Internal amino acids promote Gap1 permease ubiquitylation via TORC1/Npr1/14-3-3-dependent control of the Bul arrestin-like adaptors

Molecular and Cellular Biology

Volumn 32, Issue 22, 2012, Pages 4510-4522

  Merhi, Ahmad ^a   André, Bruno ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; AMINO ACID; AMMONIA; NITROGEN; PERMEASE; PHOSPHATASE; PROTEIN 14 3 3; PROTEIN BUL1; PROTEIN BUL2; PROTEIN GAP1; PROTEIN NPR1; PROTEIN TORC1; RETINA S ANTIGEN; SIT4 PHOSPHATASE; UBIQUITIN LIGASE RSP5; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DISSOCIATION; DOWN REGULATION; ENDOCYTOSIS; ENZYME INACTIVATION; ENZYME INHIBITION; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

14-3-3 PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS; GENE EXPRESSION REGULATION, FUNGAL; LYSOSOMES; PHOSPHORYLATION; PROTEIN KINASES; PROTEOLYSIS; QUATERNARY AMMONIUM COMPOUNDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84868676870     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00463-12     Document Type: Article

References (72)

1. Béchet J, Grenson M, Wiame JM. 1970. Mutations affecting the repressibility of arginine biosynthetic enzymes in Saccharomyces cerevisiae. Eur. J. Biochem. 12:31-39.
2. Beck T, Schmidt A, Hall MN. 1999. Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146: 1227-1238.
3. Becuwe M, et al. 2012. A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 196:247- 259.
4. Binda M, et al. 2009. The Vam6 GEF controls TORC1 by activating the EGO complex. Mol. Cell 35:563-573.
5. Boeckstaens M, Andre B, Marini AM. 2007. The yeast ammonium transport protein Mep2 and its positive regulator, the Npr1 kinase, play an important role in normal and pseudohyphal growth on various nitrogen media through retrieval of excreted ammonium. Mol. Microbiol. 64:534- 546.
6. Bonfils G, et al. 2012. Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol. Cell 46:105-110.
7. Bonneaud N, et al. 1991. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 7:609-615.
8. Breitkreutz A, et al. 2010. A global protein kinase and phosphatase interaction network in yeast. Science 328:1043-1046.
9. Bridges D, Moorhead GB. 2005. 14-3-3 proteins: a number of functions for a numbered protein. Sci. STKE 2005:re10. doi:10.1126/ stke.2962005re10.
10. Crespo JL, Powers T, Fowler B, Hall MN. 2002. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci. U. S. A. 99:6784- 6789.
11. Crespo JL, Hall MN. 2002. Elucidating TOR signaling and rapamycin action: lessons from Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 66:579 -591.
12. De Craene JO, Soetens O, André B. 2001. The Npr1 kinase controls biosynthetic and endocytic sorting of the yeast Gap1 permease. J. Biol. Chem. 276:43939-43948.
13. De Virgilio C. 2012. The essence of yeast quiescence. FEMS Microbiol. Rev. 36:306 -339.
14. Dubouloz F, Deloche O, Wanke V, Cameroni E, De Virgilio C. 2005. The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol. Cell 19:15-26.
15. Dupré S, Urban-Grimal D, Haguenauer-Tsapis R. 2004. Ubiquitin and endocytic internalization in yeast and animal cells. Biochim. Biophys. Acta 1695:89 -111.
16. Duvel K, Broach JR. 2004. The role of phosphatases in TOR signaling in yeast. Curr. Top. Microbiol. Immunol. 279:19 -38.
17. Funakoshi M, Hochstrasser M. 2009. Small epitope-linker modules for PCR-based C-terminal tagging in Saccharomyces cerevisiae. Yeast 26: 185-192.
18. Galan JM, Moreau V, André 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.
19. Gander S, et al. 2008. Identification of the rapamycin-sensitive phosphorylation sites within the Ser/Thr-rich domain of the yeast Npr1 protein kinase. Rapid Commun. Mass Spectrom. 22:3743-3753.
20. Gonzalez A, Ruiz A, Casamayor A, Arino J. 2009. Normal function of the yeast TOR pathway requires the type 2C protein phosphatase Ptc1. Mol. Cell. Biol. 29:2876 -2888.
21. Grenson M. 1983. Inactivation-reactivation process and repression of permease formation regulate several ammonia-sensitive permeases in the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 133:135-139.
22. Grenson M. 1983. Study of the positive control of the general amino-acid permease and other ammonia-sensitive uptake systems by the product of the NPR1 gene in the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 133:141-144.
23. Grenson M, Dubois E, Piotrowska M, Drillien R, Aigle M. 1974. Ammonia assimilation in Saccharomyces cerevisiae as mediated by the two glutamate dehydrogenases. Evidence for the gdhA locus being a structural gene for the NADP-dependent glutamate dehydrogenase. Mol. Gen. Genet. 128:73- 85.
24. Han JM, et al. 2012. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 149:410-424.
25. Hatakeyama R, Kamiya M, Takahara T, Maeda T. 2010. Endocytosis of the aspartic acid/glutamic acid transporter Dip5 is triggered by substratedependent recruitment of the Rsp5 ubiquitin ligase via the arrestin-like protein Aly2. Mol. Cell. Biol. 30:5598 -5607.
26. Hein C, Springael J-Y, Volland C, Haguenauer-Tsapis R, André B. 1995. NPI1, an essential gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:77- 87.
27. Helliwell SB, Losko S, Kaiser CA. 2001. Components of a ubiquitin ligase complex specify polyubiquitylation and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153:649-662.
28. Herrador A, Herranz S, Lara D, Vincent O. 2010. Recruitment of the ESCRT machinery to a putative seven-transmembrane-domain receptor is mediated by an arrestin-related protein. Mol. Cell. Biol. 30:897-907.
29. Hicke L, Riezman H. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277-287.
30. Huibregtse JM, Scheffner M, Beaudenon SL, Howley PM. 1995. A family of proteins structurally and functionally related to the E6-AP ubiquitinprotein ligase. Proc. Natl. Acad. Sci. U. S. A. 92:2563-2567.
31. Huibregtse JM, Yang JC, Beaudenon SL. 1997. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. U. S. A. 94:3656-3661.
32. Jacinto E, Guo B, Arndt KT, Schmelzle T, Hall MN. 2001. TIP41 interacts with TAP42 and negatively regulates the TOR signaling pathway. Mol. Cell 8:1017-1026.
33. Jacobs P, Jauniaux JC, Grenson M. 1980. A cis-dominant regulatory mutation linked to the argB-argC gene cluster in Saccharomyces cerevisiae. J. Mol. Biol. 139:691-704.
34. Jauniaux JC, Grenson M. 1990. GAP1, the general amino acid permease gene of Saccharomyces cerevisiae. Nucleotide sequence, protein similarity with the other bakers yeast amino acid permeases, and nitrogen catabolite repression. Eur. J. Biochem. 190:39-44.
35. Kakiuchi K, et al. 2007. Proteomic analysis of in vivo 14-3-3 interactions in the yeast Saccharomyces cerevisiae. Biochemistry 46:7781-7792.
36. Katzmann DJ, Babst M, Emr SD. 2001. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145-155.
37. Kee Y, Munoz W, Lyon N, Huibregtse JM. 2006. The deubiquitinating enzyme Ubp2 modulates Rsp5-dependent Lys63-linked polyubiquitin conjugates in Saccharomyces cerevisiae. J. Biol. Chem. 281:36724 -36731.
38. Kolling R, Hollenberg CP. 1994. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13:3261-3271.
39. Lauwers E, Erpapazoglou Z, Haguenauer-Tsapis R, André B. 2010. The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20:196- 204.
40. Lauwers E, Jacob C, André B. 2009. K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J. Cell Biol. 185:493-502.
41. Lauwers E, Grossmann G, André B. 2007. Evidence for coupled biogenesis of yeast Gap1 permease and sphingolipids: essential role in transport activity and normal control by ubiquitination. Mol. Biol. Cell 18:3068- 3080.
42. Lefkowitz RJ, Shenoy SK. 2005. Transduction of receptor signals by beta-arrestins. Science 308:512-517.
43. Léon S, Haguenauer-Tsapis R. 2009. Ubiquitin ligase adaptors: regulators of ubiquitylation and endocytosis of plasma membrane proteins. Exp. Cell Res. 315:1574 -1583.
44. 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.
45. Loewith R, Hall MN. 2011. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189:1177-1201.
46. 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.
47. Magasanik B, Kaiser CA. 2002. Nitrogen regulation in Saccharomyces cerevisiae. Gene 290:1-18.
48. Marini AM, Soussi-Boudekou S, Vissers S, André B. 1997. A family of ammonium transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 17: 4282-4293.
49. Marini AM, Vissers S, Urrestarazu A, André B. 1994. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J. 13:3456-3463.
50. Martin Y, Gonzalez YV, Cabrera E, Rodriguez C, Siverio JM. 2011. Npr1 Ser/Thr protein kinase links nitrogen source quality and carbon availability with the yeast nitrate transporter (Ynt1) levels. J. Biol. Chem. 286:27225-27235.
51. Mayordomo I, Regelmann J, Horak J, Sanz P. 2003. Saccharomyces cerevisiae 14-3-3 proteins Bmh1 and Bmh2 participate in the process of catabolite inactivation of maltose permease. FEBS Lett. 544:160 -164.
52. Messenguy F, Colin D, Ten Have JP. 1980. Regulation of compartmentation of amino acid pools in Saccharomyces cerevisiae and its effects on metabolic control. Eur. J. Biochem. 108:439-447.
53. Miller SM, Magasanik B. 1990. Role of NAD-linked glutamate dehydrogenase in nitrogen metabolism in Saccharomyces cerevisiae. J. Bacteriol. 172:4927- 4935.
54. Navarro FJ, Martin Y, Siverio JM. 2008. Phosphorylation of the yeast nitrate transporter Ynt1 is essential for delivery to the plasma membrane during nitrogen limitation. J. Biol. Chem. 283:31208 -31217.
55. Nikko E, Marini AM, André B. 2003. Permease recycling and ubiquitination status reveal a particular role for Bro1 in the multivesicular body pathway. J. Biol. Chem. 278:411- 430.
56. Nikko E, Pelham HR. 2009. Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10:1856 -1867.
57. Nikko E, Sullivan JA, Pelham HRB. 2008. Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep. 9:1216 -1221.
58. O'Donnell AF, Apffel A, Gardner RG, Cyert MS. 2010. Alpha-arrestins Aly1 and Aly2 regulate intracellular trafficking in response to nutrient signaling. Mol. Biol. Cell 21:3552-3566.
59. Paiva S, et al. 2009. Glucose-induced ubiquitylation and endocytosis of the yeast JEN1 transporter: role of K63-linked ubiquitin chains. J. Biol. Chem. 284:19228 -19236.
60. Reggiori F, Pelham HR. 2001. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J. 20: 5176. doi:10.1093/emboj/20.18.5176.
61. Roberts RL, Mosch HU, Fink GR. 1997. 14-3-3 proteins are essential for RAS/MAPK cascade signaling during pseudohyphal development in S. cerevisiae. Cell 89:1055-1065.
62. Rotin D, Kumar S. 2009. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10:398-409.
63. 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.
64. Soetens O, De Craene JO, André B. 2001. Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem. 276:43949-43957.
65. Springael JY, André B. 1998. Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9:1253-1263.
66. Springael JY, Galan JM, Haguenauer-Tsapis R, André B. 1999. NH4+-induced down-regulation of the Saccharomyces cerevisiae Gap1p permease involves its ubiquitination with lysine-63-linked chains. J. Cell Sci. 112:1375-1383.
67. Stringer DK, Piper RC. 2011. A single ubiquitin is sufficient for cargo protein entry into MVBs in the absence of ESCRT ubiquitination. J. Cell Biol. 192:229 -242.
68. Urbanowski JL, Piper RC. 2001. Ubiquitin sorts proteins into the intralumenal degradative compartment of the late-endosome/vacuole. Traffic 2:622. doi:10.1034/j.1600-0854.2001.20905.x.
69. Vandenbol M, Jauniaux JC, Grenson M. 1990. The Saccharomyces cerevisiae NPR1 gene required for the activity of ammonia-sensitive amino acid permeases encodes a protein kinase homologue. Mol. Gen. Genet. 222:393-399.
70. Wiame JM, Grenson M, Arst HN, Jr. 1985. Nitrogen catabolite repression in yeasts and filamentous fungi. Adv. Microb. Physiol. 26:1- 88.
71. Yashiroda H, Kaida D, Toh-e A, Kikuchi Y. 1998. The PY-motif of Bul1 protein is essential for growth of Saccharomyces cerevisiae under various stress conditions. Gene 225:39-46.
72. Ziv I, et al. 2011. A perturbed ubiquitin landscape distinguishes between ubiquitin in trafficking and in proteolysis. Mol. Cell. Proteomics 10: M111.009753. doi:10.1074/mcp.M111.009753.