Secretory pathway quality control operating in Golgi, plasmalemmal, and endosomal systems

Traffic

Volumn 3, Issue 11, 2002, Pages 771-780

  Arvan, Peter ^a   Zhao, Xiang ^a   Ramos Castaneda, Jose ^a   Chang, Amy ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Degradation; Multivesicular endosome; Proteasome; Ubiquitylation; Vps genes

Indexed keywords

MEMBRANE PROTEIN; MUTANT PROTEIN; POLYPEPTIDE; PROTEASOME; PROTEIN; PROTEIN SUBUNIT; PROTEINASE; UBIQUITIN; CARRIER PROTEIN;

CELL ACTIVITY; CELL COMPARTMENTALIZATION; CELL MEMBRANE TRANSPORT; CELL SECRETION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENDOSOME; GOLGI COMPLEX; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN TRANSPORT; QUALITY CONTROL; REVIEW; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ENDOSOMES; GOLGI APPARATUS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PROTEIN TRANSPORT;

EID: 0036843023     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0854.2002.31102.x     Document Type: Review

References (95)

1. Ellgaard L, Molinari M, Helenius A. Setting the standards: quality control in the secretory pathway. Science 1999;286:1882-1888.
2. Fewell SW, Travers KJ, Weissman JS, Brodsky JL. The action of molecular chaperones in the early secretory pathway. Annu Rev Genet 2001;35:149-191.
3. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 1999;10:3787-3799.
4. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JP. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 2000;6:1355-1364.
5. Chen X, Shen J, Prywes R. The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J Biol Chem 2002;277:13045-13052.
6. Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, Yoshida A, Morimoto R. Kurnit DM, Mori K, Kaufman RJ. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 2001:107:893-903.
7. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001;107:881-891.
8. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, Okada T, Yoshida H, Mori K, Kaufman RJ. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 2002;16:452-466.
9. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature (Lond) 2002; 415;92-96.
10. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000:2:326-332.
11. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000;6:1099-1108.
12. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. PERK is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000;5:897-904.
13. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000:101:249-268.
14. Belden WJ, Barlowe C. Role of Erv29p in collecting soluble secretory proteins into ER-derived transport vesicles. Science 2001;294:1528-1531.
15. Caldwell SR, Hill KJ, Cooper AA. Degradation of endoplasmic reticulum (ER) quality control substrates requires transport between the ER and Golgi. J Biol Chem 2001;276:23296-23303.
16. Vashist S, Kim W, Belden WJ, Spear ED, Barlowe C, Ng DT. Distinct retrieval and retention mechanisms are required for the quality control of endoplasmic reticulum protein folding. J Cell Biol 2001:155:355-368.
17. Haynes CM, Caldwell S, Cooper AA. An HRD/DER-independent ER quality control mechanism involves Rsp5p-dependent ubiquitination and ER-Golgi transport. J Cell Biol 2002;158:91-101.
18. Taxis C, Vogel F, Wolf DH. ER-Golgi traffic is a prerequisite for efficient ER degradation. Mol Biol Cell 2002;13:1806-1818.
19. Reggiori F, Black MW, Pelham HR. Polar transmembrane domains target proteins to the interior of the yeast vacuole. Mol Biol Cell 2000;11:3737-3749.
20. Sato K, Sato M, Nakano A. Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. J Cell Biol 2001;152:935-944.
21. Letourneur F, Cosson P. Targeting to the endoplasmic reticulum in yeast cells by determinants present in transmembrane domains. J Biol Chem 1998;273:33273-33278.
22. Hammond C, Helenius A. 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 1994;126:41-52.
23. Winitz D, Shachar I, Elkabetz Y, Amitay R, Samuelov M, Bar-Nun S. Degradation of distinct assembly forms of immunoglobulin M occurs in multiple sites in permeabilized B cells. J Biol Chem 1996;271: 27645-27651.
24. Park B, Lee S, Kim E, Chang S, Jin M, Ahn K. The truncated cytoplasmic tail of HLA-G serves a quality-control function in post-ER compartments. Immunity 2001;15:213-224.
25. Ito M, Amizuka N, Ozawa H, Oda K. Retention at the cis-Golgi and delayed degradation of tissue-non-specific alkaline phosphatase with an Asn 153 →Asp substitution, a cause of perinatal hypophosphatasia. Biochem J 2002;361:473-480.
26. Dusseljee S, Wubbolts R, Verwoerd D, Tulp A, Janssen H, Calafat J, Neefjes J. Removal and degradation of the free MHC class II beta chain in the endoplasmic reticulum requires proteasomes and is accelerated by BFA. J Cell Sci 1998;111:2217-2226.
27. Yamamoto K, Fujii R, Toyofuku Y, Saito T, Koseki H, Hsu VW, Aoe T. The KDEL receptor mediates a retrieval mechanism that contributes to quality control at the endoplasmic reticulum. EMBO J 2001;20: 3082-3091.
28. Chang A, Fink GR. Targeting of the yeast plasma membrane [H+]ATPase: a novel gene AST1 prevents mislocalization of mutant ATPase to the vacuole. J Cell Biol 1995;128:39-49.
29. Hong E, Davidson AR, Kaiser CA. A pathway for targeting soluble misfolded proteins to the yeast vacuole. J Cell Biol 1996:135:623-633.
30. Luo W, Chang A. Novel genes involved in endosomal traffic in yeast revealed by suppression of a targeting-defective plasma membrane ATPase mutant. J Cell Biol 1997;138:731-746.
31. Li Y, Kane T, Tipper C, Spatrick P, Jenness DD. Yeast mutants affecting possible quality control of plasma membrane proteins. Mol Cell Biol 1999;19:3588-3599.
32. Reggiori F, Pelham HR. A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat Cell Biol 2002:4:117-123.
33. Armstrong J, Patel S, Riddle P. Lysosomal sorting mutants of coronavirus E1 protein, a Golgi membrane protein. J Cell Sci 1990;95:191-197.
34. Bishop N, Horman A, Woodman P. Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol 2002:157:91-101.
35. Musil LS, Goodenough DA. Multisubunit assembly of an integral plasma membrane channel protein occurs after exit from the ER. Cell 1993;74:1065-1077.
36. Koval M, Harley JE, Hick E, Steinberg TH. Connexin46 is retained as monomers in a trans-Golgi compartment of osteoblastic cells. J Cell Biol 1997;137:847-857.
37. Minami Y, Weissman AM, Samelson LE, Klausner RD. Building a multichain receptor. synthesis, degradation and assembly of the T-cell antigen receptor. Proc Natl Acad Sci USA 1987:84:2688-2692.
38. Marcusson EG, Horazdovsky BF, Cereghino JL, Gharakhanian E, Emr SD. The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 1994;77:579-586.
39. Cooper AA, Stevens TH. Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J Cell Biol 1996:133:529-541.
40. Holkeri H, Makarow M. Different degradation pathways for heterologous glycoproteins in yeast. FEBS Lett 1998;429:162-166.
41. Jorgensen MU, Emr SD, Winther JR. Ligand recognition and domain structure of Vps10p, a vacuolar protein sorting receptor in Saccharomyces cerevisiae. Eur J Biochem 1999:260:461-469.
42. Zhang B-y, Chang A, Kjeldsen TB, Arvan P. Intracellular retention of newly-synthesized insulin in yeast is caused by endoproteolytic processing in the Golgi complex. J Cell Biol 2001;153:1187-1197.
43. Busca R, Martinez M, Vilella E, Pognonec P, Deeb S, Auwerx J, Reina M, Vilaro S. The mutation Gly 142 →Glu in human lipoprotein lipase produces a missorted protein that is diverted to lysosomes. J Biol Chem 1996;271:2139-2146.
44. Millar CA, Meerloo T, Martin S, Hickson GRX, Shimwell NJ, Wakelam MJO, James DE, Gould GW. Adipsin and the glucose transporter GLUT4 traffic to the cell surface via independent pathways in adipocytes. Traffic 2000;1:141-161.
45. Turner M, Arvan P. Protein traffic from the secretory pathway to the endosomal system in pancreatic β-cells. J Biol Chem 2000;275: 14025-14030.
46. Harsay E, Schekman R. A subset of yeast vacuolar protein sorting mutants is blocked in one branch of the exocytic pathway. J Cell Biol 2002;156:271-286.
47. Munro S. Localization of proteins to the Golgi apparatus. Trends Cell Biol 1998;8:11-15.
48. Pelham HRB. Traffic through the Golgi apparatus. J Cell Biol 2001;155:1099.
49. Verkade P, Simons K. Robert Feulgen Lecture 1997. Lipid micro-domains and membrane trafficking in mammalian cells. Histochem Cell Biol 1997;108:211-220.
50. Nichols BJ, Kenworthy AK, Polishchuk RS, Lodge R, Roberts TH. Hirschberg K, Phair RD, Lippincott-Schwartz J. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol 2001;153:529-541.
51. Sotgia F, Razani B, Bonuccelli G, Schubert W, Battista M, Lee H, Capozza F, Schubert AC, Minetti C, Buckley JT, Lisanti MP. Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol Cell Biol 2002;22:3905-3926.
52. Puertollano R, Martin-Belmonte F, Millan J, de Marco MC, Albar JP, Kremer L, Alonso MA. The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J Cell Biol 1999;145:141-151.
53. Martin-Belmonte F, Arvan P, Alonso MA. MAL mediates apical transport of secretory proteins in polarized epithelial Madin-Darby canine kidney cells. J Biol Chem 2001:276:49337-49342.
54. Gut A, Kappeler F, Hyka N, Balda MS, Hauri HP, Matter K. Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO J 1998;17:1919-1929.
55. Bagnat M, Keranen S, Shevchenko A, Shevchenko A, Simons K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 2000;97:3254-3259.
56. Bagnat M, Chang A, Simons K. Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol Biol Cell 2001;12:4129-4138.
57. Ono A, Kawakita M. Conformational aberrance of the sendai virus F0 protein in thapsigargin-treated cells allowing exit from the endoplasmic reticulum but causing arrest at the Golgi complex. J Biochem 1995;118:1248-1264.
58. Munro S. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J 1995;14:4695-4704.
59. Wolins N, Bosshart H, Kuster H, Bonifacino JS. Aggregation as a determinant of protein fate in post-Golgi compartments: role of the luminal domain of furin in lysosomal targeting. J Cell Biol 1997;139: 1735-1745.
60. Gilch S, Winklhofer KF, Groschup MH, Nunziante M, Lucassen R, Spielhaupter C, Muranyi W, Riesner D, Tatzelt J, Schatzl HM. Intracellular re-routing of prion protein prevents propagation of PrP (Sc) and delays onset of prion disease. EMBO J 2001;20:3957-3966.
61. Egner R, Kuchler K. The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett 1996;378:177-181.
62. Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved andosomal protein sorting complex, ESCRT-I. Cell 2001;106:145-155.
63. Shih SC, Katzmann DJ, Schnell JD, Sutanto M, Emr SD, Hicke L. Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat Cell Biol 2002;4:389-393.
64. Neumann D, Wikstrom L, Watowich SS, Lodish HF. Intermediates in degradation of the erythropoietin receptor accumulate and are degraded in lysosomes. J Biol Chem 1993;268:13639-13649.
65. Egner R, Mahe Y, Pandjaitan R, Kuchler K. Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol Cell Biol 1995;15:5879-5887.
66. Berkower C, Loayza D, Michaelis S. Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae. Mol Biol Cell 1994;5:1185-1198.
67. Buttner C, Sadtler S, Leyendecker A, Laube B, Griffon N, Betz H, Schmalzing G. Ubiquitination precedes internalization and proteolytic cleavage of plasma membrane-bound glycine receptors. J Biol Chem 2001;276:42978-42985.
68. Piper RC, Luzio JP. Late endosomes: sorting and partitioning in multi-vesicular bodies. Traffic 2001;2:612-221.
69. Dupre S, Volland C, Haguenauer-Tsapis R. Membrane transport: ubiquitylation in endosomal sorting. Curr Biol 2001;11:R932-R934.
70. Benharouga M, Haardt M, Kartner N, Lukacs GL. COOH-terminal truncations promote proteasome-dependent degradation of mature cystic fibrosis transmembrane conductance regulator from post-Golgi compartments. J Cell Biol 2001;153:957-970.
71. Zhou M, Schekman R. The engagement of Sec61p in the ER dislocation process. Mol Cell 1999;4:925-934.
72. +) ATPase and implications for the organization of membrane domains in polarized cells. Nature (Lond) 1987;328:533-536.
73. +-ATPase, ankyrin, and fodrin in Madin-Darby canine kidney (MDCK) cells: Implications for the biogenesis of epithelial cell polarity. J Cell Biol 1989;108:893-902.
74. Zhang Z, Devarajan P, Dorfman AL, Morrow JS. Structure of the ankyrin-binding domain of alpha-Na,K-ATPase. J Biol Chem 1998;273: 18681-18684.
75. Dubreuil RR, Wang P, Dahl S, Lee J, Goldstein LS. Drosophila beta spectrin functions independently of alpha spectrin to polarize the Na,K ATPase in epithelial cells. J Cell Biol 2000:149:647-656.
76. Nelson WJ, Veshnock PJ. Modulation of fodrin (membrane skeleton) stability by cell-cell contact in Madin-Darby canine kidney epithelial cells. J Cell Biol 1987;104:1527-1537.
77. +-ATPase and the membrane skeleton in adult rat intestine during fetal development and after epithelial isolation. J Cell Biol 1989;109:2129-2138.
78. Gut A, Balda MS, Matter K. The cytoplasmic domains of a beta1 integrin mediate polarization in Madin-Darby canine kidney cells by selective basolateral stabilization. J Biol Chem 1998;273:29381-29388.
79. + ATPase in polarized epithelial cells. Science 1991;254:847-850.
80. Mays RW, Siemers KA, Fritz BA, Lowe AW, van Meer G, Nelson WJ. Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells. J Cell Biol 1995;130:1105-1115.
81. Gong X, Chang A. A mutant plasma membrane ATPase, Pma1-10, is defective in stability at the yeast cell surface. Proc Natl Acad Sci USA 2001;98:9104-9109.
82. Wang Q, Chang A. Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1. Proc Natl Acad Sci USA 2002;in press.
83. Beck T, Schmidt A, Hall MN. Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J Cell Biol 1999;146:1227-1238.
84. Liu XF, Culotta VC. Mutational analysis of Saccharomyces cerevisiae Smf1p, a member of the Nramp family of metal transporters. J Mol Biol 1999;289:885-891.
85. Kim Y, Yun CW, Philpott CC. Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae. EMBO J 2002;21:3632-3642.
86. Galan JM, Volland C, Urban-Grimal D, Haguenauer-Tsapis R. The yeast plasma membrane uracil permease is stabilized against stress induced degradation by a point mutation in a cyclin-like 'destruction box'. Biochem Biophys Res Comm 1994;201:769-775.
87. Riballo E, Herweijer M, Wolf DH, Lagunas R. Catabolite inactivation of the yeast maltose transporter occurs in the vacuole after internalization by endocytosis. J Bacteriol 1995;177:5622-5627.
88. Medintz I, Wang X, Hradek T, Michels CA. A PEST-like sequence in the N-terminal cytoplasmic domain of Saccharomyces maltose permease is required for glucose-induced proteolysis and rapid inactivation of transport activity. Biochem 2000;39:4518-4526.
89. Ooi CE, Rabinovich E, Dancis A, Bonifacino JS, Klausner RD. Copper-dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1 p in the apparent absence of endocytosis. EMBO J 1996:15:3515-3523.
90. Roberg KJ, Rowley N, Kaiser CA. Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J Cell Biol 1997;137:1469-1482.
91. De Craene JO, Soetens O, Andre B. The Npr1 kinase controls biosynthetic and endocytic sorting of the yeast Gap1 permease. J Biol Chem 2001;276:43939-43948.
92. Soetens O, De Craene JO, Andre B. Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J Biol Chem 2001;276:43949-43957.
93. Helliwell SB, Losko S, Kaiser CA. Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J Cell Biol 2001;153:649-662.
94. Antonny B, Schekman R. ER export: public transportation by the COPII coach. Curr Opin Cell Biol 2001;13:438-443.
95. Durr G, Strayle J, Plemper R, Elbs S, Klee K, Catty P, Wolf DH, Rudolph HK. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 1998;9:1149-1162.