Distinct retrieval and retention mechanisms are required for the quality control of endoplasmic reticulum protein folding

Journal of Cell Biology

Volumn 155, Issue 3, 2001, Pages 355-367

  Vashist, Shilpa ^a   Kim, Woong ^a   Belden, William J ^b   Spear, Eric D ^a   Barlowe, Charles ^b   Ng, Davis T W ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Endoplasmic reticulum; Glycosylation; Misfolded proteins; Protein degradation; Vesicular transport

Indexed keywords

EID: 0035851911     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.200106123     Document Type: Article

References (74)

1. Barlowe, C., and R. Schekman. 1993. SEC12 encodes a guanine-nucleotide exchange factor essential for transport vesicle budding from the ER. Nature. 365:347-349.
2. Barlowe, C., L. Orci, T. Yeung, M. Hosobuchi, S. Hamamoto, N. Salama, M.F. Rexach, M. Ravazzola, M. Amherdt, and R. Schekman. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell. 77:895-907.
3. Bays, N.W., R.G. Gardner, L.P. Seelig, C.A. Joazeiro, and R.Y. Hampton. 2001. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER associated degradation. Nat. Cell Biol. 3:24-29.
4. Belden, W.J., and C. Barlowe. 1996. Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport. J. Biol. Chem. 271:26939-26946.
5. 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.
6. Biederer, T., C. Volkwein, and T. Sommer. 1997. Role of Cue1p in ubiquitination and degradation at the ER surface. Science. 278:1806-1809.
7. Bordallo, J., R.K. Plemper, A. Finger, and D.H. Wolf. 1998. Der3p/Hrd1p is required for endoplasmic reticulum-associated degradation of misfolded lumenal and integral membrane proteins. Mol. Biol. Cell. 9:209-222.
8. Brodsky, J.L., and R. Schekman. 1993. A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome. J. Cell Biol. 123:1355-1363.
9. Brodsky, J.L., and A.A. McCracken. 1999. ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10:507-513.
10. Brodsky, J.L., E.D. Werner, M.E. Dubas, J.L. Goeckeler, K.B. Kruse, and A.A. McCracken. 1999. The requirement for molecular chaperones during endoplasmic reticulum-associated protein degradation demonstrates that protein export and import are mechanistically distinct. J. Biol. Chem. 274:3453-3460.
11. Caldwell, S.R., K.J. Hill, and A.A. Cooper. 2001. Degradation of ER quality control substrates require transport between the ER and Golgi. J. Biol. Chem. In press. 276:23296-23303.
12. Carrell, R.W., and B. Gooptu. 1998. Conformational changes and disease-serpins, prions and Alzheimer’s. Curr. Opin. Struct. Biol. 8:799-809.
13. Casagrande, R., P. Stern, M. Diehn, C. Shamu, M. Osario, M. Zuniga, P.O. Brown, and H. Ploegh. 2000. Degradation of proteins from the ER of S. cerevisiae requires an intact unfolded protein response pathway. Mol. Cell. 5:729-735.
14. Cowles, C.R., W.B. Snyder, C.G. Burd, and S.D. Emr. 1997. Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO J. 16:2769-2782.
15. Eakle, K.A., M. Bernstein, and S.D. Emr. 1988. Characterization of a component of the yeast secretion machinery: identification of the SEC18 gene product. Mol. Cell. Biol. 8:4098-4109.
16. Ellgaard, L., M. Molinari, and A. Helenius. 1999. Setting the standards: quality control in the secretory pathway. Science. 286:1882-1888.
17. Elrod-Erickson, M.J., and C.A. Kaiser. 1996. Genes that control the fidelity of endoplasmic reticulum to Golgi transport identified as suppressors of vesicle budding mutations. Mol. Biol. Cell. 7:1043-1058.
18. Finger, A., M. Knop, and D.H. Wolf. 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.
19. Friedlander, R., E. Jarosch, J. Urban, C. Volkwein, and T. Sommer. 2000. A regulatory link between ER-associated protein degradation and the unfolded protein response. Nat. Cell Biol. 2:379-384.
20. Gemmill, T.R., and R.B. Trimble. 1999. Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta. 1426:227-237.
21. Gentzsch, M., and W. Tanner. 1996. The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J. 15:5752-5759.
22. Gentzsch, M., T. Immervoll, and W. Tanner. 1995. Protein O-glycosylation in Saccharomyces cerevisiae: the protein O-mannosyltransferases Pmt1p and Pmt2p function as heterodimer. FEBS Lett. 377:128-130.
23. Gething, M.J., K. McCammon, and J. Sambrook. 1986. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell. 46:939-950.
24. Hammond, C., and A. Helenius. 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.
25. Hampton, R.Y., R.G. Gardner, and J. Rine. 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.
26. Harty, C., S. Strahl, and K. Romisch. 2001. O-mannosylation protects mutant alpha-factor precursor from endoplasmic reticulum-associated degradation. Mol. Biol. Cell. 12:1093-1101.
27. Hauri, H., C. Appenzeller, F. Kuhn, and O. Nufer. 2000. Lectins and traffic in the secretory pathway. FEBS Lett. 476:32-37.
28. Herscovics, A., and P. Orlean. 1993. Glycoprotein biosynthesis in yeast. FASEB J. 7:540-550.
29. Hiller, M.M., A. Finger, M. Schweiger, and D.H. Wolf. 1996. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science. 273:1725-1728.
30. Jakob, C.A., P. Burda, J. Roth, and M. Aebi. 1998. Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J. Cell Biol. 142:1223-1233.
31. Johnson, A.E., and M.A. van Waes. 1999. The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15:799-842.
32. Johnson, A.E., and N.G. Haigh. 2000. The ER translocon and retrotranslocation: is the shift into reverse manual or automatic. Cell. 102:709-712.
33. Kaiser, C. 2000. Thinking about p24 proteins and how transport vesicles select their cargo. Proc. Natl. Acad. Sci. USA. 97:3783-3785.
34. Katzmann, D.J., E.A. Epping, and W.S. Moye-Rowley. 1999. Mutational disruption of plasma membrane trafficking of Saccharomyces cerevisiae Yor1p, a homologue of mammalian multidrug resistance protein. Mol. Cell. Biol. 19: 2998-3009.
35. Kim, P.S., and P. Arvan. 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.
36. Knop, M., A. Finger, T. Braun, K. Hellmuth, and D.H. Wolf. 1996. Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J. 15:753-763.
37. Kopito, R.R., and D. Ron. 2000. Conformational disease. Nat. Cell Biol. 2: E207-E209.
38. Kozutsumi, Y., M. Segal, K. Normington, M.J. Gething, and J. Sambrook. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 332:462-464.
39. Kreis, T.E., and H.F. Lodish. 1986. Oligomerization is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell. 46:929-937.
40. Letourneur, F., E.C. Gaynor, S. Hennecke, C. Demolliere, R. Duden, S.D. Emr, H. Riezman, and P. Cosson. 1994. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell. 79:1199-1207.
41. Loayza, D., A. Tam, W.K. Schmidt, and S. Michaelis. 1998. Ste6p mutants defective in exit from the endoplasmic reticulum (ER) reveal aspects of an ER quality control pathway in Saccharomyces cerevisiae. Mol. Biol. Cell. 9:2767-2784.
42. Lussier, M., A.M. Sdicu, F. Bussereau, M. Jacquet, and H. Bussey. 1997. The Ktr1p, Ktr3p, and Kre2p/Mnt1p mannosyltransferases participate in the elaboration of yeast O- and N-linked carbohydrate chains. J. Biol. Chem. 272:15527-15531.
43. Machamer, C.E., R.W. Doms, D.G. Bole, A. Helenius, and J.K. Rose. 1990. Heavy chain binding protein recognizes incompletely disulfide-bonded forms of vesicular stomatitis virus G protein. J. Biol. Chem. 265:6879-6883.
44. McCracken, A.A., and J.L. Brodsky. 1996. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J. Cell Biol. 132:291-298.
45. Muniz, M., C. Nuoffer, H.P. Hauri, and H. Riezman. 2000. The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles. J. Cell Biol. 148:925-930.
46. Muniz, M., P. Morsomme, and H. Riezman. 2001. Protein sorting upon exit from the endoplasmic reticulum. Cell. 104:313-320.
47. Nakano, A., D. Brada, and R. Schekman. 1988. A membrane glycoprotein, Sec12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J. Cell Biol. 107:851-863.
48. Nehls, S., E.L. Snapp, N.B. Cole, K.J. Zaal, A.K. Kenworthy, T.H. Roberts, J. Ellenberg, J.F. Presley, E. Siggia, and J. Lippincott-Schwartz. 2000. Dynamics and retention of misfolded proteins in native ER membranes. Nat. Cell Biol. 2:288-295.
49. Ng, D.T.W., J.D. Brown, and P. Walter. 1996. Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134:269-278.
50. Ng, D.T.W., R.E. Randall, and R.A. Lamb. 1989. Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface. J. Cell Biol. 109: 3273-3289.
51. Ng, D.T.W., S.W. Hiebert, and R.A. Lamb. 1990. Different roles of individual N-linked oligosaccharide chains in folding, assembly, and transport of the simian virus 5 hemagglutinin-neuraminidase. Mol. Cell. Biol. 10:1989-2001.
52. Ng, D.T.W., E.D. Spear, and P. Walter. 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.
53. Nishikawa, S., A. Hirata, and A. Nakano. 1994. Inhibition of endoplasmic reticulum (ER)-to-Golgi transport induces relocalization of binding protein (BiP) within the ER to form the BiP bodies. Mol. Biol. Cell. 5:1129-1143.
54. Nishikawa, S., S.W. Fewell, Y. Kato, J.L. Brodsky, and T. Endo. 2001. Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J. Cell Biol. 153:1-10.
55. Nuoffer, C., P. Jeno, A. Conzelmann, and H. Riezman. 1991. Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiae GAS1 protein to the plasma membrane. Mol. Cell. Biol. 11:27-37.
56. Ogg, S.C., W.P. Barz, and P. Walter. 1998. A functional GTPase domain, but not its transmembrane domain, is required for function of the SRP receptor beta-subunit. J. Cell Biol. 142:341-354.
57. Parks, G.D., and R.A. Lamb. 1990. Folding and oligomerization properties of a soluble and secreted form of the paramyxovirus hemagglutinin-neuraminidase glycoprotein. Virology. 178:498-508.
58. Pilon, M., R. Schekman, and K. Romisch. 1997. Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J. 16:4540-4548.
59. Plemper, R.K., S. Bohmler, J. Bordallo, T. Sommer, and D.H. Wolf. 1997. Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature. 388:891-895.
60. Plemper, R.K., P.M. Deak, R.T. Otto, and D.H. Wolf. 1999. Re-entering the translocon from the lumenal side of the endoplasmic reticulum. Studies on mutated carboxypeptidase yscY species. FEBS Lett. 443:241-245.
61. Sambrook, J., E.M. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
62. Shimoni, Y., T. Kurihara, M. Ravazzola, M. Amherdt, L. Orci, and R. Schekman. 2000. Lst1p and Sec24p cooperate in sorting of the plasma membrane ATPase into COPII vesicles in Saccharomyces cerevisiae. J. Cell Biol. 151: 973-984.
63. 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.
64. Sommer, T., and S. Jentsch. 1993. A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature. 365:176-179.
65. Sommer, T., and D.H. Wolf. 1997. Endoplasmic reticulum degradation: reverse protein flow of no return. FASEB J. 11:1227-1233.
66. Spormann, D.O., J. Heim, and D.H. Wolf. 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.
67. Strahl-Bolsinger, S., M. Gentzsch, and W. Tanner. 1999. Protein O-mannosylation. Biochim Biophys Acta. 1426:297-307.
68. Travers, K.J., C.K. Patil, L. Wodicka, D.J. Lockhart, J.S. Weissman, and P. Walter. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 101:249-258.
69. Wang, Q., and A. Chang. 1999. Eps1, a novel PDI-related protein involved in ER quality control in yeast. EMBO J. 18:5972-5982.
70. Ward, C.L., S. Omura, and R.R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell. 83:121-127.
71. Werner, E.D., J.L. Brodsky, and A.A. McCracken. 1996. Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc. Natl. Acad. Sci. USA. 93:13797-13801.
72. Wiertz, E.J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T.R. Jones, T.A. Rapoport, and H.L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature. 384:432-438.
73. Wuestehube, L.J., and R.W. Schekman. 1992. Reconstitution of transport from endoplasmic reticulum to Golgi complex using endoplasmic reticulumenriched membrane fraction from yeast. Methods Enzymol. 219:124-136.
74. Zhou, M., and R. Schekman. 1999. The engagement of Sec61p in the ER dislocation process. Mol. Cell. 4:925-934.