Stress tolerance of misfolded carboxypeptidase Y requires maintenance of protein trafficking and degradative pathways

Molecular Biology of the Cell

Volumn 14, Issue 7, 2003, Pages 2756-2767

  Spear, Eric D ^a   Ng, Davis T W ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE C;

ARTICLE; CELL DAMAGE; CELL DEATH; CELLULAR IMMUNITY; CYTOTOXICITY; ENDOPLASMIC RETICULUM; GENE TARGETING; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STRESS; UNFOLDED PROTEIN RESPONSE; YEAST CELL;

BIOLOGICAL TRANSPORT; CARBOXYPEPTIDASE C; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLYCOSYLATION; MUTATION; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; UP-REGULATION;

SACCHAROMYCETALES;

EID: 0037769904     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-11-0717     Document Type: Article

References (64)

1. Ammerer, G., Hunter, C.P., Rothman, J.H., Saari, G.C., Valls, L.A., and Stevens, T.H. (1986). PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol. Cell. Biol. 6, 2490-2499.
2. Bays, N.W., Gardner, R.G., Seelig, L.P., Joazeiro, C.A., and Hampton, R.Y. (2001). Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol 3, 24-29.
3. Bertolotti, A., Zhang, Y., Hendershot, L.M., Harding, H.P., and Ron, D. (2000). Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol 2, 326-332.
4. Brodsky, J.L., and McCracken, A.A. (1999). ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10, 507-513.
5. Caldwell, S.R., Hill, K.J., and Cooper, A.A. (2001). Degradation of endoplasmic reticulum (ER) quality control substrates requires transport between the ER and Golgi. J. Biol. Chem. 276, 23296-23303.
6. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G., and Ron, D. (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
7. Carrell, R.W., and Gooptu, B. (1998). Conformational changes and disease - serpins, prions, and Alzheimer's. Curr. Opin. Struct. Biol. 8, 799-809.
8. Casagrande, R., Stern, P., Diehn, M., Shamu, C., Osario, M., Zuniga, M., Brown, P.O., and Ploegh, H. (2000). Degradation of proteins from the ER of S. cerevisiae requires an intact unfolded protein response pathway. Mol. Cell 5, 729-735.
9. Cowles, C.R., Odorizzi, G., Payne, G.S., and Emr, S.D. (1997). The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91, 109-118.
10. Cox, J.S., Shamu, C.E., and Walter, P. (1993). Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206.
11. Cox, J.S., and Walter, P. (1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87, 391-404.
12. Ellgaard, L., and Helenius, A. (2001). ER quality control: towards an understanding at the molecular level. Curr. Opin. Cell Biol. 13, 431-437.
13. Finger, A., Knop, M., and Wolf, D.H. (1993). Analysis of two mutated vacuolar proteins reveals a degradation pathway in the endoplasmic reticulum or a related compartment of yeast. Eur. J. Biochem. 218, 565-574.
14. Friedlander, R., Jarosch, E., Urban, J., Volkwein, C., and Sommer, T. (2000). A regulatory link between ER-associated protein degradation and the unfolded-protein response. Nat. Cell Biol 2, 379-384.
15. Gardner, R., Cronin, S., Leader, B., Rine, J., Hampton, R., and Leder, B. (1998). Sequence determinants for regulated degradation of yeast 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol. Biol. Cell 9, 2611-2626.
16. Guthrie, C., and Fink, G. R. (eds.) (1991). Guide to Yeast Genetics and Molecular Biology. San Diego: Academic Press, Inc.
17. Hammond, C., and Helenius, A. (1994). Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126, 41-52.
18. Harding, H.P., Zhang, Y., Bertolotti, A., Zeng, H., and Ron, D. (2000). Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5, 897-904.
19. Harding, H.P., Zhang, Y., and Ron, D. (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274.
20. Haynes, C.M., Caldwell, S., and Cooper, A.A. (2002). An HRD/DER-independent ER quality control mechanism involves Rsp5p-dependent ubiquitination and ER-Golgi transport. J. Cell Biol. 158, 91-101.
21. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and Mori, K. (1999). Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10, 3787-3799.
22. Herscovics, A., and Orlean, P. (1993). Glycoprotein biosynthesis in yeast. FASEB J. 7, 540-550.
23. 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.
24. Holkeri, H., and Makarow, M. (1998). Different degradation pathways for heterologous glycoproteins in yeast. FEBS Lett. 429, 162-166.
25. Hong, E., Davidson, A.R., and Kaiser, C.A. (1996). A pathway for targeting soluble misfolded proteins to the yeast vacuole. J. Cell Biol. 135, 623-633.
26. Kawahara, T., Yanagi, H., Yura, T., and Mori, K. (1997). Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Haclp/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 8, 1845-1862.
27. Kim, P.S., and Arvan, P. (1998). Endocrinopathies in the family of endoplasmic reticulum (ER) storage diseases: disorders of protein trafficking and the role of ER molecular chaperones. Endocr. Rev. 19, 173-202.
28. Klionsky, D.J., Banta, L.M., and Emr, S.D. (1988). Intracellular sorting and processing of a yeast vacuolar hydrolase: proteinase A propeptide contains vacuolar targeting information. Mol. Cell. Biol. 8, 2105-2116.
29. Knop, M., Finger, A., Braun, T., Hellmuth, K., and Wolf, D.H. (1996a). Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J..15, 753-763.
30. Knop, M., Hauser, N., and Wolf, D.H. (1996b). N-Glycosylation affects endoplasmic reticulum degradation of a mutated derivative of carboxypeptidase yscY in yeast. Yeast 12, 1229-1238.
31. Kopito, R.R., and Ron, D. (2000). Conformational disease. Nat. Cell Biol. 2, E207-E209.
32. Kopito, R.R., and Sitia, R. (2000). Aggresomes and Russell bodies. Symptoms of cellular indigestion? EMBO Rep. 1, 225-231.
33. Kushnirov, V.V. (2000). Rapid and reliable protein extraction from yeast. Yeast 16, 857-860.
34. Marcusson, E.G., Horazdovsky, B.F., Cereghino, J.L., Gharakhanian, E., and Emr, S.D. (1994). The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77, 579-586.
35. Mori, K., Ma, W., Gething, M.J., and Sambrook, J. (1993). A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756.
36. Ng, D.T., Spear, E.D., and Walter, P. (2000). The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J. Cell Biol. 150, 77-88.
37. Nierras, C.R., and Warner, J.R. (1999). Protein kinase C enables the regulatory circuit that connects membrane synthesis to ribosome synthesis in Saccharomyces cerevisiae. J. Biol. Chem. 274, 13235-13241.
38. Nuoffer, C., Jeno, P., Conzelmann, A., and Riezman, H. (1991). Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiae GAS1 protein to the plasma membrane. Mol. Cell. Biol. 11, 27-37.
39. Okamura, K., Kimata, Y., Higashio, H., Tsuru, A., and Kohno, K. (2000). Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun. 279, 445-450.
40. Patil, C., and Walter, P. (2001). Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13, 349-355.
41. 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.
42. 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.
43. Plemper, R.K., and Wolf, D.H. (1999). Retrograde protein translocation: ERADication of secretory proteins in health and disease. Trends Biochem. Sci. 24, 266-270.
44. Sambrook, J., Fritsch, E.M., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Plainview: Cold Spring Harbor Laboratory Press.
45. Schubert, U., Anton, L.C., Gibbs, J., Norbury, C.C., Yewdell, J.W., and Bennink, J.R. (2000). Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404, 770-774.
46. Shen, J., Chen, X., Hendershot, L., and Prywes, R. (2002). ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3, 99-111.
47. Shen, X. et al. (2001). Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107, 893-903.
48. Shi, Y., Vattem, K.M., Sood, R., An, J., Liang, J., Stramm, L., and Wek, R.C. (1998). Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18, 7499-7509.
49. 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.
50. Spear, E., and Ng, D.T. (2001). The unfolded protein response: no longer just a special teams player. Traffic 2, 515-523.
51. Spormann, D.O., Heim, J., and Wolf, D.H. (1992). Biogenesis of the yeast vacuole (lysosome). The precursor forms of the soluble hydrolase carboxypeptidase yscS are associated with the vacuolar membrane. J. Biol. Chem. 267, 8021-8029.
52. te Heesen, S., Janetzky, B., Lehle, L., and Aebi, M. (1992). The yeast WBP1 is essential for oligosaccharyltransferase activity in vivo and in vitro. EMBO J. 11, 2071-2075.
53. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., and Walter, P. (2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
54. Turner, G.C., and Varshavsky, A. (2000). Detecting and measuring cotranslational protein degradation in vivo. Science 289, 2117-2120.
55. Umebayashi, K., Fukuda, R., Hirata, A., Horiuchi, H., Nakano, A., Ohta, A., and Takagi, M. (2001). Activation of the Ras-cAMP signal transduction pathway inhibits the proteasome-independent degradation of misfolded protein aggregates in the endoplasmic reticulum lumen. J. Biol. Chem. 276, 41444-41454.
56. Umebayashi, K., Hirata, A., Horiuchi, H., Ohta, A., and Takagi, M. (1999). Unfolded protein response-induced BiP/Kar2p production protects cell growth against accumulation of misfolded protein aggregates in the yeast endoplasmic reticulum. Eur J. Cell Biol. 78, 726-738.
57. Vashist, S., Kim, W., Belden, W.J., Spear, E.D., Barlowe, C., and Ng, D.T. (2001). Distinct retrieval and retention mechanisms are required for the quality control of endoplasmic reticulum protein folding. J. Cell Biol. 155, 355-368.
58. Walter, P., and Johnson, A.E. (1994). Signal Sequence Recognition and Protein Targeting to the Endoplasmic Reticulum Membrane. Annu. Rev. Cell Biol. 10, 87-119.
59. Ward, C.L., Omura, S., and Kopito, R.R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
60. Yamamoto, K., Fujii, R., Toyofuku, Y., Saito, T., Koseki, H., Hsu, V.W., and Aoe, T. (2001). The KDEL receptor mediates a retrieval mechanism that contributes to quality control at the endoplasmic reticulum. EMBO J. 20, 3082-3091.
61. Ye, J., Rawson, R.B., Komuro, R., Chen, X., Dave, U.P., Prywes, R., Brown, M.S., and Goldstein, J.L. (2000). ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6, 1355-1364.
62. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. (2001). XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891.
63. Zhang, J.X., Braakman, I., Matlack, K.E., and Helenius, A. (1997). Quality control in the secretory pathway: the role of calreticulin, calnexin, and BiP in the retention of glycoproteins with C-terminal truncations. Mol. Biol. Cell 8, 1943-1954.
64. Zhou, M., and Schekman, R. (1999). The engagement of Sec61p in the ER dislocation process. Mol. Cell 4, 925-934.