Ste6p mutants defective in exit from the endoplasmic reticulum (ER) reveal aspects of an ER quality control pathway in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 9, Issue 10, 1998, Pages 2767-2784

  Loayza, Diego ^a,b   Tam, Amy ^a   Schmidt, Walter K ^a   Michaelis, Susan ^a  

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

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; UBIQUITIN;

ARTICLE; ENDOPLASMIC RETICULUM; FUNGUS MUTATION; IMMUNOFLUORESCENCE TEST; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; STRAIN DIFFERENCE; TRANSPORT KINETICS;

SACCHAROMYCES CEREVISIAE;

EID: 0031690373     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.10.2767     Document Type: Article

References (50)

1. Amara, J.F., Cheng, S.H., and Smith, A.E. (1992). Intracellular protein trafficking defects in human disease. Trends Cell Biol. 2, 145-149.
2. Berkower, C. (1995). Analysis of STE6, a Saccharomyces cerevisiae ATP Binding Cassette (ABC) Protein. Ph.D. Thesis. Baltimore, MD: Johns Hopkins University.
3. Berkower, C., Loayza, D., and Michaelis, S. (1994). Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae. Mol. Biol. Cell 5, 1185-1198.
4. Berkower, C., and Michaelis, S. (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.
5. Berkower, C., and Michaelis, S. (1996). ATP binding cassette proteins in yeast. In: Membrane Protein Transport, ed. S. Rothman, Greenwich, CT: JAI Press, 231-277.
6. Biederer, T., Volkwein, C., and Sommer, T. (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. Bogyo, M., McMaster, J.S., Gaczynska, M., Tortorella, D., Goldberg, A.L., and Ploegh, H. (1997). Covalent modification of the active site threonine of proteasomal B subunits and the Escherichia coli homolog HslIV by a new class of inhibitors. Proc. Natl. Acad. Sci. USA 94, 6629-6634.
8. Bonifacino, J.S., and Lippincott-Schwartz, J. (1991). Degradation of proteins within the endoplasmic reticulum. Curr. Opin. Cell Biol. 3, 592-600.
9. Brodsky, J.L., and McCracken, A.A. (1997). ER-associated and proteasome-mediated protein degradation: how two topologically restricted events came together. Trends Cell Biol. 7, 151-156.
10. Chen, P., Johnson, P., Sommer, T., Jentsch, S., and Hochstrasser, M. (1993). Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast Matα2 repressor. Cell 74, 357-369.
11. Doms, R.W., Keller, D.S., Helenius, A., and Balch, W.E. (1987). Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J. Cell Biol. 105, 1957-1969.
12. Elble, R. (1992). A simple and efficient procedure for transformation of yeasts. Biotechniques 13, 18-20.
13. Gaber, R.F., Copple, D.M., Kennedy, B.K., Vidal, M., and Mard, M. (1989). The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol. Cell. Biol. 9, 3447-3456.
14. Geller, D., Taglicht, D., Edgar, R., Tam, A., Pines, O., Michaelis, S., and Bibi, E. (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.
15. Graham, T.R., Scott, P.A., and Emr, S.D. (1993). Brefeldin A reversibly blocks early but not late protein transport steps in the yeast secretory pathway. EMBO J. 12, 869-877.
16. Hammond, C., and Helenius, A. (1995). Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7, 523-529.
17. Hampton, R.Y., Gardner, R.G., and Rine, J. (1996). Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol. Biol. Cell 7, 2029-2044.
18. Heinemeyer, W., Gruhler, A., Mohrle, V., Mahe, Y., and Wolf, D.H. (1993). PRE2, highly homologous to the human major histocompatibility 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., Kleinschmidt, J.A., Saidowsky, J., Escher, C., and Wolf, D.H. (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, 555-562.
20. Hiller, M.M., Finger, A., Schweiger, M., and Wolf, D.H. (1996). ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 273, 1725-1728.
21. Hochstrasser, M., Ellison, M.J., Chau, V., and Varshavsky, A. (1991). The short-lived MATα2 transcriptional regulator is ubiquitinated in vivo. Proc. Natl. Acad. Sci. USA 88, 4606-4610.
22. Hughes, E.A., Hammond, C., and Cresswell, P. (1997). Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. USA 94, 1896-1901.
23. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
24. Jensen, T.J., Loo, M.A., Pind, S., Williams, D.B., Goldberg, A.L., and Riordan, J.R. (1995). Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135.
25. Kaiser, C., Michaelis, S., and Mitchell, A. (1994). Methods in Yeast Genetics: A Cold Spring Harbor Course Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
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. Kölling, R., and Losko, S. (1997). The linker region of the ABC transporter Ste6 mediates ubiquitination and fast turnover of the protein. EMBO J. 16, 2251-2261.
28. Kopito, R.R. (1997). ER quality control: the cytoplasmic connection. Cell 88, 427-430.
29. Kuchler, K., Sterne, R.E., and Thorner, J. (1989). Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells. EMBO J. 8, 3973-3984.
30. Lee, D.H., and Goldberg, A.L. (1996). Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J. Biol. Chem. 271, 27280-27284.
31. Loayza, D., and Michaelis, S. (1998). Role for the ubiquitin-proteasome system in the vacuolar degradation of Ste6p, the a-factor transporter in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 779-789.
32. McCracken, A.A., and Brodsky, J.L. (1996). Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J. Cell Biol. 132, 291-298.
33. Michaelis, S., and Herskowitz, I. (1988). The a-factor pheromone of Saccharomyces cerevisiae is essential for mating. Mol. Cell. Biol. 8, 1309-1318.
34. Novick, P., Ferro, S., and Schekman, R. (1981). Order of events in the yeast secretory pathway. Cell 25, 461-9.
35. Paddon, C., Loayza, D., Vangelista, L., Solari, R., and Michaelis, S. (1996). Analysis of the localization of STE6/CFTR chimeras in a Saccharomyces cerevisiae model for the cystic fibrosis defect CFTRΔF508. Mol. Microbiol. 19, 1007-1017.
36. Papa, F.R., and Hochstrasser, M. (1993). The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366, 313-319.
37. Pilon, M., Schekman, R., and Romisch, K. (1997). Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J. 16, 4540-4548.
38. Pind, S., Riordan, J.R., and Williams, D.B. (1994). Participation of the endoplasmic reticulum chaperone calnexin (p88, IP90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269, 12784-12788.
39. Plemper, R.K., Bohmler, S., Bordallo, J., Sommer, T., and Wolf, D.H. (1997). Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature 388, 891-895.
40. Romano, J.D., Schmidt, W.K., and Michaelis, S. (1998). The CAAX methyltransferase Ste14p is localized to the ER. Mol. Biol. Cell 9, 2231-2247.
41. Sikorski, R.S., and Boeke, J.D. (1991). In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. In: Methods in Enzymology: Guide to Yeast Genetics and Molecular Biology, ed. C. Guthrie and G.R. Fink, San Diego CA: Academic Press, 302-318.
42. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
43. Sommer, T., and Jentsch, S. (1993). A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature 365, 176-179.
44. Taglicht, D., and Michaelis, S. (1998). A complete catalogue of Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. In: Methods in Enzymology. ABC Transporters: Biochemical, Cellular, and Molecular Aspects, ed. S.V. Ambudkar and M.M. Gottesman, New York: Academic Press.
45. Thomas, P.J., Bao-He, Q., and Pedersen, P. (1995). Defective protein folding as a basis of human disease. Trends Biochem. Sci. 20, 456-459.
46. Tsurumi, C., Shimizu, Y., Saeki, M., Kato, S., and Tanaka, K. (1996). cDNA cloning and functional analysis of the p97 subunit of the 26S proteasome, a polypeptide identical to the type-1 tumor-necrosisfactor-receptor-associated protein-2/55.11. Eur. J. Biochem. 239, 912-921.
47. Ward, C.L., Omura, S., and Kopito, R.R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
48. Werner, E.D., Brodsky, J.L., and McCracken, A.A. (1996). Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc. Natl. Acad. Sci. USA 93, 13797-13801.
49. Wiertz, E.J., Jones, T.R., Sun, L., Bogyo, M., Geuze, H.J., and Ploegh, H.L. (1996). The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779.
50. Wiertz, E.J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T.R., Rapoport, T.A., and Ploegh, H.L. (1996). Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.