Role for the ubiquitin-proteasome system in the vacuolar degradation of Ste6p, the a-factor transporter in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 18, Issue 2, 1998, Pages 779-789

  Loayza, Diego ^a   Michaelis, Susan ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; UBIQUITIN;

ARTICLE; CELL MEMBRANE TRANSPORT; ENZYME SUBSTRATE COMPLEX; INTRACELLULAR TRANSPORT; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

EID: 0031950846     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.2.779     Document Type: Article

References (57)

1. Amara, J. F., S. H. Cheng, and A. E. Smith. 1992. Intracellular protein trafficking defects in human disease. Trends Cell Biol. 2:145-149.
2. Berkower, C., D. Loayza, and S. Michaelis. 1994. Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae. Mol. Biol. Cell 5:1185-1198.
3. Berkower, C., and S. Michaelis. 1991. Mutational analysis of the yeast a-factor transporter STE6, a member of the ATP binding cassette (ABC) protein superfamily. EMBO J. 10:3777-3785.
4. Berkower, C., and S. Michaelis. ATP binding cassette proteins in yeast. In S. Rothman (ed.), Membrane protein transport, in press. JAI Press, Greenwich, Conn.
5. Berkower, C., D. Taglicht, and S. Michaelis. 1996. Functional and physical interactions between partial molecules of STE6, a yeast ATP-binding-cassette transport protein. J. Biol. Chem. 271:22983-22989.
6. Biederer, T., C. Volkwein, and T. Sommer. 1996. Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway. EMBO J. 15:2069-2076.
7. Boeke, J. D., J. Trueheart, G. Natsoulis, and G. R. Fink. 1987. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 152:481-504.
8. Chiang, H. L., and R. Schekman. 1991. Regulated import and degradation of a cytosolic protein in the yeast vacuole. Nature 350:313-318.
9. Davis, N. G., J. L. Horecka, and G. F. Sprague, Jr. 1993. Cis- and transacting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122:53-65.
10. Decottignies, A., and A. Goffeau. 1997. Complete inventory of the yeast ABC proteins. Nat. Genet. 15:137-145.
11. Egner, R., and K. Kuchler. 1996. The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett. 378:177-181.
12. Egner, R., Y. Mahe, R. Pandjaitan, and K. Kuchler. 1995. Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:5879-5887.
13. Elble, R. 1992. A simple and efficient procedure for transformation of yeasts. BioTechniques 13:18-20.
14. Finley, D., and V. Chau. 1991. Ubiquitination. Annu. Rev. Cell Biol. 7:25-69.
15. Franzusoff, A., K. Redding, J. Crosby, R. S. Fuller, and R. Schekman. 1991. Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J. Cell Biol. 112:27-37.
16. Galan, J. M., V. Moreau, B. Andre, C. Volland, and R. Haguenauer-Tsapis. 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.
17. Geller, D., D. Taglicht, R. Edgar, A. Tam, O. Pines, S. Michaelis, and E. Bibi. 1996. Comparative topology studies in Saccharomyces cerevisiae and in Escherichia coli of the N-terminal half of the yeast ABC protein, Ste6. J. Biol. Chem. 271:13746-13753.
18. Heinemeyer, W., A. Gruhler, V. Mohrle, Y. Mahe, and D. H. Wolf. 1993. PRE2, highly homologous to the human major histocompatihility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chymotryptic activity and degradation of ubiquitinated proteins. J. Biol. Chem. 268:5115-5120.
19. Heinemeyer, W., J. A. Kleinschmidt, J. Saidowsky, C. Escher, and D. H. Wolf. 1991. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 10:555-582.
20. Hershko, A., and A. Ciechanover. 1992. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61:761-807.
21. Hicke, L., and H. Riezman. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277-287.
22. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
23. Hochstrasser, M. 1995. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7:215-223.
24. Hochstrasser, M. 1996. Protein degradation or regulation: Ub the judge. Cell 84:813-815.
25. Hochstrasser, M., M. J. Ellison, V. Chau, and A. Varshavsky. 1991. The short-lived MATα2 transcriptional regulator is ubiquitinated in vivo. Proc. Natl. Acad. Sci. USA 88:4606-4610.
26. Huang, P.-H., and H.-L. Chiang. 1997. Identification of novel vesicles in the cytosol to vacuole protein degradation pathway. J. Cell Biol. 136:803-810.
27. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
28. Jensen, T. J., M. A. Loo, S. Pind, D. B. Williams, A. L. Goldberg, and J. R. Riordan. 1995. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83:129-135.
29. Jentsch, S. 1992. Ubiquitin-dependent protein degradation: a cellular perspective. Trends Cell Biol. 2:98-103.
30. Jones, E. W. 1991. Three proteolytic systems in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 266:7963-7966. (Review.)
31. Kaiser, C., S. Michaelis, and A. Mitchell. 1994. Methods in yeast genetics. A Cold Spring Harbor course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
32. Kölling, R., and C. P. Hollenberg. 1994. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13:3261-3271.
33. Kölling, R., and S. Losko. 1997. The linker region of the ABC transporter Ste6 mediates ubiquitination and fast turnover of the protein. EMBO J. 16:2251-2261.
34. Kuchler, K., R. E. Sterne, and J. Thorner. 1989. Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells. EMBO J. 8:3973-3984.
35. Loayza, D., and S. Michaelis. Unpublished observation.
36. McGrath, J. P., and A. Varshavsky. 1989. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature 340:400-404.
37. Michaelis, S., and I. Herskowitz. 1988. The a-factor pheromone of Saccharomyces cerevisiae is essential for mating. Mol. Cell. Biol. 8:1309-1318.
38. 508. Mol. Microbiol. 19:1007-1017.
39. Paolini, R., and J.-P. Kinet. 1993. Cell surface control of the multiubiquitination and deubquitination of high-affinity immunoglobulin E receptors. EMBO J. 12:779-786.
40. Papa, F. R., and M. Hochstrasser. 1993. The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366:313-319.
41. Piper, R. C., A. A. Cooper, H. Yang, and T. H. Stevens. 1995. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell Biol. 131:603-617.
42. Prince, L. S., J. Workman, and R. B. Marchase. 1994. Rapid endocytosis of the cystic fibrosis transmembrane conductance regulator chloride channel. Proc. Natl. Acad. Sci. USA 91:5192-5196.
43. Raymond, C. K., I. Howald-Stevenson, C. A. Vater, and T. H. Stevens. 1992. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3:1389-1402.
44. Redding, K., C. Holcomb, and R. S. Fuller. 1991. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae. J. Cell Biol. 113:527.
45. Redding, K., M. Seeger, G. S. Payne, and R. S. Fuller. 1996. The effects of clathrin inactivation on localization of Kex2 protease are independent of the TGN localization signal in the cytosolic signal in hte cytosolic tail of Kex2p. Mol. Biol. Cell 7:1667-1677.
46. Riballo, E., M. Herweijer, D. H. Wolf, and R. Lagunas. 1995. Catabolite inactivation of the yeast maltose transporter occurs in the vacuole after internalization by endocytosis. J. Bacteriol. 177:5622-5627.
47. Richter-Ruoff, B., D. H. Wolf, and M. Hochstrasser. 1994. Degradation of the yeast MATα2 transcriptional regulator is mediated by the proteasome. FEBS Lett. 354:50-52.
48. Roth, A. F., and N. G. Davis. 1996. Ubiquitination of the yeast a-factor receptor. J. Cell Biol. 134:661-674.
49. Schmidt, W., and S. Michaelis. Unpublished data.
50. Schork, S. M., M. Thumm, and D. H. Wolf. 1995. Catabolite inactivation of fructose-1,6-bisphosphatase of Saccharomyces cerevisiae. J. Biol. Chem. 270: 26446-26450.
51. Seufert, W., and S. Jentsch. 1990. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 9:543-550.
52. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
53. Taglicht, D., and S. Michaelis. A complete catalog of Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. Methods Enzymol., in press.
54. Thomas, P. J., Q. Bao-He, and P. Pedersen. 1995. Defective protein folding as a basis of human disease. Trends Biochem. Sci. 20:456-459.
55. Ward, C. L., and R. R. Kopito. 1994. Intracellular turnover of cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269:25710-25718.
56. Ward, C. L., S. Omura, and R. R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83:121-127.
57. Wilcox, C. A., R. Redding, R. Wright, and R. S. Fuller. 1992. Mutation of a tyrosine localization signal in the cytosolic tail of yeast Kex2 protease disrupts Golgi retention and results in default transport to the vacuole. Mol. Biol. Cell 3:1353-1371.