Cargo Capture and Bulk Flow in the Early Secretory Pathway

Annual Review of Cell and Developmental Biology

Volumn 32, Issue , 2016, Pages 197-222

  Barlowe, Charles ^a   Helenius, Ari ^b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b ETH ZURICH   (Switzerland)

Author keywords

Coat proteins; ER; Golgi; Protein secretion; Trafficking

Indexed keywords

ADAPTOR PROTEIN; CHAPERONE; COAT PROTEIN COMPLEX II; CORNICHON PROTEIN; ENDOPLASMIC RETICULUM GOLGI INTERMEDIATE COMPARTMENT PROTEIN 53; GAG PROTEIN; GLYCOPROTEIN; MEMBRANE PROTEIN; PROTEIN ERV26; PROTEIN ERV29; PROTEIN IRHOMS; PROTEIN SCAP; RECEPTOR PROTEIN; SECRETORY PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM MEMBRANE; ENZYME ACTIVITY; FLOW RATE; GOLGI COMPLEX; HUMAN; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TRANSPORT; SECRETORY PATHWAY; TRANSPORT VESICLE; ANIMAL; COP-COATED VESICLE; METABOLISM;

ANIMALS; COP-COATED VESICLES; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HUMANS; PROTEIN TRANSPORT; SECRETORY PATHWAY; TRANSPORT VESICLES;

EID: 84990833491     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-111315-125016     Document Type: Article

References (184)

1. Achour L, Labbe-Jullie C, Scott MG, Marullo S. 2008. An escort for GPCRs: implications for regulation of receptor density at the cell surface. Trends Pharmacol. Sci. 29:528-35
2. Adrain C, Freeman M. 2012. New lives for old: evolution of pseudoenzyme function illustrated by iRhoms. Nat. Rev. Mol. Cell Biol. 13:489-98
3. Anelli T, Sannino S, Sitia R. 2015. Proteostasis and "redoxtasis" in the secretory pathway: tales of tails from ERp44 and immunoglobulins. Free Radic. Biol. Med. 83:323-30
4. AppenzellerC, AnderssonH, Kappeler F,Hauri HP. 1999. The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat. Cell Biol. 1:330-34
5. Appenzeller-Herzog C, Hauri HP. 2006. The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J. Cell Sci. 119:2173-83
6. Appenzeller-Herzog C, Nyfeler B, Burkhard P, Santamaria I, Lopez-Otin C, HauriHP. 2005. Carbohydrateand conformation-dependent cargo capture for ER-exit. Mol. Biol. Cell 16:1258-67
7. Balch WE, McCaffery JM, Plutner H, Farquhar MG. 1994. Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell 76:841-52
8. Bannykh SI, Rowe T, Balch WE. 1996. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135:19-35
9. Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, et al. 2006. Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439:604-7
10. Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, et al. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895-907
11. Belden WJ, Barlowe C. 2001. Role of Erv29p in collecting soluble secretory proteins into ER-derived transport vesicles. Science 294:1528-31
12. Bendayan M, Roth J, Perrelet A, Orci L. 1980. Quantitative immunocytochemical localization of pancreatic secretory proteins in subcellular compartments of the rat acinar cell. J. Histochem. Cytochem. 28:149-60
13. Bevis BJ, Hammond AT, Reinke CA, Glick BS. 2002. De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat. Cell Biol. 4:750-56
14. Boehm J, Letourneur F, BallensiefenW, Ossipov D, Demolliere C, SchmittHD. 1997. Sec 12p requires Rer1p for sorting to coatomer (COPI)-coated vesicles and retrieval to the ER. J. Cell Sci. 110(Pt. 8):991-1003
15. Bokel C, Dass S, Wilsch-Brauninger M, Roth S. 2006. Drosophila Cornichon acts as cargo receptor for ER export of the TGFα-like growth factor Gurken. Development 133:459-70
16. Boncompain G, Divoux S, Gareil N, de Forges H, Lescure A, et al. 2012. Synchronization of secretory protein traffic in populations of cells. Nat. Methods 9:493-98
17. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116:153-66
18. Bonnon C,Wendeler MW, Paccaud JP, Hauri HP. 2010. Selective export of human GPI-anchored proteins from the endoplasmic reticulum. J. Cell Sci. 123:1705-15
19. Booth C, Koch GL. 1989. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell 59:729-37
20. Borgese N. 2016. Getting membrane proteins on and off the shuttle bus between the endoplasmic reticulum and the Golgi complex. J. Cell Sci. 129:1537-45
21. Braakman I, Bulleid NJ. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 80:71-99
22. Brandizzi F, Irons SL, Johansen J, Kotzer A, Neumann U. 2004. GFP is the way to glow: bioimaging of the plant endomembrane system. J. Microsc. 214:138-58
23. Bu G. 2001. The roles of receptor-associated protein (RAP) as a molecular chaperone for members of the LDL receptor family. Int. Rev. Cytol. 209:79-116
24. Budnik A, Stephens DJ. 2009. ER exit sites-localization and control of COPII vesicle formation. FEBS Lett. 583:3796-803
25. Bue CA, Barlowe C. 2009. Molecular dissection of Erv26p identifies separable cargo binding and coat protein sorting activities. J. Biol. Chem. 284:24049-60
26. Caldwell SR,Hill KJ,Cooper AA. 2001. Degradation of endoplasmic reticulum (ER) quality control substrates requires transport between the ER and Golgi. J. Biol. Chem. 276:23296-303
27. Castellino F, Zhong G, Germain RN. 1997. Antigen presentation byMHC class II molecules: invariant chain function, protein trafficking, and the molecular basis of diverse determinant capture. Hum. Immunol. 54:159-69
28. Castillon GA, Aguilera-Romero A, Manzano-Lopez J, Epstein S, Kajiwara K, et al. 2011. The yeast p24 complex regulates GPI-anchored protein transport and quality control by monitoring anchor remodeling. Mol. Biol. Cell 22:2924-36
29. Connerly PL, Esaki M, Montegna EA, Strongin DE, Levi S, et al. 2005. Sec 16 is a determinant of transitional ER organization. Curr. Biol. 15:1439-47
30. Copeland CS, Doms RW, Bolzau EM,Webster RG, Helenius A. 1986. Assembly of influenza hemagglutinin trimers and its role in intracellular transport. J. Cell Biol. 103:1179-91
31. Cortini M, Sitia R. 2010. ERp44 and ERGIC-53 synergize in coupling efficiency and fidelity of IgM polymerization and secretion. Traffic 11:651-59
32. Costantini LM, Irvin SC, Kennedy SC, Guo F, Goldstein H, et al. 2015. Engineering and exploitation of a fluorescent HIV-1 gp120 for live cell CD4 binding assays. Virology 476:240-48
33. D'Angelo G, Prencipe L, Iodice L, Beznoussenko G, Savarese M, et al. 2009. GRASP65 and GRASP55 sequentially promote the transport ofC-terminal valine-bearing cargos to and through the Golgi complex. J. Biol. Chem. 284:34849-60
34. Dancourt J, Barlowe C. 2009. Erv26p-dependent export of alkaline phosphatase from the ER requires lumenal domain recognition. Traffic 10:1006-18
35. Dayel MJ, Hom EF, Verkman AS. 1999. Diffusion of green fluorescent protein in the aqueous-phase lumen of endoplasmic reticulum. Biophys. J. 76:2843-51
36. De Meyer T, Depicker A. 2014. Trafficking of endoplasmic reticulum-retained recombinant proteins is unpredictable in Arabidopsis thaliana. Front. Plant Sci. 5:473
37. Doly S, ShirvaniH,GataG,Meye FJ, Emerit MB, et al. 2015.GABAB receptor cell-surface export is controlled by an endoplasmic reticulum gatekeeper. Mol. Psychiatry 21:480-90
38. Dominguez M, Dejgaard K, Fullekrug J, Dahan S, Fazel A, et al. 1998. gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer. J. Cell Biol. 140:751-65
39. Dong C, Filipeanu CM, Duvernay MT, Wu G. 2007. Regulation of G protein-coupled receptor export trafficking. Biochim. Biophys. Acta 1768:853-70
40. Dooley K, Bulutoglu B, Banta S. 2014. Doubling the cross-linking interface of a rationally designed beta roll peptide for calcium-dependent proteinaceous hydrogel formation. Biomacromolecules 15:3617-24
41. Dukhovny A, Yaffe Y, Shepshelovitch J, Hirschberg K. 2009. The length of cargo-protein transmembrane segments drives secretory transport by facilitating cargo concentration in export domains. J. Cell Sci. 122:1759-67
42. Eiden-Plach A, Zagorc T, HeintelT, Carius Y, Breinig F, SchmittMJ. 2004. Viral preprotoxin signal sequence allows efficient secretion of green fluorescent protein by Candida glabrata, Pichia pastoris, Saccharomyces cerevisiae, and Schizosaccharomyces pombe. Appl. Environ. Microbiol. 70:961-66
43. El Omari K, Iourin O, Kadlec J, Sutton G, Harlos K, et al. 2014. Unexpected structure for the N-terminal domain of hepatitis C virus envelope glycoprotein E1. Nat. Commun. 5:4874
44. Farhan H, Weiss M, Tani K, Kaufman RJ, Hauri HP. 2008. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J. 27:2043-54
45. Farhan H, WendelerMW,Mitrovic S, Fava E, Silberberg Y, et al. 2010.MAPKsignaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189:997-1011
46. Fath S, Mancias JD, Bi X, Goldberg J. 2007. Structure and organization of coat proteins in the COPII cage. Cell 129:1325-36
47. Fitting T, Kabat D. 1982. Evidence for a glycoprotein "signal" involved in transport between subcellular organelles. Two membrane glycoproteins encoded by murine leukemia virus reach the cell surface at different rates. J. Biol. Chem. 257:14011-17
48. Fitzgerald I, Glick BS. 2014. Secretion of a foreign protein from budding yeasts is enhanced by cotranslational translocation and by suppression of vacuolar targeting. Microb. Cell Fact. 13:125
49. Forster R, Weiss M, Zimmermann T, Reynaud EG, Verissimo F, et al. 2006. Secretory cargo regulates the turnover of COPII subunits at single ER exit sites. Curr. Biol. 16:173-79
50. Fossati M, Colombo SF, BorgeseN. 2014. A positive signal prevents secretorymembrane cargo from recycling between the Golgi and the ER. EMBO J. 33:2080-97
51. Fries E, Lindstrom I. 1986. The effects of low temperatures on intracellular transport of newly synthesized albumin and haptoglobin in rat hepatocytes. Biochem. J. 237:33-39
52. Fullekrug J, Boehm J, Rottger S, Nilsson T, Mieskes G, Schmitt HD. 1997. Human Rer1 is localized to the Golgi apparatus and complements the deletion of the homologous Rer1 protein of Saccharomyces cerevisiae. Eur. J. Cell Biol. 74:31-40
53. Gaudin Y, Moreira S, Benejean J, Blondel D, Flamand A, Tuffereau C. 1999. Soluble ectodomain of rabies virus glycoprotein expressed in eukaryotic cells folds in a monomeric conformation that is antigenically distinct from the native state of the complete, membrane-anchored glycoprotein. J. Gen. Virol. 80(Pt. 7):1647-56
54. Geiger R, Gautschi M, Thor F, Hayer A, Helenius A. 2011. Folding, quality control, and secretion of pancreatic ribonuclease in live cells. J. Biol. Chem. 286:5813-22
55. Geva Y, Schuldiner M. 2014. The back and forth of cargo exit from the endoplasmic reticulum. Curr. Biol. 24:R130-36
56. Goldstein JL, DeBose-Boyd RA, Brown MS. 2006. Protein sensors for membrane sterols. Cell 124:35-46
57. Griffiths G, Warren G, Quinn P, Mathieu-Costello O, Hoppeler H. 1984. Density of newly synthesized plasma membrane proteins in intracellular membranes. I. Stereological studies. J. Cell Biol. 98:2133-41
58. Haggie PM, Stanton BA, Verkman AS. 2002. Diffusional mobility of the cystic fibrosis transmembrane conductance regulator mutant, F508-CFTR, in the endoplasmic reticulum measured by photobleaching of GFP-CFTR chimeras. J. Biol. Chem. 277:16419-25
59. Hammond C, 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
60. Hauri HP, Kappeler F, Andersson H, Appenzeller C. 2000. ERGIC-53 and traffic in the secretory pathway. J. Cell Sci. 113(Pt. 4):587-96
61. HauriHP, Schweizer A. 1992. The endoplasmic reticulum-Golgi intermediate compartment. Curr. Opin. Cell Biol. 4:600-8
62. Heffernan LF, Simpson JC. 2014. The trials and tubule-ations of Rab6 involvement inGolgi-to-ER retrograde transport. Biochem. Soc. Trans. 42:1453-59
63. Herrmann JM, Malkus P, Schekman R. 1999. Out of the ER-outfitters, escorts and guides. Trends Cell Biol. 9:5-7
64. Herzig Y, Sharpe HJ, Elbaz Y, Munro S, Schuldiner M. 2012. A systematic approach to pair secretory cargo receptors with their cargo suggests a mechanism for cargo selection by Erv14. PLOS Biol. 10:e1001329
65. Hirz M, Richter G, Leitner E, Wriessnegger T, PichlerH. 2013. A novel cholesterol-producing Pichia pastoris strain is an ideal host for functional expression of human Na,K-ATPase α3β1 isoform. Appl. Microbiol. Biotechnol. 97:9465-78
66. Hsu CL, Prasad R, Blackman C, Ng DT. 2012. Endoplasmic reticulum stress regulation of the Kar2p/BiP chaperone alleviates proteotoxicity via dual degradation pathways. Mol. Biol. Cell 23:630-41
67. Hulsmann BB, Labokha AA, Gorlich D. 2012. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150:738-51
68. Hurtley SM, Helenius A. 1989. Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:277-307
69. Hutt DM, Balch WE. 2013. Expanding proteostasis by membrane trafficking networks. Cold Spring Harb. Perspect. Med. 5:a013383
70. Hyman AA, Simons K. 2012. Cell biology. Beyond oil and water-phase transitions in cells. Science 337:1047-49
71. Itin C, Roche AC, Monsigny M, Hauri HP. 1996. ERGIC-53 is a functional mannose-selective and calciumdependent human homologue of leguminous lectins. Mol. Biol. Cell 7:483-93
72. Jansen G, Maattanen P, Denisov AY, Scarffe L, Schade B, et al. 2012. An interaction map of endoplasmic reticulum chaperones and foldases. Mol. Cell. Proteom. 11:710-23
73. Kamada A, Nagaya H, Tamura T, Kinjo M, Jin HY, et al. 2004. Regulation of immature protein dynamics in the endoplasmic reticulum. J. Biol. Chem. 279:21533-42
74. Kanapin A, Batalov S, Davis MJ, Gough J, Grimmond S, et al. 2003. Mouse proteome analysis. Genome Res. 13:1335-44
75. Kappeler F, KlopfensteinDR, Foguet M, Paccaud JP, HauriHP. 1997. The recycling ofERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum-exit determinant interacting with COPII. J. Biol. Chem. 272:31801-8
76. Kim JY, Kim YG, LeeGM. 2012.CHOcells in biotechnology for production of recombinant proteins: current state and further potential. Appl. Microbiol. Biotechnol. 93:917-30
77. Kota J, Gilstring CF, Ljungdahl PO. 2007. Membrane chaperone Shr3 assists in folding amino acid permeases preventing precocious ERAD. J. Cell Biol. 176:617-28
78. Kota J, Ljungdahl PO. 2005. Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER. J. Cell Biol. 168:79-88
79. Kowalski JM, Parekh RN, Mao J,Wittrup KD. 1998. Protein folding stability can determine the efficiency of escape from endoplasmic reticulum quality control. J. Biol. Chem. 273:19453-58
80. Kuehn MJ, Herrmann JM, Schekman R. 1998. COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391:187-90
81. Lai CW, Aronson DE, Snapp EL. 2010. BiP availability distinguishes states of homeostasis and stress in the endoplasmic reticulum of living cells. Mol. Biol. Cell 21:1909-21
82. LeeMC, Miller EA, Goldberg J, Orci L, Schekman R. 2004. Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20:87-123
83. Letourneur F, Gaynor EC,Hennecke S,Demolliere C, DudenR, et al. 1994. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79:1199-207
84. Li P, Banjade S, Cheng HC, Kim S, Chen B, et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336-40
85. Lippincott-Schwartz J, RobertsTH, Hirschberg K. 2000. Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16:557-89
86. Lodish HF, KongN, SniderM, Strous GJ. 1983. Hepatoma secretory proteins migrate from rough endoplasmic reticulum to Golgi at characteristic rates. Nature 304:80-83
87. Loos A, Van Droogenbroeck B, Hillmer S, Grass J, Pabst M, et al. 2011. Expression of antibody fragments with a controlled N-glycosylation pattern and induction of endoplasmic reticulum-derived vesicles in seeds of Arabidopsis. Plant Physiol. 155:2036-48
88. Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS. 2006. Golgi maturation visualized in living yeast. Nature 441:1002-6
89. Lynes EM, Simmen T. 2011. Urban planning of the endoplasmic reticulum (ER): how diverse mechanisms segregate the many functions of the ER. Biochim. Biophys. Acta 1813:1893-905
90. Malchus N, Weiss M. 2010. Anomalous diffusion reports on the interaction of misfolded proteins with the quality control machinery in the endoplasmic reticulum. Biophys. J. 99:1321-28
91. Malhotra V, Erlmann P,Nogueira C. 2015. Procollagen export from the endoplasmic reticulum. Biochem. Soc. Trans. 43:104-7
92. Malkus P, Jiang F, Schekman R. 2002. Concentrative sorting of secretory cargo proteins into COPII-coated vesicles. J. Cell Biol. 159:915-21
93. Manzano-Lopez J, Perez-Linero AM, Aguilera-Romero A, Martin ME, Okano T, et al. 2015. COPII coat composition is actively regulated by luminal cargo maturation. Curr. Biol. 25:152-62
94. Marcus NY, Perlmutter DH. 2000. Glucosidase and mannosidase inhibitors mediate increased secretion of mutant α1 antitrypsin Z. J. Biol. Chem. 275:1987-92
95. Martinez-Menarguez JA, GeuzeHJ, Slot JW, Klumperman J. 1999. Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 98:81-90
96. Matsuoka K, Schekman R, Orci L, Heuser JE. 2001. Surface structure of the COPII-coated vesicle. PNAS 98:13705-9
97. Mayor S, Riezman H. 2004. Sorting GPI-anchored proteins. Nat. Rev. Mol. Cell Biol. 5:110-20
98. Meldolesi J, Pozzan T. 1998. The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem. Sci. 23:10-14
99. Meunier L, Usherwood YK, Chung KT, Hendershot LM. 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13:4456-69
100. Mezzacasa A, Helenius A. 2002. The transitional ER defines a boundary for quality control in the secretion of tsO45 VSV glycoprotein. Traffic 3:833-49
101. Michelsen K, Yuan H, Schwappach B. 2005. Hide and run. Arginine-based endoplasmic-reticulum-sorting motifs in the assembly of heteromultimeric membrane proteins. EMBO Rep. 6:717-22
102. Miller EA, Barlowe C. 2010. Regulation of coat assembly-sorting things out at the ER. Curr. Opin. Cell Biol. 22:447-53
103. Miller EA, Beilharz TH, Malkus PN, Lee MC, Hamamoto S, et al. 2003. Multiple cargo binding sites on the COPII subunit Sec 24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:497-509
104. Mossessova E, Bickford LC, Goldberg J. 2003. SNARE selectivity of the COPII coat. Cell 114:483-95
105. Muller L, Zhu X, Lindberg I. 1997. Mechanism of the facilitation of PC2 maturation by 7B2: involvement in ProPC2 transport and activation but not folding. J. Cell Biol. 139:625-38
106. Munro S, Pelham HR. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48:899-907
107. Nehls S, Snapp EL, Cole NB, Zaal KJ, Kenworthy AK, et al. 2000. Dynamics and retention of misfolded proteins in native ER membranes. Nat. Cell Biol. 2:288-95
108. Nichols WC, Seligsohn U, Zivelin A, Terry VH, Hertel CE, et al. 1998. Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell 93:61-70
109. Nigam SK, Goldberg AL, Ho S, Rohde MF, Bush KT, Sherman M. 1994. A set of endoplasmic reticulum proteins possessing properties of molecular chaperones includes Ca2+-binding proteins and members of the thioredoxin superfamily. J. Biol. Chem. 269:1744-49
110. Nikonov AV, Snapp E, Lippincott-Schwartz J, Kreibich G. 2002. Active translocon complexes labeled with GFP-Dad1 diffuse slowly as large polysome arrays in the endoplasmic reticulum. J. Cell Biol. 158:497-506
111. Nishimura N, Bannykh S, Slabough S, Matteson J, Altschuler Y, et al. 1999. A di-acidic (DXE) code directs concentration of cargo during export from the endoplasmic reticulum. J. Biol. Chem. 274:15937-46
112. Nufer O,Mitrovic S, Hauri HP. 2003. Profile-based data base scanning for animal L-type lectins and characterization of VIPL, a novel VIP36-like endoplasmic reticulum protein. J. Biol. Chem. 278:15886-96
113. Nyfeler B, Reiterer V, Wendeler MW, Stefan E, Zhang B, et al. 2008. Identification of ERGIC-53 as an intracellular transport receptor of α1-antitrypsin. J. Cell Biol. 180:705-12
114. Nyfeler B, Zhang B, GinsburgD, Kaufman RJ,Hauri HP. 2006. Cargo selectivity of the ERGIC-53/MCFD2 transport receptor complex. Traffic 7:1473-81
115. Orci L, Ravazzola M, Meda P, Holcomb C, MooreHP, et al. 1991. Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. PNAS 88:8611-15
116. Ostrovsky O, Makarewich CA, Snapp EL, Argon Y. 2009. An essential role for ATP binding and hydrolysis in the chaperone activity of GRP94 in cells. PNAS 106:11600-5
117. Otte S, Barlowe C. 2004. Sorting signals can direct receptor-mediated export of soluble proteins into COPII vesicles. Nat. Cell Biol. 6:1189-94
118. Otte S, Belden WJ, Heidtman M, Liu J, Jensen ON, Barlowe C. 2001. Erv41p and Erv46p: new components of COPII vesicles involved in transport between the ER and Golgi complex. J. Cell Biol. 152:503-18
119. Pagant S, Wu A, Edwards S, Diehl F, Miller EA. 2015. Sec24 is a coincidence detector that simultaneously binds two signals to drive ER export. Curr. Biol. 25:403-12
120. Palade G. 1975. Intracellular aspects of the process of protein synthesis. Science 189:867
121. Papanikou E, Glick BS. 2014. Golgi compartmentation and identity. Curr. Opin. Cell Biol. 29:74-81
122. Park SY, Yang JS, Schmider AB, Soberman RJ,Hsu VW. 2015. Coordinated regulation of bidirectional COPI transport at the Golgi by CDC42. Nature 521:529-32
123. Pelham HR. 1991. Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr. Opin. Cell Biol. 3:585-91
124. Pelham HR. 1994. About turn for the COPs? Cell 79:1125-27
125. Pena F, Jansens A, van ZadelhoffG, Braakman I. 2010. Calcium as a crucial cofactor for low density lipoprotein receptor folding in the endoplasmic reticulum. J. Biol. Chem. 285:8656-64
126. Pfeffer SR, Rothman JE. 1987. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu. Rev. Biochem. 56:829-52
127. Powers J, Barlowe C. 1998. Transport of Axl2p depends on Erv14p, an ER-vesicle protein related to the Drosophila cornichon gene product. J. Cell Biol. 142:1209-22
128. Powers J, Barlowe C. 2002. Erv14p directs a transmembrane secretory protein into COPII-coated transport vesicles. Mol. Biol. Cell 13:880-91
129. Presley JF, Cole NB, Schroer TA,HirschbergK,Zaal KJ,Lippincott-Schwartz J. 1997. ER-to-Golgi transport visualized in living cells. Nature 389:81-85
130. Raykhel I, Alanen H, Salo K, Jurvansuu J, Nguyen VD, et al. 2007. A molecular specificity code for the three mammalian KDEL receptors. J. Cell Biol. 179:1193-204
131. Rolls MM, Hall DH, Victor M, Stelzer EH, Rapoport TA. 2002. Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol. Biol. Cell 13:1778-91
132. Romisch K, Schekman R. 1992. Distinct processes mediate glycoprotein and glycopeptide export from the endoplasmic reticulum in Saccharomyces cerevisiae. PNAS 89:7227-31
133. Ronchi P, Colombo S, Francolini M, Borgese N. 2008. Transmembrane domain-dependent partitioning of membrane proteins within the endoplasmic reticulum. J. Cell Biol. 181:105-18
134. Roth S, Neuman-Silberberg FS, Barcelo G, Schupbach T. 1995. cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81:967-78
135. Saito K, Yamashiro K, Shimazu N, Tanabe T, Kontani K, Katada T. 2014. Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export. J. Cell Biol. 206:751-62
136. Salama NR, Yeung T, Schekman RW. 1993. The Sec13p complex and reconstitution of vesicle budding from the ER with purified cytosolic proteins. EMBO J. 12:4073-82
137. Sambrook JF. 1990. The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell 61:197-99
138. Sannino S, Anelli T, Cortini M, Masui S, Degano M, et al. 2014. Progressive quality control of secretory proteins in the early secretory compartment by ERp44. J. Cell Sci. 127:4260-69
139. Sato K, Sato M, Nakano A. 2003. Rer1p, a retrieval receptor for ER membrane proteins, recognizes transmembrane domains in multiple modes. Mol. Biol. Cell 14:3605-16
140. Sato M, Sato K, Nakano A. 2004. Endoplasmic reticulum quality control of unassembled iron transporter depends on Rer1p-mediated retrieval from the Golgi. Mol. Biol. Cell 15:1417-24
141. Sauvageau E, RochdiMD, OueslatiM,Hamdan FF, Percherancier Y, et al. 2014. CNIH4 interacts with newly synthesized GPCR and controls their export from the endoplasmic reticulum. Traffic 15:383-400
142. Sbalzarini IF, Mezzacasa A, Helenius A, Koumoutsakos P. 2005. Effects of organelle shape on fluorescence recovery after photobleaching. Biophys. J. 89:1482-92
143. Scales SJ, Pepperkok R, Kreis TE. 1997. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90:1137-48
144. Schimmoller F, Singer-Kruger B, Schroder S, Kruger U, Barlowe C, Riezman H. 1995. The absence of Emp24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J. 14:1329-39
145. Schwenk J, Harmel N, Zolles G, Bildl W, Kulik A, et al. 2009. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323:1313-19
146. Semenza JC, HardwickKG,DeanN,PelhamHR.1990.ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61:1349-57
147. Sengupta P, Satpute-Krishnan P, Seo AY, Burnette DT, Patterson GH, Lippincott-Schwartz J. 2015. ER trapping reveals Golgi enzymes continually revisit the ER through a recycling pathway that controls Golgi organization. PNAS 112:6752-61
148. Sharpe HJ, Stevens TJ, Munro S. 2010. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142:158-69
149. Shi XL, Feng MQ, Shi J, Shi ZH, Zhong J, Zhou P. 2007. High-level expression and purification of recombinant human catalase in Pichia pastoris. Protein Expr. Purif. 54:24-29
150. Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA. 2010. Mechanisms determining the morphology of the peripheral ER. Cell 143:774-88
151. Shibuya A, Margulis N, Christiano R,Walther TC, Barlowe C. 2015. The Erv41-Erv46 complex serves as a retrograde receptor to retrieve escaped ER proteins. J. Cell Biol. 208:197-209
152. Shimizu Y, Hendershot LM. 2007. Organization of the functions and components of the endoplasmic reticulum. Adv. Exp. Med. Biol. 594:37-46
153. Shindiapina P, Barlowe C. 2010. Requirements for transitional endoplasmic reticulum site structure and function in Saccharomyces cerevisiae. Mol. Biol. Cell 21:1530-45
154. Singh I, Doms RW, Wagner KR, Helenius A. 1990. Intracellular transport of soluble and membrane-bound glycoproteins: folding, assembly and secretion of anchor-free influenza hemagglutinin.EMBOJ. 9:631-39
155. Smith AJ, Daut J, Schwappach B. 2011. Membrane proteins as 14-3-3 clients in functional regulation and intracellular transport. Physiology 26:181-91
156. Snapp EL, Sharma A, Lippincott-Schwartz J, Hegde RS. 2006. Monitoring chaperone engagement of substrates in the endoplasmic reticulum of live cells. PNAS 103:6536-41
157. Sonnichsen B, Fullekrug J, Nguyen Van P, Diekmann W, Robinson DG, Mieskes G. 1994. Retention and retrieval: Both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J. Cell Sci. 107(Pt. 10):2705-17
158. Spear ED, Ng DT. 2003. Stress tolerance of misfolded carboxypeptidase Y requires maintenance of protein trafficking and degradative pathways. Mol. Biol. Cell 14:2756-67
159. Stagg SM, Gurkan C, Fowler DM, LaPointe P, Foss TR, et al. 2006. Structure of the Sec13/31 COPII coat cage. Nature 439:234-38
160. Stamnes MA, Craighead MW, Hoe MH, Lampen N, Geromanos S, et al. 1995. An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding. PNAS 92:8011-15
161. Stephens DJ. 2003. De novo formation, fusion and fission of mammalian COPII-coated endoplasmic reticulum exit sites. EMBO Rep. 4:210-17
162. Strating JR, van Bakel NH, Leunissen JA, Martens GJ. 2009. A comprehensive overview of the vertebrate p24 family: identification of a novel tissue-specifically expressed member. Mol. Biol. Evol. 26:1707-14
163. Strous GJ, Lodish HF. 1980. Intracellular transport of secretory and membrane proteins in hepatoma cells infected by vesicular stomatitis virus. Cell 22:709-17
164. Tabata KV, Sato K, Ide T, Nishizaka T, Nakano A, Noji H. 2009. Visualization of cargo concentration by COPII minimal machinery in a planar lipid membrane. EMBO J. 28:3279-89
165. Takida S, Maeda Y, Kinoshita T. 2008. Mammalian GPI-anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane. Biochem. J. 409:555-62
166. Tatu U, Helenius A. 1997. Interactions between newly synthesized glycoproteins, calnexin and a network of resident chaperones in the endoplasmic reticulum. J. Cell Biol. 136:555-65
167. Thor F, Gautschi M, Geiger R, Helenius A. 2009. Bulk flow revisited: transport of a soluble protein in the secretory pathway. Traffic 10:1819-30
168. Vavassori S, Cortini M, Masui S, Sannino S, Anelli T, et al. 2013. A pH-regulated quality control cycle for surveillance of secretory protein assembly. Mol. Cell 50:783-92
169. Voeltz GK, Rolls MM, Rapoport TA. 2002. Structural organization of the endoplasmic reticulum. EMBO Rep. 3:944-50
170. Walter P, RonD. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-86
171. Wang ZV, Schraw TD, Kim JY, Khan T, Rajala MW, et al. 2007. Secretion of the adipocyte-specific secretory protein adiponectin critically depends on thiol-mediated protein retention. Mol. Cell. Biol. 27:3716-31
172. Warren G. 2013. Transport through the Golgi in Trypanosoma brucei. Histochem. Cell Biol. 140:235-38
173. Warren G, Mellman I. 1999. Bulk flow redux? Cell 98:125-27
174. Wiedmann M, Huth A, Rapoport TA. 1984. Xenopus oocytes can secrete bacterial beta-lactamase. Nature 309:637-39
175. Wieland FT, Gleason ML, Serafini TA, Rothman JE. 1987. The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell 50:289-300
176. Williams DB, Swiedler SJ, Hart GW. 1985. Intracellular transport of membrane glycoproteins: Two closely related histocompatibility antigens differ in their rates of transit to the cell surface. J. Cell Biol. 101:725-34
177. Wiseman RL, Koulov A, Powers E, Kelly JW, Balch WE. 2007. Protein energetics in maturation of the early secretory pathway. Curr. Opin. Cell Biol. 19:359-67
178. Yamamoto K, Fujii R, Toyofuku Y, Saito T, Koseki H, et al. 2001. The KDEL receptor mediates a retrieval mechanism that contributes to quality control at the endoplasmic reticulum. EMBO J. 20:3082-91
179. Yelinek JT, He CY, Warren G. 2009. Ultrastructural study of Golgi duplication in Trypanosoma brucei. Traffic 10:300-6
180. Zanetti G, Pahuja KB, Studer S, Shim S, Schekman R. 2012. COPII and the regulation of protein sorting in mammals. Nat. Cell Biol. 14:20-28
181. Zettl M, Adrain C, Strisovsky K, Lastun V, Freeman M. 2011. Rhomboid family pseudoproteases use the ER quality control machinery to regulate intercellular signaling. Cell 145:79-91
182. Zhang B. 2009. Recent developments in the understanding of the combined deficiency of FV and FVIII. Br. J. Haematol. 145:15-23
183. Zhang JX, Braakman I, Matlack KE, 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 8:1943-54
184. Zhang Y,Motamed M, Seemann J, Brown MS, Goldstein JL. 2013. Point mutation in luminal loop 7 of Scap protein blocks interaction with loop 1 and abolishes movement to Golgi. J. Biol. Chem. 288:14059-67