Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Dec 2;123(6):1365–1371. doi: 10.1083/jcb.123.6.1365

Hydrolysis of bound GTP by ARF protein triggers uncoating of Golgi- derived COP-coated vesicles

PMCID: PMC2290881  PMID: 8253837

Abstract

The cycle of nucleotide exchange and hydrolysis by a small GTP-binding protein, ADP-ribosylation factor (ARF), helps to provide vectoriality to vesicle transport. Coat assembly is triggered when ARF binds GTP, initiating transport vesicle budding, and coat disassembly is triggered when ARF hydrolyzes GTP, allowing the uncoated vesicle to fuse.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balch W. E., Dunphy W. G., Braell W. A., Rothman J. E. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell. 1984 Dec;39(2 Pt 1):405–416. doi: 10.1016/0092-8674(84)90019-9. [DOI] [PubMed] [Google Scholar]
  2. Balch W. E., Rothman J. E. Characterization of protein transport between successive compartments of the Golgi apparatus: asymmetric properties of donor and acceptor activities in a cell-free system. Arch Biochem Biophys. 1985 Jul;240(1):413–425. doi: 10.1016/0003-9861(85)90046-3. [DOI] [PubMed] [Google Scholar]
  3. Bourne H. R. Do GTPases direct membrane traffic in secretion? Cell. 1988 Jun 3;53(5):669–671. doi: 10.1016/0092-8674(88)90081-5. [DOI] [PubMed] [Google Scholar]
  4. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991 Jan 10;349(6305):117–127. doi: 10.1038/349117a0. [DOI] [PubMed] [Google Scholar]
  5. Brennwald P., Novick P. Interactions of three domains distinguishing the Ras-related GTP-binding proteins Ypt1 and Sec4. Nature. 1993 Apr 8;362(6420):560–563. doi: 10.1038/362560a0. [DOI] [PubMed] [Google Scholar]
  6. Der C. J., Finkel T., Cooper G. M. Biological and biochemical properties of human rasH genes mutated at codon 61. Cell. 1986 Jan 17;44(1):167–176. doi: 10.1016/0092-8674(86)90495-2. [DOI] [PubMed] [Google Scholar]
  7. Donaldson J. G., Cassel D., Kahn R. A., Klausner R. D. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein beta-COP to Golgi membranes. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6408–6412. doi: 10.1073/pnas.89.14.6408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Donaldson J. G., Finazzi D., Klausner R. D. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature. 1992 Nov 26;360(6402):350–352. doi: 10.1038/360350a0. [DOI] [PubMed] [Google Scholar]
  9. Dubendorff J. W., Studier F. W. Controlling basal expression in an inducible T7 expression system by blocking the target T7 promoter with lac repressor. J Mol Biol. 1991 May 5;219(1):45–59. doi: 10.1016/0022-2836(91)90856-2. [DOI] [PubMed] [Google Scholar]
  10. Dunn B., Stearns T., Botstein D. Specificity domains distinguish the Ras-related GTPases Ypt1 and Sec4. Nature. 1993 Apr 8;362(6420):563–565. doi: 10.1038/362563a0. [DOI] [PubMed] [Google Scholar]
  11. Duronio R. J., Jackson-Machelski E., Heuckeroth R. O., Olins P. O., Devine C. S., Yonemoto W., Slice L. W., Taylor S. S., Gordon J. I. Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1506–1510. doi: 10.1073/pnas.87.4.1506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Haun R. S., Tsai S. C., Adamik R., Moss J., Vaughan M. Effect of myristoylation on GTP-dependent binding of ADP-ribosylation factor to Golgi. J Biol Chem. 1993 Apr 5;268(10):7064–7068. [PubMed] [Google Scholar]
  13. Helms J. B., Palmer D. J., Rothman J. E. Two distinct populations of ARF bound to Golgi membranes. J Cell Biol. 1993 May;121(4):751–760. doi: 10.1083/jcb.121.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Helms J. B., Rothman J. E. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature. 1992 Nov 26;360(6402):352–354. doi: 10.1038/360352a0. [DOI] [PubMed] [Google Scholar]
  15. Higuchi R., Krummel B., Saiki R. K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 1988 Aug 11;16(15):7351–7367. doi: 10.1093/nar/16.15.7351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hosobuchi M., Kreis T., Schekman R. SEC21 is a gene required for ER to Golgi protein transport that encodes a subunit of a yeast coatomer. Nature. 1992 Dec 10;360(6404):603–605. doi: 10.1038/360603a0. [DOI] [PubMed] [Google Scholar]
  17. Kahn R. A. Fluoride is not an activator of the smaller (20-25 kDa) GTP-binding proteins. J Biol Chem. 1991 Aug 25;266(24):15595–15597. [PubMed] [Google Scholar]
  18. Kahn R. A., Gilman A. G. The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J Biol Chem. 1986 Jun 15;261(17):7906–7911. [PubMed] [Google Scholar]
  19. Kahn R. A., Randazzo P., Serafini T., Weiss O., Rulka C., Clark J., Amherdt M., Roller P., Orci L., Rothman J. E. 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. 1992 Jun 25;267(18):13039–13046. [PubMed] [Google Scholar]
  20. Klausner R. D., Donaldson J. G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol. 1992 Mar;116(5):1071–1080. doi: 10.1083/jcb.116.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. Melançon P., Glick B. S., Malhotra V., Weidman P. J., Serafini T., Gleason M. L., Orci L., Rothman J. E. Involvement of GTP-binding "G" proteins in transport through the Golgi stack. Cell. 1987 Dec 24;51(6):1053–1062. doi: 10.1016/0092-8674(87)90591-5. [DOI] [PubMed] [Google Scholar]
  23. Northup J. K., Smigel M. D., Gilman A. G. The guanine nucleotide activating site of the regulatory component of adenylate cyclase. Identification by ligand binding. J Biol Chem. 1982 Oct 10;257(19):11416–11423. [PubMed] [Google Scholar]
  24. Orci L., Glick B. S., Rothman J. E. A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack. Cell. 1986 Jul 18;46(2):171–184. doi: 10.1016/0092-8674(86)90734-8. [DOI] [PubMed] [Google Scholar]
  25. Orci L., Malhotra V., Amherdt M., Serafini T., Rothman J. E. Dissection of a single round of vesicular transport: sequential intermediates for intercisternal movement in the Golgi stack. Cell. 1989 Feb 10;56(3):357–368. doi: 10.1016/0092-8674(89)90239-0. [DOI] [PubMed] [Google Scholar]
  26. Orci L., Palmer D. J., Ravazzola M., Perrelet A., Amherdt M., Rothman J. E. Budding from Golgi membranes requires the coatomer complex of non-clathrin coat proteins. Nature. 1993 Apr 15;362(6421):648–652. doi: 10.1038/362648a0. [DOI] [PubMed] [Google Scholar]
  27. Orci L., Tagaya M., Amherdt M., Perrelet A., Donaldson J. G., Lippincott-Schwartz J., Klausner R. D., Rothman J. E. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae. Cell. 1991 Mar 22;64(6):1183–1195. doi: 10.1016/0092-8674(91)90273-2. [DOI] [PubMed] [Google Scholar]
  28. Orcl L., Palmer D. J., Amherdt M., Rothman J. E. Coated vesicle assembly in the Golgi requires only coatomer and ARF proteins from the cytosol. Nature. 1993 Aug 19;364(6439):732–734. doi: 10.1038/364732a0. [DOI] [PubMed] [Google Scholar]
  29. Palade G. Intracellular aspects of the process of protein synthesis. Science. 1975 Aug 1;189(4200):347–358. doi: 10.1126/science.1096303. [DOI] [PubMed] [Google Scholar]
  30. Palmer D. J., Helms J. B., Beckers C. J., Orci L., Rothman J. E. Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J Biol Chem. 1993 Jun 5;268(16):12083–12089. [PubMed] [Google Scholar]
  31. Pepperkok R., Scheel J., Horstmann H., Hauri H. P., Griffiths G., Kreis T. E. Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell. 1993 Jul 16;74(1):71–82. doi: 10.1016/0092-8674(93)90295-2. [DOI] [PubMed] [Google Scholar]
  32. Peter F., Plutner H., Zhu H., Kreis T. E., Balch W. E. Beta-COP is essential for transport of protein from the endoplasmic reticulum to the Golgi in vitro. J Cell Biol. 1993 Sep;122(6):1155–1167. doi: 10.1083/jcb.122.6.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pfeffer S. R. GTP-binding proteins in intracellular transport. Trends Cell Biol. 1992 Feb;2(2):41–46. doi: 10.1016/0962-8924(92)90161-f. [DOI] [PubMed] [Google Scholar]
  34. Plutner H., Cox A. D., Pind S., Khosravi-Far R., Bourne J. R., Schwaninger R., Der C. J., Balch W. E. Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J Cell Biol. 1991 Oct;115(1):31–43. doi: 10.1083/jcb.115.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pryer N. K., Wuestehube L. J., Schekman R. Vesicle-mediated protein sorting. Annu Rev Biochem. 1992;61:471–516. doi: 10.1146/annurev.bi.61.070192.002351. [DOI] [PubMed] [Google Scholar]
  36. Rothman J. E., Orci L. Molecular dissection of the secretory pathway. Nature. 1992 Jan 30;355(6359):409–415. doi: 10.1038/355409a0. [DOI] [PubMed] [Google Scholar]
  37. Serafini T., Orci L., Amherdt M., Brunner M., Kahn R. A., Rothman J. E. ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell. 1991 Oct 18;67(2):239–253. doi: 10.1016/0092-8674(91)90176-y. [DOI] [PubMed] [Google Scholar]
  38. Serafini T., Stenbeck G., Brecht A., Lottspeich F., Orci L., Rothman J. E., Wieland F. T. A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin. Nature. 1991 Jan 17;349(6306):215–220. doi: 10.1038/349215a0. [DOI] [PubMed] [Google Scholar]
  39. Stamnes M. A., Rothman J. E. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell. 1993 Jun 4;73(5):999–1005. doi: 10.1016/0092-8674(93)90277-w. [DOI] [PubMed] [Google Scholar]
  40. Stearns T., Kahn R. A., Botstein D., Hoyt M. A. ADP ribosylation factor is an essential protein in Saccharomyces cerevisiae and is encoded by two genes. Mol Cell Biol. 1990 Dec;10(12):6690–6699. doi: 10.1128/mcb.10.12.6690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stenbeck G., Schreiner R., Herrmann D., Auerbach S., Lottspeich F., Rothman J. E., Wieland F. T. Gamma-COP, a coat subunit of non-clathrin-coated vesicles with homology to Sec21p. FEBS Lett. 1992 Dec 14;314(2):195–198. doi: 10.1016/0014-5793(92)80973-k. [DOI] [PubMed] [Google Scholar]
  42. Sztul E. S., Melançon P., Howell K. E. Targeting and fusion in vesicular transport. Trends Cell Biol. 1992 Dec;2(12):381–386. doi: 10.1016/0962-8924(92)90051-n. [DOI] [PubMed] [Google Scholar]
  43. Söllner T., Whiteheart S. W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., Rothman J. E. SNAP receptors implicated in vesicle targeting and fusion. Nature. 1993 Mar 25;362(6418):318–324. doi: 10.1038/362318a0. [DOI] [PubMed] [Google Scholar]
  44. Taylor T. C., Kahn R. A., Melançon P. Two distinct members of the ADP-ribosylation factor family of GTP-binding proteins regulate cell-free intra-Golgi transport. Cell. 1992 Jul 10;70(1):69–79. doi: 10.1016/0092-8674(92)90534-j. [DOI] [PubMed] [Google Scholar]
  45. Walker M. W., Bobak D. A., Tsai S. C., Moss J., Vaughan M. GTP but not GDP analogues promote association of ADP-ribosylation factors, 20-kDa protein activators of cholera toxin, with phospholipids and PC-12 cell membranes. J Biol Chem. 1992 Feb 15;267(5):3230–3235. [PubMed] [Google Scholar]
  46. Waters M. G., Serafini T., Rothman J. E. 'Coatomer': a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature. 1991 Jan 17;349(6306):248–251. doi: 10.1038/349248a0. [DOI] [PubMed] [Google Scholar]
  47. Weiss O., Holden J., Rulka C., Kahn R. A. Nucleotide binding and cofactor activities of purified bovine brain and bacterially expressed ADP-ribosylation factor. J Biol Chem. 1989 Dec 15;264(35):21066–21072. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES