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COPI proteins: A model for their role in vesicle budding

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Summary

COPI-coated vesicles are involved in intracellular trafficking between the endoplasmic reticulum and the Golgi complex. In the current model for COPI assembly the small GTP-binding protein ADP-ribosylation factor 1 is recruited from the cytoplasm to the Golgi membrane followed by binding of the hetero-oligomeric protein complex coatomer. However, the mechanism of subsequent vesicle budding is discussed controversially. This review summarizes the available experimental data on the COPI coat and discusses a model of how the major coat protein, coatomer, might act in vesicle budding.

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References

  • Amor JC, Harrison DH, Kahn RA, Ringe D (1994) Structure of the human ADP-ribosylation factor 1 complexed with GDP. Nature 372: 704–708

    Google Scholar 

  • Barlowe C (1998) COPII and selective export from the endoplasmic reticulum. Biochim Biophys Acta 1404: 67–76

    Google Scholar 

  • Belden WJ, Barlowe C (1996) Erv 25p, a component of COP.II-coated vesicles, forms a complex with Emp24 that is required for efficient endoplasmic-reticulum to Golgi transport. J Biol Chem 271: 26939–26946

    Google Scholar 

  • Boman AL, Kahn RA (1995) Arf proteins: the membrane traffic police? Trends Biochem Sci 20: 147–150

    Google Scholar 

  • Bremser M, Nickel W, Schweikert M, Ravazzola M, Amherdt M, Hughes CA, Söllner TH, Rothman JE, Wieland FT (1999) Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell 96: 495–506

    Google Scholar 

  • Brown HA, Gutowski CR, Moomaw C, Slaughter C, Sternweiss PC (1993) ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75: 1137–1144

    Google Scholar 

  • Chardin P, Paris S, Antonny B, Robineau S, Beraud Dufour S, Jackson CL, Chabre M (1996) A human exchange factor for ARF contains Sec7- and pleckstrin-homology domains. Nature 384: 481–484

    Google Scholar 

  • Cockcroft S, Thomas GM, Fensome A, Geny B, Cunningham E, Gout I, Hiles I, Totty NF, Truong O, Hsuan JJ (1994) Phospholipase D: a downstream effector of ARF in granulocytes. Science 263: 523–526

    Google Scholar 

  • Cosson P, Letourneur F (1994) Coatomer interaction with dilysine endoplasmic reticulum retention motifs. Science 263: 1629–1631

    Google Scholar 

  • —, Démollière C, Hennecke S, Duden R, Letourneur F (1996) Delta- and Zeta-COP, two coatomer subunits homologous to clathrin-associated proteins, are involved in ER retrieval. EMBO J 15: 1792–1798

    Google Scholar 

  • Dominguez M, Dejgaard K, Füllekrug J, Dahan S, Fazel A, Paccaud J-P, Thomas DY, Bergeron JJM, Nilsson T (1998) gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COPI and II coatomer. J Cell Biol 140: 751–765

    Google Scholar 

  • Donaldson JG, Cassel D, Kahn RA, Klausner RD (1992a) ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer beta-COP to Golgi membranes. Proc Natl Acad Sci USA 89: 6408–6412

    Google Scholar 

  • —, Finazzi D, Klausner RD (1992b) Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360: 350–352

    Google Scholar 

  • Duden R, Griffiths G, Frank R, Argos P, Kreis TE (1991) Beta-COP, a 110 kd protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to beta-adaptin. Cell 64: 649–665

    Google Scholar 

  • —, Hosobuchi M, Hamamoto S, Winey M, Byers B, Schekman R (1994) Yeast Beta- and Beta'-coat proteins (COP): two coatomer subunits essential for endoplasmic reticulum-to-Golgi protein traffic. J Biol Chem 269: 24486–24495

    Google Scholar 

  • —, Kajikawa L, Wuestehube L, Schekman R (1998) ɛ-COP is a structural component of coatomer that functions to stabilize α-COP. EMBO J 17: 985–995

    Google Scholar 

  • Faulstich D, Auerbach S, Orci L, Ravazzola M, Wegehingel S, Lottspeich F, Stenbeck G, Harter C, Wieland FT, Tschochner H (1996) Architecture of coatomer: molecular characterization of delta COP and protein interactions within the complex. J Cell Biol 135: 53–61

    Google Scholar 

  • Fiedler K, Veit M, Stamnes MA, Rothman JE (1996) Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science 273: 1396–1399

    Google Scholar 

  • Gerich B, Orci L, Tschochner H, Lottspeich F, Ravazzola M, Amherdt M, Wieland F, Harter C (1995) Non-clathrin-coat protein alpha is a conserved subunit of coatomer and inSaccharomyces cerevisiae is essential for growth. Proc Natl Acad Sci USA 92: 3229–3233

    Google Scholar 

  • Gommel D, Orci L, Emig EM, Hannah MJ, Ravazzola M, Nickel W, Helms JB, Wieland FT, Sohn K (1999) p24 and p23, the major transmembrane proteins of COPI-coated transport vesicles, form hetero-oligomeric complexes and cycle between the organelles of the early secretory pathway. FEBS Lett 447: 179–185

    Google Scholar 

  • Hara-Kuge S, Kuge O, Orci L, Amherdt M, Ravazzola M, Wieland FT, Rothman JE (1994) En bloc incorporation of coatomer subunits during the assembly of COP-coated vesicles. J Cell Biol 124: 883–892

    Google Scholar 

  • Harrison-Lavoie KJ, Lewis VA, Hynes GM, Collison KS, Nutland E, Willison KR (1993) A 102 kDa subunit of a Golgi-associated particle has homology to beta subunits of trimeric G proteins. EMBO J 12: 2847–2853

    Google Scholar 

  • Harter C, Wieland FT (1998) A single binding site for di-lysine retrieval motifs and p23 within the γ-subunit of coatomer. Proc Natl Acad Sci USA 95: 11649–11654

    Google Scholar 

  • —, Pavel J, Coccia F, Draken E, Wegehingel S, Tschochner H, Wieland F (1996) Nonclathrin coat protein gamma, a subunit of coatomer, binds to the cytoplasmic dilysine motif of membrane proteins of the early secretory pathway. Proc Natl Acad Sci USA 93: 1902–1906

    Google Scholar 

  • Helms JB, Rothman JE (1992) Inhibition by Brefeldin A of a Golgi membrane enzyme that catalyses exchange of a guanine nucleotide bound to ARF. Nature 360: 352–354

    Google Scholar 

  • —, Palmer DJ, Rothman JE (1993) Two distinct populations of ARF bound to Golgi membranes. J Cell Biol 121: 751–760

    Google Scholar 

  • Hosobuchi M, Kreis T, Schekman R (1992) SEC21 is a gene required for ER to Golgi protein transport that encodes a subunit of a yeast coatomer. Nature 360: 603–605

    Google Scholar 

  • Jackson MR, Nilsson T, Peterson PA (1993) Retrieval of trans-membrane proteins to the endoplasmic reticulum. J Cell Biol 121: 317–333

    Google Scholar 

  • Kahn RA, Gilman AG (1986) The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J Biol Chem 261: 7906–7911

    Google Scholar 

  • Kahn RA, Randazzo P, Serafini T, Weiss O, Rulka C, Clark J, Amherdt M, Roller P, Orci L, Rothman JE (1992) The amino terminus of ADP-ribosylation factor (ARF) is a critical determinant of ARF activities and is a potent and specific inhibitor of protein transport. J Biol Chem 267: 13039–13046

    Google Scholar 

  • Kaiser CA, Schekman R (1990) Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 61: 723–733

    Google Scholar 

  • Ktistakis NT, Brown HA, Waters MG, Sternweis PC, Roth MG (1996) Evidence that phospholipase D mediates ADP-ribosylation factor dependent formation Golgi coated vesicles. J Cell Biol 134: 295–306

    Google Scholar 

  • Kuge O, Hara Kuge S, Orci L, Ravazzola M, Amherdt M, Tanigawa G, Wieland FT, Rothman JE (1993) Zeta-COP, a subunit of coatomer, is required for COP-coated vesicle assembly. J Cell Biol 123: 1727–1734

    Google Scholar 

  • Letourneur F, Gaynor EC, Hennecke S, Demolliere C, Duden R, Emr SD, Riezman H, Cosson P (1994) Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79: 1199–1207

    Google Scholar 

  • Lowe M, Kreis TE (1995) In vitro assembly and disassembly of coatomer. J Biol Chem 270: 31364–31371

    Google Scholar 

  • Malhotra V, Serafini T, Orci L, Shepherd JC, Rothman JE (1989) Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58: 329–336

    Google Scholar 

  • Meacci E, Tsai SC, Adamik R, Moss J, Vaughan M (1997) Cytohesin 1, a cytosolic guanine nucleotide exchange protein for ADP ribosylation factor. Proc Natl Acad Sci USA 94: 1745–1748

    Google Scholar 

  • Melancon P, Glick BS, Malhotra V, Weidman PJ, Serafini T, Gleason ML, Orci L, Rothman JE (1987) Involvement of GTP-binding “G” proteins in transport through the Golgi stack. Cell 51: 1053–1062

    Google Scholar 

  • Neer EJ, Schmidt CJ, Nambudripad R, Smith TF (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371: 297–300

    Google Scholar 

  • Nilsson T, Jackson M, Peterson PA (1989) Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58: 707–718

    Google Scholar 

  • Orci L, Glick BS, Rothman JE (1986) A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack. Cell 46: 171–184

    Google Scholar 

  • —, Malhotra V, Amherdt M, Serafini T, Rothman JE (1989) Dissection of a single round of vesicular transport: sequential intermediates for intercisternal movement in the Golgi stack. Cell 56: 357–368

    Google Scholar 

  • —, Palmer DJ, Amherdt M, Rothman JE (1993) Coated vesicle assembly in the Golgi requires only coatomer and ARF proteins from the cytosol. Nature 364: 732–734

    Google Scholar 

  • —, Stamnes M, Ravazzola M, Amherdt M, Perrelet A, Söllner TH, Rothman JE (1997) Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90: 335–349

    Google Scholar 

  • Ostermann J, Orci L, Tani K, Amherdt M, Ravazzola M, Elazar Z, Rothman JE (1993) Stepwise assembly of functionally active transport vesicles. Cell 75: 1015–1025

    Google Scholar 

  • Palmer DJ, Helms JB, Beckers CJ, Orci L, Rothman JE (1993) Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J Biol Chem 268: 12083–12089

    Google Scholar 

  • Paris S, Beraud-Dufour S, Robineau S, Bigay J, Antonny B, Chabre M, Chardin P (1997) Role of protein-phospholipid interactions in the activation of ARF1 by guanine nucleotide exchange factor Arno. J Biol Chem 272: 22221–22226

    Google Scholar 

  • Pavel J, Harter C, Wieland FT (1998) Reversible dissociation of coatomer: functional characterization of a β/δ-coat protein subcomplex. Proc Natl Acad Sci USA 95: 2140–2145

    Google Scholar 

  • Pelham H (1995) Sorting and retrieval between the endoplasmic reticulum and Golgi apparatus. Curr Opin Cell Biol 7: 530–535

    Google Scholar 

  • Pepperkok R, Scheel J, Horstmann H, Hauri HP, Griffiths G, Kreis TE (1993) Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell 74: 71–82

    Google Scholar 

  • Peyroche A, Paris S, Jackson CL (1996) Nucleotide exchange on ARF mediated by yeast Geal protein. Nature 384: 479–481

    Google Scholar 

  • Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJM, Lippincott-Schwartz J (1997) ER-to-Golgi transport visualized in living cells. Nature 389: 81–85

    Google Scholar 

  • Randazzo PA (1997) Functional interaction of adp ribosylation factor 1 with phosphatidylinositol 4,5 bisphosphate. J Biol Chem 272: 7688–7692

    Google Scholar 

  • Reinhard C, Harter C, Bremser B, Brügger B, Sohn K, Helms JB, Wieland F (1999) Receptor induced polymerization of coatomer. Proc Natl Acad Sci USA 96: 1224–1228

    Google Scholar 

  • Rosa JL, Casarolimarano RP, Buckler AJ, Vilaro S, Barbacid M (1996) P619, a giant protein related to the chromosome condensation regulator rccl, stimulates guanine nucleotide exchange on ARF1 and rab proteins. EMBOJ 15: 4262–4273

    Google Scholar 

  • Rothman JE (1994) Mechanisms of intracellular protein transport. Nature 372: 55–63

    Google Scholar 

  • —, Wieland FT (1996) Protein sorting by transport vesicles. Science 272: 227–234

    Google Scholar 

  • 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: 1137–1148

    Google Scholar 

  • Schekman R, Orci L (1996) Coat proteins and vesicle budding. Science 271: 1526–1533

    Google Scholar 

  • Schimmöller F, Singer-Krüger B, Schröder S, Krüger U, Barlowe C, Riezman H (1995) The absence of Emp24p, a component of ER-derived COP II-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J 14: 1329–1339

    Google Scholar 

  • Schweizer A, Hauri H-P (1992) The endoplasmic reticulum-Golgi intermediate compartment. Curr Opin Cell Biol 4: 600–608

    Google Scholar 

  • Serafini T, Stenbeck G, Brecht A, Lottspeich F, Orci L, Rothman JE, Wieland FT (1991a) A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin. Nature 349: 215–220

    Google Scholar 

  • —, Orci L, Amherdt M, Brunner M, Kahn RA, Rothman JE (1991b) ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell 67: 239–253

    Google Scholar 

  • Sohn K, Orci L, Ravazzola M, Amherdt M, Bremser M, Lottspeich F, Fiedler K, Helms JB, Wieland FT (1996) A major membrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding. J Cell Biol 135: 1239–1248

    Google Scholar 

  • Stamnes MA, Craighead MW, Hoe MH, Lampen N, Geromanos S, Tempst P, Rothman JE (1995) An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding. Proc Natl Acad Sci USA 92: 8011–8015

    Google Scholar 

  • —, Schiavo G, Stenbeck G, Sollner TH, Rothman JE (1998) ADP-ribosylation factor and phosphatidic acid levels in Golgi membranes during budding of coatomer-coated vesicles. Proc Natl Acad Sci USA 95: 13676–13680

    Google Scholar 

  • Stenbeck G, Schreiner R, Herrmann D, Auerbach S, Lottspeich F, Rothman JE, Wieland FT (1992) Gamma-COP, a coat subunit of non-clathrin-coated vesicles with homology to Sec21p. FEBS Lett 314: 195–198

    Google Scholar 

  • —, Harter C, Brecht A, Herrmann D, Lottspeich F, Orci L, Wieland FT (1993) Beta'-COP, a novel subunit of coatomer. EMBO J 12: 2841–2845

    Google Scholar 

  • Tisdale EJ, Plutner H, Matteson J, Balch WE (1997) P53/58 binds COPI and is required for selective transport through the early secretory pathway. J Cell Biol 137: 581–593

    Google Scholar 

  • Waters MG, Serafini T, Rothman JE (1991) “Coatomer”: a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature 349: 248–251

    Google Scholar 

  • Zhao LY, Helms JB, Brugger B, Harter C, Martoglio B, Graf R, Brunner J, Wieland FT (1997) Direct and GTP-dependent interaction of ADP-ribosylation factor 1 with coatomer subunit beta. Proc Natl Acad Sci USA 94: 4418–4423

    Google Scholar 

  • — —, Brunner J, Wieland FT (1999) GTP-dependent binding of ADP-ribosylation factor to coatomer in close proximity to the binding site for dilysine retrieval motifs and p23. J Biol Chem 274: 14198–14203

    Google Scholar 

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Harter, C. COPI proteins: A model for their role in vesicle budding. Protoplasma 207, 125–132 (1999). https://doi.org/10.1007/BF01282991

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