Direct Sorting of the Yeast Uracil Permease to the Endosomal System Is Controlled by Uracil Binding and Rsp5p-dependent Ubiquitylation

Molecular Biology of the Cell

Volumn 15, Issue 2, 2004, Pages 883-895

  Blondel, Marie Odile ^a   Morvan, Joëlle ^a   Dupré, Sophie ^a   Urban Grimal, Danièle ^a   Haguenauer Tsapis, Rosine ^a   Volland, Christiane ^a  

^a INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL ENZYME; FUR4P PERMEASE; MEMBRANE PROTEIN; PERMEASE; RSP5P PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; URACIL; URIDINE;

ARTICLE; BINDING AFFINITY; CELL LEVEL; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME METABOLISM; ENZYME REGULATION; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UBIQUITINATION; YEAST;

CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; NUCLEOTIDE TRANSPORT PROTEINS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINS; URACIL;

EID: 0742288015     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-04-0202     Document Type: Article

References (58)

1. Amerik, A.Y., Nowak, J., Swaminathan, S., and Hochstrasser, M. (2000). The doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11, 3365-3380.
2. Arnason, T., and Ellison, M.J. (1994). Stress resistance in Saccharomyces cerevisiae is strongly correlated with assembly of a novel type of mulfiubiquitin chain. Mol. Cell. Biol. 14, 7876-7883.
3. Arvan, P., Zhao, X., Ramos-Castaneda, J., and Chang, A. (2002). Secretory pathway quality control operating in Golgi, plasmalemmal, and endosomal systems. Traffic 3, 771-80.
4. Bagnat, M., Chang, A., and Simons, K. (2001). Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol. Biol. Cell 12, 4129-38.
5. Bagnat, M., Keranen, S., Shevchenko, A., and Simons, K. (2000). Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. USA 97, 3254-3259.
6. 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.
7. Benedetti, H., Raths, S., Crausaz, F., and Riezman, H. (1994). The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell 5, 1023-1037.
8. 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.
9. Donaldson, K.M., Yin, H., Gekakis, N., Supek, F., and Joazeiro, C.A. (2003). Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258-262.
10. Dupre, S., and Haguenauer-Tsapis, R. (2001). Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol. Cell. Biol. 21, 4482-4494.
11. Dupre, S., and Haguenauer-Tsapis, R. (2003). Raft partitioning of the yeast uracil permease during trafficking along the endocytic pathway. Traffic 4, 83-96.
12. Ellison, M. and Hochstrasser, M. (1991). Epitope-tagged ubiquitin. A new probe for analyzing ubiquitin function. J. Biol. Chem. 266, 21150-21157.
13. Galan, J.-M. and Haguenauer-Tsapis, R. (1997). Ubiquitin Lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16, 5847-5854.
14. Galan, J.M., Moreau, V., André, 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.
15. Gerrard, S.R., Levi, B.P., and Stevens, T.H. (2000). Pep12p is a multifunctional yeast syntaxin that controls entry of biosynthetic, endocytic and retrograde traffic into the prevacuolar compartment. Traffic 1, 259-69.
16. Gietz, D., St. Jean, A., Woods, R.A., and Schiestl, R.H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20, 1425
17. Gurunathan, S., David, D. and Gerst, J.E. (2002). Dynamin and clathrin are required for the biogenesis of a distinct class of secretory vesicles in yeast. EMBO J. 21.
18. Harsay, E., and Schekman, R. (2002). A subset of yeast vacuolar protein sorting mutants is blocked in one branch of the exocytic pathway. J. Cell Biol. 156, 271-285.
19. Hein, C., Springael, J.Y., Volland, C., Haguenauer-Tsapis, R., and André, B. (1995). NPI1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18, 77-87.
20. Helliwell, S.B., Losko, S., and Kaiser, C.A. (2001). Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153, 649-662.
21. Hicke, L. (2001). A new ticket for entry into budding vesicles-ubiquitin. Cell 106, 527-530.
22. Katzmarm, D.J., Babst, M., and Emr, S.D. (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.
23. Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.
24. Keleman, K., Rajagopalan, S., Cleppien, D., Teis, D., Paiha, K., Huber, L.A., Technau, G.M., and Dickson, B.J. (2002). Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110, 415-427.
25. Kim, Y., Yun, C.W., and Philpott, C.C. (2002). Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae. EMBO J. 21, 3632-3642.
26. Kölling, R., and Hollenberg, C.P. (1994). The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO. J. 13, 3261-3271.
27. Liu, X.F., and Culotta, V.C. (1999a). Mutational analysis of Saccharomyces cerevisiae Smf1p, a member of the Nramp family of metal transporters. J. Mol. Biol. 289, 885-891.
28. Liu, X.F., and Culotta, V.C. (1999b). Post-translation control of Nramp metal transport in yeast. Role of metal ions and the BSD2 gene. J. Biol. Chem. 274, 4863-4868.
29. Longtine, M.S., A., M. I., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
30. Losko, S., Kopp, F., Kranz, A., and Kolling, R. (2001). Uptake of the ATP-binding cassette (ABC) transporter Ste6 into the yeast vacuole is blocked in the doa4 Mutant. Mol. Biol. Cell 12, 1047-1059.
31. Marchal, C., Dupre, S., and Urban-Grimal, D. (2002). Casein kinase I controls a late step in the endocytic trafficking of yeast uracil permease. J. Cell Sci. 115, 217-226.
32. Marchal, C., Haguenauer-Tsapis, R., and Urban-Grimal, D. (1998). A PEST-like sequence mediates phosphorylation and efficient ubiquitination of the yeast uracil permease. Mol. Cell Biol. 18, 314-321.
33. Marchal, C., Haguenauer-Tsapis, R., and Urban-Grimal, D. (2000). Casein kinase I-dependent phosphorylation within a PEST sequence and ubiquitination at nearby lysines, signal endocytosis of yeast uracil permease. J. Biol. Chem. 275, 23608-23614.
34. Murphey, R., and Godenschwege, T.A. (2002). New roles for ubiquitin in the assembly and function of neuronal circuits. Neuron 36, 5-8.
35. Papa, F.R., Amerik, A.Y., and Hochstrasser, M. (1999). Interaction of the Doa4 deubiquitinating enzyme with the yeast 26S proteasome. Mol. Biol. Cell 10, 741-756.
36. Piper, R.C., and Luzio, J.P. (2001). Late endosomes: sorting and partitioning in multivesicular bodies. Traffic 2, 612-621.
37. Portnoy, M.E., Liu, X.F., and Culotta, V.C. (2000). Saccharomyces cerevisiae expresses three functionally distinct homologues of the nramp family of metal transporters. Mol. Cell Biol. 20, 7893-7902.
38. Reggiori, F., and Pelham, H.R.B. (2001). Sorting of proteins into mutivesicular bodies: ubiquitin dependent and independent targeting. EMBO J. 20, 5176-5186.
39. Reggiori, F., and Pelham, H.R.B. (2002). A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat. Cell Biol. 4, 117-123.
40. Roberg, K.J., Rowley, N., and Kaiser, C.A. (1997). Physiological regulation of membrane sorting late in the secretory pathway of Saccharomyces cerevisiae. J. Cell Biol. 137, 1469-1482.
41. Roth, A.F., and Davis, N.G. (2000). Ubiquitination of the PEST-like endocytosis signal of the yeast a-factor receptor. J. Biol. Chem. 275, 8143-8153.
42. Rotin, D., Staub, O., and Haguenauer-Tsapis, R. (2000). Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176, 1-17.
43. Séron, K., Blondel, M.-O., Haguenauer-Tsapis, R., and Volland, C. (1999). Uracil-induced down regulation of the yeast uracil permease. J. Bacteriol. 181, 1793-1800.
44. 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.
45. 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.
46. Springael, J.Y., and Andre, B. (1998). Nitrogen-regulated ubiquitination of the Gapl permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1253-1263.
47. Swaminathan, S., Amerik, A.Y., and Hochstrasser, M. (1999). The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol. Biol. Cell 10, 2583-2594.
48. Terrell, J., Shih, S., Dunn, R., and Hicke, L. (1998). A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1, 193-202.
49. Umebayashi, K., and Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J. Cell Biol. 161, 1117-31.
50. Urban-Grimal, D., Pinson, B., Chevallier, J., and Haguenauer-Tsapis, R. (1995). Replacement of Lys by Glu in a transmembrane segment strongly impairs the function of the uracil permease from Saccharomyces cerevisiae. Biochem. J. 308, 847-851.
51. Urbanowski, J., and Piper, R.C. (2001). Ubiquitin sorts proteins into the lumenal degradative compartment of the late endosome/vacuole. Traffic 2, 622-30.
52. Vancura, A., Sessler, A., Leichus, B., and Kuret, J. (1994). A prenylation motif is required for plasma membrane localization and biochemical function of casein kinase 1 in budding yeast. J. Biol. Chem. 269, 19271-19278.
53. Volland, C., Garnier, C. and Haguenauer-Tsapis, R. (1992). In vivo phosphorylation of the yeast uracil permease. J. Biol. Chem. 267, 23767-23771.
54. 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.
55. Wach, A. (1996). PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12, 259-265.
56. Wagner, R., de Montigny, J., de Wergifosse, P., Souciet, J.L., and Potier, S. (1998). The ORF YBL042 of Saccharomyces cerevisiae encodes a uridine permease. FEMS Microbiol. Lett. 159, 69-75.
57. Wang, G., McCaffery, J.M., Wendland, B., Dupre, S., Haguenauer-Tsapis, R., and Huibregtse, J.M. (2001). Localization of the Rsp5p ubiquitin-protein ligase at multiple sites within the endocytic pathway. Mol. Cell Biol. 21, 3564-3575.
58. Yashiroda, H., Oguchi, T., Yasuda, Y., Toh-e, A. and Kikuchi, Y. (1996). Bul1, a new protein that bind to the Rsp5 Ubiquitin ligase. Mol. Cell Biol. 16, 3255-3263.