Substrate-induced ubiquitylation and endocytosis of yeast amino acid permeases

Molecular and Cellular Biology

Volumn 34, Issue 24, 2014, Pages 4447-4463

  Ghaddar, Kassem ^a   Merhi, Ahmad ^a   Saliba, Elie ^a   Krammer, Eva Maria ^a   Prévost, Martine ^a   André, Bruno ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMINO ACID TRANSPORTER; ARGININE; CAN1 PROTEIN; FUNGAL ENZYME; GAP1 PROTEIN; LYSINE; NITROGEN; PERMEASE; RETINA S ANTIGEN; UNCLASSIFIED DRUG; CAN1 PROTEIN, S CEREVISIAE; ESCRT PROTEIN; GAP1 PROTEIN, S CEREVISIAE; RSP5 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN PROTEIN LIGASE;

AMINO ACID TRANSPORT; ARTICLE; BINDING SITE; CATALYSIS; CELL MEMBRANE; CELL SURFACE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DOWN REGULATION; ELECTROPHORETIC MOBILITY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENZYME CONFORMATION; ENZYME KINETICS; FLUORESCENCE MICROSCOPY; HYDROGEN BOND; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN DEPHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; UBIQUITINATION; WESTERN BLOTTING; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LYSOSOME; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

SACCHAROMYCES CEREVISIAE;

AMINO ACID TRANSPORT SYSTEMS; AMINO ACID TRANSPORT SYSTEMS, BASIC; AMINO ACIDS; BINDING SITES; BIOCATALYSIS; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE EXPRESSION REGULATION, FUNGAL; LYSOSOMES; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINATION;

EID: 84918767282     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00699-14     Document Type: Article

References (50)

1. Mukhopadhyay D, Riezman H. 2007. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201-205. http://dx.doi.org/10.1126/science.1127085.
2. Lauwers E, Erpapazoglou Z, Haguenauer-Tsapis R, André B. 2010. The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20:196-204. http://dx.doi.org/10.1016/j.tcb.2010.01.004.
3. Becuwe M, Herrador A, Haguenauer-Tsapis R, Vincent O, Léon S. 2012. Ubiquitin-mediated regulation of endocytosis by proteins of the arrestin family. Biochem. Res. Int. 2012:242764. http://dx.doi.org/10.1155/2012/242764.
4. MacGurn JA, Hsu P-C, Emr SD. 2012. Ubiquitin and membrane protein turnover: from cradle to grave. Annu. Rev. Biochem. 81:231-259. http://dx.doi.org/10.1146/annurev-biochem-060210-093619.
5. Alvaro CG, O'Donnell AF, Prosser DC, Augustine AA, Goldman A, Brodsky JL, Cyert MS, Wendland B, Thorner J. 2014. Specific α-arrestins negatively regulate Saccharomyces cerevisiae pheromone response by down-modulating the G-protein coupled receptor Ste2. Mol. Cell. Biol. 34:2660-2681. http://dx.doi.org/10.1128/MCB.00230-14.
6. 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. http://dx.doi.org/10.1093/emboj/17.23.6924.
7. Merhi A, 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. http://dx.doi.org/10.1128/MCB.00463-12.
8. Becuwe M, Vieira N, Lara D, Gomes-Rezende J, Soares-Cunha C, Casal M, Haguenauer-Tsapis R, Vincent O, Paiva S, Léon S. 2012. A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 196:247-259. http://dx.doi.org/10.1083/jcb.201109113.
9. MacGurn JA, Hsu P-C, Smolka MB, Emr SD. 2011. TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147:1104-1117. http://dx.doi.org/10.1016/j.cell.2011.09.054.
10. Zhao Y, MacGurn JA, Liu M, 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. http://dx.doi.org/10.7554/eLife.00459.
11. Babst M. 2014. Quality control: quality control at the plasma membrane: one mechanism does not fit all. J. Cell Biol. 205:11-20. http://dx.doi.org/10.1083/jcb.201310113.
12. 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. http://dx.doi.org/10.1091/mbc.E07-03-0196.
13. Crapeau M, Merhi A, André B. 2014. Stress conditions promote yeast Gap1 permease ubiquitylation and down-regulation via the arrestin-like Bul and Aly proteins. J. Biol. Chem. 289:22103-22116. http://dx.doi.org/10.1074/jbc.M114.582320.
14. Lai K, Bolognese CP, Swift S, McGraw P. 1995. Regulation of inositol transport in Saccharomyces cerevisiae involves inositol-induced changes in permease stability and endocytic degradation in the vacuole. J. Biol. Chem. 270:2525-2534. http://dx.doi.org/10.1074/jbc.270.6.2525.
15. Haguenauer-Tsapis R, André B. 2004. Membrane trafficking of yeast transporters: mechanisms and physiological control of downregulation, p 273-323. In Topics in current genetics, vol 9. Springer, Berlin, Germany.
16. 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. http://dx.doi.org/10.1016/S0014-5793(98)01583-X.
17. Nikko E, Pelham HRB. 2009. Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10:1856-1867. http://dx.doi.org/10.1111/j.1600-0854.2009.00990.x.
18. Stanbrough M, Magasanik B. 1995. Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae. J. Bacteriol. 177:94-102.
19. Rubio-Texeira M, Van Zeebroeck G, Thevelein JM. 2012. Peptides induce persistent signaling from endosomes by a nutrient transceptor. Nat. Chem. Biol. 8:400-408. http://dx.doi.org/10.1038/nchembio.910.
20. Opekarová M, Caspari T, Pinson B, Bréthes D, Tanner W. 1998. Post-translational fate of CAN1 permease of Saccharomyces cerevisiae. Yeast 14:215-224. http://dx.doi.org/10.1002/(SICI)1097-0061(199802)14:3<215::AID-YEA214>3.0.CO;2-3.
21. 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. http://dx.doi.org/10.1016/j.cell.2008.09.025.
22. 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. http://dx.doi.org/10.1128/MCB.00464-10.
23. Séron K, Blondel MO, Haguenauer-Tsapis R, Volland C. 1999. Uracilinduced down-regulation of the yeast uracil permease. J. Bacteriol. 181:1793-1800.
24. Gournas C, Amillis S, Vlanti A, Diallinas G. 2010. Transport-dependent endocytosis and turnover of a uric acid-xanthine permease. Mol. Microbiol. 75:246-260. http://dx.doi.org/10.1111/j.1365-2958.2009.06997.x.
25. Keener JM, Babst M. 2013. Quality control and substrate-dependent downregulation of the nutrient transporter Fur4. Traffic 14:412-427. http://dx.doi.org/10.1111/tra.12039.
26. Hein C, Springael JY, Volland C, Haguenauer-Tsapis R, 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. http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_18010077.x.
27. 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. http://dx.doi.org/10.1016/0022-2836(80)90055-8.
28. Grenson M, Mousset M, Wiame JM, Béchet 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.
29. Ghaddar K, Krammer E-M, Mihajlovic N, Brohée S, André B, Prévost M. 2014. Converting the yeast arginine Can1 permease to a lysine permease. J. Biol. Chem. 289:7232-7246. http://dx.doi.org/10.1074/jbc.M113.525915.
30. Merhi A, Gérard N, Lauwers E, Prévost M, André B. 2011. Systematic mutational analysis of the intracellular regions of yeast Gap1 permease. PLoS One 6:e18457. http://dx.doi.org/10.1371/journal.pone.0018457.
31. Iraqui I, Vissers S, Bernard F, De Craene JO, Boles E, Urrestarazu A, André B. 1999. Amino acid signaling in Saccharomyces cerevisiae: a permease-like sensor of external amino acids and F-Box protein Grr1p are required for transcriptional induction of the AGP1 gene, which encodes a broad-specificity amino acid permease. Mol. Cell. Biol. 19:989-1001.
32. Gao X, Lu F, Zhou L, Dang S, Sun L, Li X, Wang J, Shi Y. 2009. Structure and mechanism of an amino acid antiporter. Science 324:1565-1568. http://dx.doi.org/10.1126/science.1173654.
33. Fang Y, Jayaram H, Shane T, Kolmakova-Partensky L, Wu F, Williams C, Xiong Y, Miller C. 2009. Structure of a prokaryotic virtual proton pump at 3.2 A resolution. Nature 460:1040-1043. http://dx.doi.org/10.1038/nature08201.
34. Gao X, Zhou L, Jiao X, Lu F, Yan C, Zeng X, Wang J, Shi Y. 2010. Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 463:828-832. http://dx.doi.org/10.1038/nature08741.
35. Opekarová M, Caspari T, Tanner W. 1993. Unidirectional arginine transport in reconstituted plasma-membrane vesicles from yeast overexpressing CAN1. Eur. J. Biochem. 211:683-688. http://dx.doi.org/10.1111/j.1432-1033.1993.tb17596.x.
36. Kowalczyk L, Ratera M, Paladino A, Bartoccioni P, Errasti-Murugarren E, Valencia E, Portella G, Bial S, Zorzano A, Fita I, Orozco M, Carpena X, Vázquez-Ibar JL, Palacín M. 2011. Molecular basis of substrateinduced permeation by an amino acid antiporter. Proc. Natl. Acad. Sci. U. S. A. 108:3935-3940. http://dx.doi.org/10.1073/pnas.1018081108.
37. Springael JY, André B. 1998. Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9:1253-1263. http://dx.doi.org/10.1091/mbc.9.6.1253.
38. Donaton MCV, Holsbeeks I, Lagatie O, Van Zeebroeck G, Crauwels M, Winderickx J, Thevelein JM. 2003. The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase A targets in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 50:911-929. http://dx.doi.org/10.1046/j.1365-2958.2003.03732.x.
39. Kriel J, Haesendonckx S, Rubio-Texeira M, Van Zeebroeck G, Thevelein JM. 2011. From transporter to transceptor: signaling from transporters provokes re-evaluation of complex trafficking and regulatory controls: endocytic internalization and intracellular trafficking of nutrient transceptors may, at least in part, be governed by their signaling function. Bioessays 33:870-879. http://dx.doi.org/10.1002/bies.201100100.
40. Jeschke G. 2013. A comparative study of structures and structural transitions of secondary transporters with the LeuT fold. Eur. Biophys. J. 42:181-197. http://dx.doi.org/10.1007/s00249-012-0802-z.
41. Kniazeff J, Shi L, Loland CJ, Javitch JA, Weinstein H, Gether U. 2008. An intracellular interaction network regulates conformational transitions in the dopamine transporter. J. Biol. Chem. 283:17691-17701. http://dx.doi.org/10.1074/jbc.M800475200.
42. Krishnamurthy H, Gouaux E. 2012. X-ray structures of LeuT in substrate-free outward-open and apo inward-open states. Nature 481:469-474. http://dx.doi.org/10.1038/nature10737.
43. Ljungdahl PO. 2009. Amino-acid-induced signalling via the SPS-sensing pathway in yeast. Biochem. Soc. Trans. 37:242-247. http://dx.doi.org/10.1042/BST0370242.
44. Bernard F, André B. 2001. Genetic analysis of the signalling pathway activated by external amino acids in Saccharomyces cerevisiae. Mol. Microbiol. 41:489-502. http://dx.doi.org/10.1046/j.1365-2958.2001.02538.x.
45. Fischer W-N, Loo DDF, Koch W, Ludewig U, Boorer KJ, Tegeder M, Rentsch D, Wright EM, Frommer WB. 2002. Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J. 29:717-731. http://dx.doi.org/10.1046/j.1365-313X.2002.01248.x.
46. Hein C, André B. 1997. A C-terminal di-leucine motif and nearby sequences are required for NH4(+)-induced inactivation and degradation of the general amino acid permease, Gap1p, of Saccharomyces cerevisiae. Mol. Microbiol. 24:607-616. http://dx.doi.org/10.1046/j.1365-2958.1997.3771735.x.
47. Bonneaud N, Ozier-Kalogeropoulos O, Li GY, Labouesse M, Minvielle-Sebastia L, 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. http://dx.doi.org/10.1002/yea.320070609.
48. Mumberg D, Müller R, Funk M. 1994. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22:5767-5768. http://dx.doi.org/10.1093/nar/22.25.5767.
49. 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. 278:50732-50743. http://dx.doi.org/10.1074/jbc.M306953200.
50. Lauwers E, André B. 2006. Association of yeast transporters with detergent-resistant membranes correlates with their cell-surface location. Traffic 7:1045-1059. http://dx.doi.org/10.1111/j.1600-0854.2006.00445.x.