman K, (2004) Yeast TOR signaling: a mechanism for metabolic regulation. Curr Top Microbiol Immunol 279: 39-51.
9. Powers T, Walter P, (1999) Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol Biol Cell 10: 987-1000.
10. Roosen J, Engelen K, Marchal K, Mathys J, Griffioen G, et al. (2005) PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol Microbiol 55: 862-880.
11. Petkova MI, Pujol-Carrion N, Arroyo J, Garcia-Cantalejo J, Angeles de la Torre-Ruiz M, (2010) Mtl1 is required to activate general stress response through Tor1 and Ras2 inhibition under conditions of glucose starvation and oxidative stress. J Biol Chem 285: 19521-19531.
12. De Wever V, Reiter W, Ballarini A, Ammerer G, Brocard C, (2005) A dual role for PP1 in shaping the Msn2-dependent transcriptional response to glucose starvation. EMBO J 24: 4115-4123.
13. Schmelzle T, Beck T, Martin DE, Hall MN, (2004) Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol Cell Biol 24: 338-351.
14. Pedruzzi I, Dubouloz F, Cameroni E, Wanke V, Roosen J, et al. (2003) TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell 12: 1607-1613.
15. 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.
16. Haney SA, Broach JR, (1994) Cdc25p, the guanine nucleotide exchange factor for the Ras proteins of Saccharomyces cerevisiae, promotes exchange by stabilizing Ras in a nucleotide-free state. J Biol Chem 269: 16541-16548.
17. Broek D, Toda T, Michaeli T, Levin L, Birchmeier C, et al. (1987) The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell 48: 789-799.
18. Matsumoto K, Uno I, Oshima Y, Ishikawa T, (1982) Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc Natl Acad Sci U S A 79: 2355-2359.
19. Tanaka K, Lin BK, Wood DR, Tamanoi F, (1991) IRA2, an upstream negative regulator of RAS in yeast, is a RAS GTPase-activating protein. Proc Natl Acad Sci U S A 88: 468-472.
20. Tanaka K, Nakafuku M, Satoh T, Marshall MS, Gibbs JB, et al. (1990) S. cerevisiae genes IRA1 and IRA2 encode proteins that may be functionally equivalent to mammalian ras GTPase activating protein. Cell 60: 803-807.
21. Nikawa J, Cameron S, Toda T, Ferguson KM, Wigler M, (1987) Rigorous feedback control of cAMP levels in Saccharomyces cerevisiae. Genes Dev 1: 931-937.
22. Wilson RB, Tatchell K, (1988) SRA5 encodes the low-Km cyclic AMP phosphodiesterase of Saccharomyces cerevisiae. Mol Cell Biol 8: 505-510.
23. Cameroni E, Hulo N, Roosen J, Winderickx J, De Virgilio C, (2004) The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle 3: 462-468.
24. Krampe S, Boles E, (2002) Starvation-induced degradation of yeast hexose transporter Hxt7p is dependent on endocytosis, autophagy and the terminal sequences of the permease. FEBS Lett 513: 193-196.
25. Snowdon C, Hlynialuk C, van der Merwe G, (2008) Components of the Vid30c are needed for the rapamycin-induced degradation of the high-affinity hexose transporter Hxt7p in Saccharomyces cerevisiae. FEMS Yeast Res 8: 204-216.
26. Roberts GG, Hudson AP, (2006) Transcriptome profiling of Saccharomyces cerevisiae during a transition from fermentative to glycerol-based respiratory growth reveals extensive metabolic and structural remodeling. Mol Genet Genomics 276: 170-186.
27. Snowdon C, Schierholtz R, Poliszczuk P, Hughes S, van der Merwe G, (2009) ETP1/YHL010c is a novel gene needed for the adaptation of Saccharomyces cerevisiae to ethanol. FEMS Yeast Res 9: 372-380.
28. Pitre S, Dehne F, Chan A, Cheetham J, Duong A, et al. (2006) PIPE: a protein-protein interaction prediction engine based on the re-occurring short polypeptide sequences between known interacting protein pairs. BMC Bioinformatics 7: 365.
29. Braun B, Pfirrmann T, Menssen R, Hofmann K, Scheel H, et al. (2011) Gid9, a second RING finger protein contributes to the ubiquitin ligase activity of the Gid complex required for catabolite degradation. FEBS Lett 585: 3856-3861.
30. Santt O, Pfirrmann T, Braun B, Juretschke J, Kimmig P, et al. (2008) The yeast GID complex, a novel ubiquitin ligase (E3) involved in the regulation of carbohydrate metabolism. Mol Biol Cell 19: 3323-3333.
31. Hung GC, Brown CR, Wolfe AB, Liu J, Chiang HL, (2004) Degradation of the gluconeogenic enzymes fructose-1,6-bisphosphatase and malate dehydrogenase is mediated by distinct proteolytic pathways and signaling events. J Biol Chem 279: 49138-49150.
32. Regelmann J, Schule T, Josupeit FS, Horak J, Rose M, et al. (2003) Catabolite degradation of fructose-1,6-bisphosphatase in the yeast Saccharomyces cerevisiae: a genome-wide screen identifies eight novel GID genes and indicates the existence of two degradation pathways. Mol Biol Cell 14: 1652-1663.
33. Hatakeyama R, Kamiya M, Takahara T, Maeda T, (2010) Endocytosis of the aspartic acid/glutamic acid transporter Dip5 is triggered by substrate-dependent recruitment of the Rsp5 ubiquitin ligase via the arrestin-like protein Aly2. Mol Cell Biol 30: 5598-5607.
34. Springael JY, De Craene JO, Andre B, (1999) The yeast Npi1/Rsp5 ubiquitin ligase lacking its N-terminal C2 domain is competent for ubiquitination but not for subsequent endocytosis of the Gap1 permease. Biochem Biophys Res Commun 257: 561-566.
35. Leon S, Haguenauer-Tsapis R, (2009) Ubiquitin ligase adaptors: regulators of ubiquitylation and endocytosis of plasma membrane proteins. Exp Cell Res 315: 1574-1583.
36. 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.
37. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.
38. Van Driessche B, Tafforeau L, Hentges P, Carr AM, Vandenhaute J, (2005) Additional vectors for PCR-based gene tagging in Saccharomyces cerevisiae and Schizosaccharomyces pombe using nourseothricin resistance. Yeast 22: 1061-1068.
39. Cruz MC, Goldstein AL, Blankenship J, Del Poeta M, Perfect JR, et al. (2001) Rapamycin and less immunosuppressive analogs are toxic to Candida albicans and Cryptococcus neoformans via FKBP12-dependent inhibition of TOR. Antimicrob Agents Chemother 45: 3162-3170.
40. Robinson LC, Gibbs JB, Marshall MS, Sigal IS, Tatchell K, (1987) CDC25: a component of the RAS-adenylate cyclase pathway in Saccharomyces cerevisiae. Science 235: 1218-1221.
41. Onodera J, Ohsumi Y, (2004) Ald6p is a preferred target for autophagy in yeast, Saccharomyces cerevisiae. J Biol Chem 279: 16071-16076.
42. Hedbacker K, Carlson M, (2008) SNF1/AMPK pathways in yeast. Front Biosci 13: 2408-2420.
43. Benanti JA, Cheung SK, Brady MC, Toczyski DP, (2007) A proteomic screen reveals SCFGrr1 targets that regulate the glycolytic-gluconeogenic switch. Nat Cell Biol 9: 1184-1191.
44. Mbonyi K, Thevelein JM, (1988) The high-affinity glucose uptake system is not required for induction of the RAS-mediated cAMP signal by glucose in cells of the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 971: 223-226.
45. Crechet JB, Poullet P, Camonis J, Jacquet M, Parmeggiani A, (1990) Different kinetic properties of the two mutants, RAS2Ile152 and RAS2Val19, that suppress the CDC25 requirement in RAS/adenylate cyclase pathway in Saccharomyces cerevisiae. J Biol Chem 265: 1563-1568.
46. 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.
47. Schmidt A, Beck T, Koller A, Kunz J, Hall MN, (1998) The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J 17: 6924-6931.
48. MacGurn JA, Hsu PC, Smolka MB, Emr SD, (2011) TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147: 1104-1117.
49. Martin DE, Soulard A, Hall MN, (2004) TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969-979.
50. Ramachandran V, Herman PK, (2011) Antagonistic interactions between the cAMP-dependent protein kinase and Tor signaling pathways modulate cell growth in Saccharomyces cerevisiae. Genetics 187: 441-454.
51. Reinders A, Burckert N, Boller T, Wiemken A, De Virgilio C, (1998) Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev 12: 2943-2955.
52. Galan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R, (1996) Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 271: 10946-10952.
53. Springael JY, Andre B, (1998) Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol Biol Cell 9: 1253-1263.
54. Lin CH, MacGurn JA, Chu T, Stefan CJ, Emr SD, (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135: 714-725.
55. Nikko E, Sullivan JA, Pelham HR, (2008) Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep 9: 1216-1221.
56. Krampe S, Stamm O, Hollenberg CP, Boles E, (1998) Catabolite inactivation of the high-affinity hexose transporters Hxt6 and Hxt7 of Saccharomyces cerevisiae occurs in the vacuole after internalization by endocytosis. FEBS Lett 441: 343-347.
57. Hoffman M, Chiang HL, (1996) Isolation of degradation-deficient mutants defective in the targeting of fructose-1,6-bisphosphatase into the vacuole for degradation in Saccharomyces cerevisiae. Genetics 143: 1555-1566.
58. van der Merwe GK, Cooper TG, van Vuuren HJ, (2001) Ammonia regulates VID30 expression and Vid30p function shifts nitrogen metabolism toward glutamate formation especially when Saccharomyces cerevisiae is grown in low concentrations of ammonia. J Biol Chem 276: 28659-28666.
59. Griffioen G, Thevelein JM, (2002) Molecular mechanisms controlling the localisation of protein kinase A. Curr Genet. 41: 199-207.
60. Zaman S, Lippman SI, Zhao X, Broach JR, (2008) How Saccharomyces responds to nutrients. Annu Rev Genet 42: 27-81.
61. Santangelo GM, (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 253-282.
62. Schmelzle T, Hall MN, (2000) TOR, a central controller of cell growth. Cell 103: 253-262.
63. Dennis PB, Fumagalli S, Thomas G, (1999) Target of rapamycin (TOR): balancing the opposing forces of protein synthesis and degradation. Curr Opin Genet Dev 9: 49-54.
64. Vidan S, Mitchell AP, (1997) Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol Cell Biol 17: 2688-2697.
65. Perez-Valle J, Jenkins H, Merchan S, Montiel V, Ramos J, et al. (2007) Key role for intracellular K+ and protein kinases Sat4/Hal4 and Hal5 in the plasma membrane stabilization of yeast nutrient transporters. Mol Cell Biol 27: 5725-5736.
66. Perez-Valle J, Rothe J, Primo C, Martinez Pastor M, Arino J, et al. (2010) Hal4 and Hal5 protein kinases are required for general control of carbon and nitrogen uptake and metabolism. Eukaryot Cell 9: 1881-1890.