1932

Abstract

Transport of newly synthesized proteins from the endoplasmic reticulum (ER) to the Golgi complex is highly selective. As a general rule, such transport is limited to soluble and membrane-associated secretory proteins that have reached properly folded and assembled conformations. To secure the efficiency, fidelity, and control of this crucial transport step, cells use a combination of mechanisms. The mechanisms are based on selective retention of proteins in the ER to prevent uptake into transport vesicles, on selective capture of proteins in COPII carrier vesicles, on inclusion of proteins in these vesicles by default as part of fluid and membrane bulk flow, and on selective retrieval of proteins from post-ER compartments by retrograde vesicle transport.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-111315-125016
2016-10-06
2024-06-16
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/32/1/annurev-cellbio-111315-125016.html?itemId=/content/journals/10.1146/annurev-cellbio-111315-125016&mimeType=html&fmt=ahah

Literature Cited

  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  4. Appenzeller C, Andersson H, Kappeler F, Hauri HP. 1999. The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat. Cell Biol. 1:330–34 [Google Scholar]
  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 [Google Scholar]
  6. Appenzeller-Herzog C, Nyfeler B, Burkhard P, Santamaria I, Lopez-Otin C, Hauri HP. 2005. Carbohydrate- and conformation-dependent cargo capture for ER-exit. Mol. Biol. Cell 16:1258–67 [Google Scholar]
  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 [Google Scholar]
  8. Bannykh SI, Rowe T, Balch WE. 1996. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135:19–35 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  11. Belden WJ, Barlowe C. 2001. Role of Erv29p in collecting soluble secretory proteins into ER-derived transport vesicles. Science 294:1528–31 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  14. Boehm J, Letourneur F, Ballensiefen W, Ossipov D, Demolliere C, Schmitt HD. 1997. Sec 12p requires Rer1p for sorting to coatomer (COPI)-coated vesicles and retrieval to the ER. J. Cell Sci. 110:Pt. 8991–1003 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  17. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116:153–66 [Google Scholar]
  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 [Google Scholar]
  19. Booth C, Koch GL. 1989. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell 59:729–37 [Google Scholar]
  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 [Google Scholar]
  21. Braakman I, Bulleid NJ. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 80:71–99 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  24. Budnik A, Stephens DJ. 2009. ER exit sites—localization and control of COPII vesicle formation. FEBS Lett 583:3796–803 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  27. Castellino F, Zhong G, Germain RN. 1997. Antigen presentation by MHC class II molecules: invariant chain function, protein trafficking, and the molecular basis of diverse determinant capture. Hum. Immunol. 54:159–69 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  33. D'Angelo G, Prencipe L, Iodice L, Beznoussenko G, Savarese M. et al. 2009. GRASP65 and GRASP55 sequentially promote the transport of C-terminal valine-bearing cargos to and through the Golgi complex. J. Biol. Chem. 284:34849–60 [Google Scholar]
  34. Dancourt J, Barlowe C. 2009. Erv26p-dependent export of alkaline phosphatase from the ER requires lumenal domain recognition. Traffic 10:1006–18 [Google Scholar]
  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 [Google Scholar]
  36. De Meyer T, Depicker A. 2014. Trafficking of endoplasmic reticulum–retained recombinant proteins is unpredictable in Arabidopsis thaliana. Front. Plant Sci. 5:473 [Google Scholar]
  37. Doly S, Shirvani H, Gata G, Meye FJ, Emerit MB. et al. 2015. GABAB receptor cell-surface export is controlled by an endoplasmic reticulum gatekeeper. Mol. Psychiatry 21:480–90 [Google Scholar]
  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 [Google Scholar]
  39. Dong C, Filipeanu CM, Duvernay MT, Wu G. 2007. Regulation of G protein–coupled receptor export trafficking. Biochim. Biophys. Acta 1768:853–70 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  42. Eiden-Plach A, Zagorc T, Heintel T, Carius Y, Breinig F, Schmitt MJ. 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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  45. Farhan H, Wendeler MW, Mitrovic S, Fava E, Silberberg Y. et al. 2010. MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189:997–1011 [Google Scholar]
  46. Fath S, Mancias JD, Bi X, Goldberg J. 2007. Structure and organization of coat proteins in the COPII cage. Cell 129:1325–36 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  50. Fossati M, Colombo SF, Borgese N. 2014. A positive signal prevents secretory membrane cargo from recycling between the Golgi and the ER. EMBO J 33:2080–97 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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. 71647–56 [Google Scholar]
  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 [Google Scholar]
  55. Geva Y, Schuldiner M. 2014. The back and forth of cargo exit from the endoplasmic reticulum. Curr. Biol. 24:R130–36 [Google Scholar]
  56. Goldstein JL, DeBose-Boyd RA, Brown MS. 2006. Protein sensors for membrane sterols. Cell 124:35–46 [Google Scholar]
  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 [Google Scholar]
  58. Haggie PM, Stanton BA, Verkman AS. 2002. Diffusional mobility of the cystic fibrosis transmembrane conductance regulator mutant, ΔF508-CFTR, in the endoplasmic reticulum measured by photobleaching of GFP-CFTR chimeras. J. Biol. Chem. 277:16419–25 [Google Scholar]
  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 [Google Scholar]
  60. Hauri HP, Kappeler F, Andersson H, Appenzeller C. 2000. ERGIC-53 and traffic in the secretory pathway. J. Cell Sci. 113:Pt. 4587–96 [Google Scholar]
  61. Hauri HP, Schweizer A. 1992. The endoplasmic reticulum–Golgi intermediate compartment. Curr. Opin. Cell Biol. 4:600–8 [Google Scholar]
  62. Heffernan LF, Simpson JC. 2014. The trials and tubule-ations of Rab6 involvement in Golgi-to-ER retrograde transport. Biochem. Soc. Trans. 42:1453–59 [Google Scholar]
  63. Herrmann JM, Malkus P, Schekman R. 1999. Out of the ER—outfitters, escorts and guides. Trends Cell Biol 9:5–7 [Google Scholar]
  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 [Google Scholar]
  65. Hirz M, Richter G, Leitner E, Wriessnegger T, Pichler H. 2013. A novel cholesterol-producing Pichia pastoris strain is an ideal host for functional expression of human Na,K-ATPase α 3β1 isoform. Appl. Microbiol. Biotechnol. 97:9465–78 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  68. Hurtley SM, Helenius A. 1989. Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:277–307 [Google Scholar]
  69. Hutt DM, Balch WE. 2013. Expanding proteostasis by membrane trafficking networks. Cold Spring Harb. Perspect. Med. 5:a013383 [Google Scholar]
  70. Hyman AA, Simons K. 2012. Cell biology. Beyond oil and water—phase transitions in cells. Science 337:1047–49 [Google Scholar]
  71. Itin C, Roche AC, Monsigny M, Hauri HP. 1996. ERGIC-53 is a functional mannose-selective and calcium-dependent human homologue of leguminous lectins. Mol. Biol. Cell 7:483–93 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  74. Kanapin A, Batalov S, Davis MJ, Gough J, Grimmond S. et al. 2003. Mouse proteome analysis. Genome Res 13:1335–44 [Google Scholar]
  75. Kappeler F, Klopfenstein DR, Foguet M, Paccaud JP, Hauri HP. 1997. The recycling of ERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum–exit determinant interacting with COPII. J. Biol. Chem. 272:31801–8 [Google Scholar]
  76. Kim JY, Kim YG, Lee GM. 2012. CHO cells in biotechnology for production of recombinant proteins: current state and further potential. Appl. Microbiol. Biotechnol. 93:917–30 [Google Scholar]
  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 [Google Scholar]
  78. Kota J, Ljungdahl PO. 2005. Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER. J. Cell Biol. 168:79–88 [Google Scholar]
  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 [Google Scholar]
  80. Kuehn MJ, Herrmann JM, Schekman R. 1998. COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391:187–90 [Google Scholar]
  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 [Google Scholar]
  82. Lee MC, 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 [Google Scholar]
  83. Letourneur F, Gaynor EC, Hennecke S, Demolliere C, Duden R. et al. 1994. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79:1199–207 [Google Scholar]
  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 [Google Scholar]
  85. Lippincott-Schwartz J, Roberts TH, Hirschberg K. 2000. Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16:557–89 [Google Scholar]
  86. Lodish HF, Kong N, Snider M, Strous GJ. 1983. Hepatoma secretory proteins migrate from rough endoplasmic reticulum to Golgi at characteristic rates. Nature 304:80–83 [Google Scholar]
  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 [Google Scholar]
  88. Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS. 2006. Golgi maturation visualized in living yeast. Nature 441:1002–6 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  91. Malhotra V, Erlmann P, Nogueira C. 2015. Procollagen export from the endoplasmic reticulum. Biochem. Soc. Trans. 43:104–7 [Google Scholar]
  92. Malkus P, Jiang F, Schekman R. 2002. Concentrative sorting of secretory cargo proteins into COPII-coated vesicles. J. Cell Biol. 159:915–21 [Google Scholar]
  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 [Google Scholar]
  94. Marcus NY, Perlmutter DH. 2000. Glucosidase and mannosidase inhibitors mediate increased secretion of mutant α1 antitrypsin Z. J. Biol. Chem. 275:1987–92 [Google Scholar]
  95. Martinez-Menarguez JA, Geuze HJ, 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 [Google Scholar]
  96. Matsuoka K, Schekman R, Orci L, Heuser JE. 2001. Surface structure of the COPII-coated vesicle. PNAS 98:13705–9 [Google Scholar]
  97. Mayor S, Riezman H. 2004. Sorting GPI-anchored proteins. Nat. Rev. Mol. Cell Biol. 5:110–20 [Google Scholar]
  98. Meldolesi J, Pozzan T. 1998. The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem. Sci. 23:10–14 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  102. Miller EA, Barlowe C. 2010. Regulation of coat assembly—sorting things out at the ER. Curr. Opin. Cell Biol. 22:447–53 [Google Scholar]
  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 [Google Scholar]
  104. Mossessova E, Bickford LC, Goldberg J. 2003. SNARE selectivity of the COPII coat. Cell 114:483–95 [Google Scholar]
  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 [Google Scholar]
  106. Munro S, Pelham HR. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48:899–907 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  114. Nyfeler B, Zhang B, Ginsburg D, Kaufman RJ, Hauri HP. 2006. Cargo selectivity of the ERGIC-53/MCFD2 transport receptor complex. Traffic 7:1473–81 [Google Scholar]
  115. Orci L, Ravazzola M, Meda P, Holcomb C, Moore HP. et al. 1991. Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. PNAS 88:8611–15 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  120. Palade G. 1975. Intracellular aspects of the process of protein synthesis. Science 189:867 [Google Scholar]
  121. Papanikou E, Glick BS. 2014. Golgi compartmentation and identity. Curr. Opin. Cell Biol. 29:74–81 [Google Scholar]
  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 [Google Scholar]
  123. Pelham HR. 1991. Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr. Opin. Cell Biol. 3:585–91 [Google Scholar]
  124. Pelham HR. 1994. About turn for the COPs?. Cell 79:1125–27 [Google Scholar]
  125. Pena F, Jansens A, van Zadelhoff G, Braakman I. 2010. Calcium as a crucial cofactor for low density lipoprotein receptor folding in the endoplasmic reticulum. J. Biol. Chem. 285:8656–64 [Google Scholar]
  126. Pfeffer SR, Rothman JE. 1987. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu. Rev. Biochem. 56:829–52 [Google Scholar]
  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 [Google Scholar]
  128. Powers J, Barlowe C. 2002. Erv14p directs a transmembrane secretory protein into COPII-coated transport vesicles. Mol. Biol. Cell 13:880–91 [Google Scholar]
  129. Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J. 1997. ER-to-Golgi transport visualized in living cells. Nature 389:81–85 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  132. Romisch K, Schekman R. 1992. Distinct processes mediate glycoprotein and glycopeptide export from the endoplasmic reticulum in Saccharomyces cerevisiae. PNAS 89:7227–31 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  137. Sambrook JF. 1990. The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell 61:197–99 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  141. Sauvageau E, Rochdi MD, Oueslati M, 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 [Google Scholar]
  142. Sbalzarini IF, Mezzacasa A, Helenius A, Koumoutsakos P. 2005. Effects of organelle shape on fluorescence recovery after photobleaching. Biophys. J. 89:1482–92 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  146. Semenza JC, Hardwick KG, Dean N, Pelham HR. 1990. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61:1349–57 [Google Scholar]
  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:E6752–61 [Google Scholar]
  148. Sharpe HJ, Stevens TJ, Munro S. 2010. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142:158–69 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  152. Shimizu Y, Hendershot LM. 2007. Organization of the functions and components of the endoplasmic reticulum. Adv. Exp. Med. Biol. 594:37–46 [Google Scholar]
  153. Shindiapina P, Barlowe C. 2010. Requirements for transitional endoplasmic reticulum site structure and function in Saccharomyces cerevisiae. Mol. Biol. Cell 21:1530–45 [Google Scholar]
  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. EMBO J 9:631–39 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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. 102705–17 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  161. Stephens DJ. 2003. De novo formation, fusion and fission of mammalian COPII-coated endoplasmic reticulum exit sites. EMBO Rep 4:210–17 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  169. Voeltz GK, Rolls MM, Rapoport TA. 2002. Structural organization of the endoplasmic reticulum. EMBO Rep 3:944–50 [Google Scholar]
  170. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081–86 [Google Scholar]
  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 [Google Scholar]
  172. Warren G. 2013. Transport through the Golgi in Trypanosoma brucei. Histochem. Cell Biol. 140:235–38 [Google Scholar]
  173. Warren G, Mellman I. 1999. Bulk flow redux?. Cell 98:125–27 [Google Scholar]
  174. Wiedmann M, Huth A, Rapoport TA. 1984. Xenopus oocytes can secrete bacterial beta-lactamase. Nature 309:637–39 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  179. Yelinek JT, He CY, Warren G. 2009. Ultrastructural study of Golgi duplication in Trypanosoma brucei. Traffic 10:300–6 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
  182. Zhang B. 2009. Recent developments in the understanding of the combined deficiency of FV and FVIII. Br. J. Haematol. 145:15–23 [Google Scholar]
  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 [Google Scholar]
  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 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-111315-125016
Loading
/content/journals/10.1146/annurev-cellbio-111315-125016
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error