Stress conditions promote yeast Gap1 permease ubiquitylation and down-regulation via the arrestin-like bul and aly proteins

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 22103-22116

  Crapeau, Myriam ^a   Merhi, Ahmad ^a   André, Bruno ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; PROTEINS;

DIFFERENT MECHANISMS; DOWN-REGULATION; MEMBRANE TRANSPORT PROTEINS; STRESS CONDITION; UBIQUITYLATION;

YEAST;

ALY1 PROTEIN, S CEREVISIAE; ALY2 PROTEIN, S CEREVISIAE; AMINO ACID; AMINO ACID TRANSPORTER; BUL1 PROTEIN, S CEREVISIAE; BUL2 PROTEIN, S CEREVISIAE; GAP1 PROTEIN, S CEREVISIAE; LYSINE; PROTEIN 14 3 3; RAPAMYCIN; RETINA S ANTIGEN; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TORC1 PROTEIN COMPLEX, S CEREVISIAE; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE;

ANTAGONISTS AND INHIBITORS; BINDING SITE; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DOWN REGULATION; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; SACCHAROMYCES CEREVISIAE; UBIQUITINATION;

14-3-3 PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS; ARRESTINS; BINDING SITES; DOWN-REGULATION; LYSINE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIROLIMUS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84905852280     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.582320     Document Type: Article

References (49)

1. Brohée, S., Barriot, R., Moreau, Y., and André, B. (2010) YTPdb: a wiki database of yeast membrane transporters. Biochim. Biophys. Acta 1798, 1908-1912
2. Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R., and André, B. (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20, 196-204
3. Dupré, S., Urban-Grimal, D., and Haguenauer-Tsapis, R. (2004) Ubiquitin and endocytic internalization in yeast and animal cells. Biochim. Biophys. Acta 1695, 89-111
4. Hein, C., Springael, J. Y., Volland, C., Haguenauer-Tsapis, R., and André, B. (1995) NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18, 77-87
5. Huibregtse, J. M., Scheffner, M., Beaudenon, S., and Howley, P. M. (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. U.S.A. 92, 2563-2567
6. Rotin, D., and Kumar, S. (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10, 398-409
7. Galan, J. M., and Haguenauer-Tsapis, R. (1997) Ubiquitin Lys63 is involved in ubiquitination of a yeast plasma membrane protein.EMBOJ. 16, 5847-5854
8. Springael, J. Y., Galan, J. M., Haguenauer-Tsapis, R., and 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
9. Kim, H. C., and Huibregtse, J. M. (2009) Polyubiquitination by HECT E3s and the determinants of chain type specificity. Mol. Cell. Biol. 29, 3307-3318
10. Lauwers, E., Jacob, C., and 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
11. Erpapazoglou, Z., Froissard, M., Nondier, I., Lesuisse, E., Haguenauer-Tsapis, R., and Belgareh-Touzé, N. (2008) Substrate-and ubiquitin-dependent trafficking of the yeast siderophore transporter Sit1. Traffic 9, 1372-1391
12. Becuwe, M., Herrador, A., Haguenauer-Tsapis, R., Vincent, O., and Léon, S. (2012) Ubiquitin-mediated regulation of endocytosis by proteins of the arrestin family. Biochem. Res. Int. 2012, 242764
13. Lin, C. H., MacGurn, J. A., Chu, T., Stefan, C. J., and Emr, S. D. (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135, 714-725
14. Nikko, E., Sullivan, J. A., and Pelham, H. R. (2008) Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep. 9, 1216-1221
15. Nikko, E., and Pelham, H. R. (2009) Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10, 1856-1867
16. Becuwe, M., Vieira, N., Lara, D., Gomes-Rezende, J., Soares-Cunha, C., Casal, M., Haguenauer-Tsapis, R., Vincent, O., Paiva, S., and Léon, S. (2012) A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 196, 247-259
17. MacGurn, J. A., Hsu, P.-C., Smolka, M. B., and Emr, S. D. (2011) TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147, 1104-1117
18. Grenson, M., Hou, C., and Crabeel, M. (1970) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. IV. Evidence for a general amino acid permease. J. Bacteriol. 103, 770-777
19. De Craene, J. O., Soetens, O., and Andre, B. (2001) The Npr1 kinase controls biosynthetic and endocytic sorting of the yeast Gap1 permease. J. Biol. Chem. 276, 43939-43948
20. Soetens, O., De Craene, J. O., and Andre, B. (2001) Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem. 276, 43949-43957
21. Merhi, A., and André, B. (2012) Internal amino acids promote Gap1 permease ubiquitylation via TORC1/Npr1/14-3-3-dependent control of the Bul arrestin-like adaptors. Mol. Cell. Biol. 32, 4510-4522
22. Grenson, M., Mousset, M., Wiame, J. M., and Bechet, J. (1966) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. I. Evidence for a specific arginine-transporting system. Biochim. Biophys. Acta 127, 325-338
23. Jacobs, P., Jauniaux, J. C., and Grenson, M. (1980) A cis-dominant regulatory mutation linked to the argB-argC gene cluster in Saccharomyces cerevisiae. J. Mol. Biol. 139, 691-704
24. Merhi, A., Gérard, N., Lauwers, E., Prévost, M., and André, B. (2011) Systematic mutational analysis of the intracellular regions of yeast Gap1 permease. PLoS ONE 6, e18457
25. Nikko, E., Marini, A. M., and André, B. (2003) Permease recycling and ubiquitination status reveal a particular role for Bro1 in the multivesicular body pathway. J. Biol. Chem. 278, 50732-50743
26. Springael, J. Y., and André, B. (1998) Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1253-1263
27. MacGurn, J. A., Hsu, P.-C., and Emr, S. D. (2012) Ubiquitin and membrane protein turnover: from cradle to grave. Annu. Rev. Biochem. 81, 231-259
28. O'Donnell, A. F., Apffel, A., Gardner, R. G., and Cyert, M. S. (2010)-Arrestins Aly1 and Aly2 regulate intracellular trafficking in response to nutrient signaling. Mol. Biol. Cell 21, 3552-3566
29. Kakiuchi, K., Yamauchi, Y., Taoka, M., Iwago, M., Fujita, T., Ito, T., Song, S.-Y., Sakai, A., Isobe, T., and Ichimura, T. (2007) Proteomic analysis of in vivo 14-3-3 interactions in the yeast Saccharomyces cerevisiae. Biochemistry 46, 7781-7792
30. Loewith, R., and Hall, M. N. (2011) Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189, 1177-1201
31. Urban, J., Soulard, A., Huber, A., Lippman, S., Mukhopadhyay, D., Deloche, O., Wanke, V., Anrather, D., Ammerer, G., Riezman, H., Broach, J. R., De Virgilio, C., Hall, M. N., and Loewith, R. (2007) Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26, 663-674
32. Binda, M., Péli-Gulli, M.-P., Bonfils, G., Panchaud, N., Urban, J., Sturgill, T. W., Loewith, R., and De Virgilio, C. (2009) The Vam6 GEF controls TORC1 by activating the EGO complex. Mol. Cell 35, 563-573
33. Hálová, L., Du, W., Kirkham, S., Smith, D. L., and Petersen, J. (2013) Phosphorylation of the TOR ATP binding domain by AGC kinase constitutes a novel mode of TOR inhibition. J. Cell Biol. 203, 595-604
34. Reinke, A., Anderson, S., McCaffery, J. M., Yates, J., 3rd, Aronova, S., Chu, S., Fairclough, S., Iverson, C., Wedaman, K. P., and Powers, T. (2004) TOR complex 1 includes a novel component, Tco89p (YPL180w), and cooperates with Ssd1p to maintain cellular integrity in Saccharomyces cerevisiae. J. Biol. Chem. 279, 14752-14762
35. Holst, B., Lunde, C., Lages, F., Oliveira, R., Lucas, C., and Kielland-Brandt, M. C. (2000) GUP1 and its close homologue GUP2, encoding multimembrane-spanning proteins involved in active glycerol uptake in Saccharomyces cerevisiae. Mol. Microbiol. 37, 108-124
36. Galan, J. M., Moreau, V., Andre, B., Volland, C., and 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
37. Jones, C. B., Ott, E. M., Keener, J. M., Curtiss, M., Sandrin, V., and Babst, M. (2012) Regulation of membrane protein degradation by starvationresponse pathways. Traffic 13, 468-482
38. Snowdon, C., and van der Merwe, G. (2012) 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 7, e50458
39. Zhao, Y., Macgurn, J. A., Liu, M., and Emr, S. (2013) The ART-Rsp5 ubiquitin ligase network comprises a plasma membrane quality control system that protects yeast cells from proteotoxic stress. Elife 2, e00459
40. Beck, T., Schmidt, A., and Hall, M. N. (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146, 1227-1238
41. Volland, C., Urban-Grimal, D., Géraud, G., and Haguenauer-Tsapis, R. (1994) Endocytosis and degradation of the yeast uracil permease under adverse conditions. J. Biol. Chem. 269, 9833-9841
42. Krampe, S., and 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
43. Abe, F., and Iida, H. (2003) Pressure-induced differential regulation of the two tryptophan permeases Tat1 and Tat2 by ubiquitin ligase Rsp5 and its binding proteins, Bul1 and Bul2. Mol. Cell. Biol. 23, 7566-7584
44. Babst, M. (2014) Quality control: Quality control at the plasma membrane: One mechanism does not fit all. J. Cell Biol. 205, 11-20
45. Lauwers, E., Grossmann, G., and 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
46. Bonneaud, N., Ozier-Kalogeropoulos, O., Li, G. Y., Labouesse, M., Minvielle-Sebastia, L., and Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 7, 609-615
47. Mayordomo, I., Regelmann, J., Horak, J., and 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
48. Ghaddar, K., Krammer, E.-M., Mihajlovic, N., Brohée, S., André, B., and Prévost, M. (2014) Converting the yeast arginine Can1 permease to a lysine permease. J. Biol. Chem. 289, 7232-7246
49. O'Donnell, A. F., Huang, L., Thorner, J., Cyert, M. S. (2013) A calcineurindependent switch controls the trafficking function of-arrestin Aly1/ Art6. J. Biol. Chem. 288, 24063-24080