Home LiteratureArticle Details
PMID: 16093346 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Oligomerization and dissociation of AP-1 adaptors are regulated by cargo signals and by ArfGAP1-induced GTP hydrolysis.

Molecular biology of the cell ·Vol. 16 ·No. 10 ·2005-10-00 ·Pages 4745-54

Meyer DM, Crottet P, Maco B, Degtyar E, Cassel D, Spiess M

Abstract

The mechanism of AP-1/clathrin coat formation was analyzed using purified adaptor proteins and synthetic liposomes presenting tyrosine sorting signals. AP-1 adaptors recruited in the presence of Arf1.GTP and sorting signals were found to oligomerize to high-molecular-weight complexes even in the absence of clathrin. The appendage domains of the AP-1 adaptins were not required for oligomerization. On GTP hydrolysis induced by the GTPase-activating protein ArfGAP1, the complexes were disassembled and AP-1 dissociated from the membrane. AP-1 stimulated ArfGAP1 activity, suggesting a role of AP-1 in the regulation of the Arf1 "GTPase timer." In the presence of cytosol, AP-1 could be recruited to liposomes without sorting signals, consistent with the existence of docking factors in the cytosol. Under these conditions, however, AP-1 remained monomeric, and recruitment in the presence of GTP was short-lived. Sorting signals allowed stable recruitment and oligomerization also in the presence of cytosol. These results suggest a mechanism whereby initial assembly of AP-1 with Arf1.GTP and ArfGAP1 on the membrane stimulates Arf1 GTPase activity, whereas interaction with cargo induces oligomerization and reduces the rate of GTP hydrolysis, thus contributing to efficient cargo sorting.

MeSH Terms
Adaptor Protein Complex 2/metabolism Animals COS Cells Cattle Cell Membrane/metabolism Chlorocebus aethiops Clathrin/metabolism Clathrin-Coated Vesicles/metabolism Cytosol/metabolism GTPase-Activating Proteins/metabolism Guanosine Triphosphate/metabolism Hydrolysis In Vitro Techniques Liposomes/metabolism Molecular Weight Protein Sorting Signals/physiology Transcription Factor AP-1/metabolism
Chemicals
Adaptor Protein Complex 2 Clathrin GTPase-Activating Proteins Liposomes Protein Sorting Signals Transcription Factor AP-1 Guanosine Triphosphate
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Meyer Daniel M
Biozentrum, University of Basel, CH-4056 Basel, Switzerland.
Crottet Pascal
Maco Bohumil
Degtyar Elena
Cassel Dan
Spiess Martin
References (58)
58 references, click to expand
  1. Receptor-induced polymerization of coatomer.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1224-8 PMID: 9990005
  2. Retrograde transport from the yeast Golgi is mediated by two ARF GAP proteins with overlapping function.
    EMBO J. 1999 Feb 1;18(3):555-64 PMID: 9927415
  3. Structural and functional analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis.
    Cell. 1999 Mar 19;96(6):893-902 PMID: 10102276
  4. ADP-ribosylation factor 1 dependent clathrin-coat assembly on synthetic liposomes.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5013-8 PMID: 10220410
  5. AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs.
    Science. 1999 Aug 20;285(5431):1268-71 PMID: 10455054
  6. GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COP I vesicles.
    EMBO J. 1999 Sep 15;18(18):4935-48 PMID: 10487746
  7. ARFGAP1 plays a central role in coupling COPI cargo sorting with vesicle formation.
    J Cell Biol. 2005 Jan 17;168(2):281-90 PMID: 15657398
  8. The small G-protein Arf6GTP recruits the AP-2 adaptor complex to membranes.
    J Biol Chem. 2005 Jun 3;280(22):21661-6 PMID: 15802264
  9. COPI vesicles accumulating in the presence of a GTP restricted arf1 mutant are depleted of anterograde and retrograde cargo.
    J Cell Sci. 2000 Jan;113 ( Pt 1):135-44 PMID: 10591632
  10. A role for ADP ribosylation factor in the control of cargo uptake during COPI-coated vesicle biogenesis.
    FEBS Lett. 1999 Dec 3;462(3):267-72 PMID: 10622709
  11. Decoding of sorting signals by coatomer through a GTPase switch in the COPI coat complex.
    Cell. 2000 Mar 17;100(6):671-9 PMID: 10761932
  12. Identification of the universal cofactor (auxilin 2) in clathrin coat dissociation.
    Eur J Cell Biol. 2000 May;79(5):336-42 PMID: 10887964
  13. Role of coatomer and phospholipids in GTPase-activating protein-dependent hydrolysis of GTP by ADP-ribosylation factor-1.
    J Biol Chem. 2000 Aug 4;275(31):23615-9 PMID: 10811810
  14. The assembly of AP-3 adaptor complex-containing clathrin-coated vesicles on synthetic liposomes.
    Mol Biol Cell. 2000 Nov;11(11):3723-36 PMID: 11071902
  15. A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex.
    Cell. 2000 Nov 10;103(4):569-81 PMID: 11106728
  16. Expression of auxilin or AP180 inhibits endocytosis by mislocalizing clathrin: evidence for formation of nascent pits containing AP1 or AP2 but not clathrin.
    J Cell Sci. 2001 Jan;114(Pt 2):353-65 PMID: 11148137
  17. Expression, purification, and properties of ADP-ribosylation factor (ARF) GTPase activating protein-1.
    Methods Enzymol. 2001;329:307-16 PMID: 11210549
  18. Three ways to make a vesicle.
    Nat Rev Mol Cell Biol. 2000 Dec;1(3):187-98 PMID: 11252894
  19. Dynamics of the COPII coat with GTP and stable analogues.
    Nat Cell Biol. 2001 Jun;3(6):531-7 PMID: 11389436
  20. Adaptor-related proteins.
    Curr Opin Cell Biol. 2001 Aug;13(4):444-53 PMID: 11454451
  21. Regulation of GTP hydrolysis on ADP-ribosylation factor-1 at the Golgi membrane.
    J Biol Chem. 2001 Dec 21;276(51):47834-9 PMID: 11592960
  22. Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1.
    J Cell Biol. 2001 Dec 24;155(7):1199-212 PMID: 11748249
  23. Overexpression of an ADP-ribosylation factor-guanine nucleotide exchange factor, BIG2, uncouples brefeldin A-induced adaptor protein-1 coat dissociation and membrane tubulation.
    J Biol Chem. 2002 Mar 15;277(11):9468-73 PMID: 11777925
  24. Cargo selection in vesicular transport: the making and breaking of a coat.
    Traffic. 2002 Aug;3(8):537-46 PMID: 12121417
  25. ARFGAP1 promotes the formation of COPI vesicles, suggesting function as a component of the coat.
    J Cell Biol. 2002 Oct 14;159(1):69-78 PMID: 12379802
  26. ARF1.GTP, tyrosine-based signals, and phosphatidylinositol 4,5-bisphosphate constitute a minimal machinery to recruit the AP-1 clathrin adaptor to membranes.
    Mol Biol Cell. 2002 Oct;13(10):3672-82 PMID: 12388765
  27. Tyrosine-based endocytic motifs stimulate oligomerization of AP-2 adaptor complexes.
    Eur J Cell Biol. 2002 Dec;81(12):647-53 PMID: 12553665
  28. A kinetic proof-reading mechanism for protein sorting.
    Traffic. 2003 Feb;4(2):65-73 PMID: 12559033
  29. EpsinR: an ENTH domain-containing protein that interacts with AP-1.
    Mol Biol Cell. 2003 Feb;14(2):625-41 PMID: 12589059
  30. HIV-1 Nef stabilizes the association of adaptor protein complexes with membranes.
    J Biol Chem. 2003 Mar 7;278(10):8725-32 PMID: 12486136
  31. AP-1 binding to sorting signals and release from clathrin-coated vesicles is regulated by phosphorylation.
    J Cell Biol. 2003 Mar 3;160(5):699-708 PMID: 12604586
  32. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature.
    Nature. 2003 Dec 4;426(6966):563-6 PMID: 14654841
  33. Gamma-COP appendage domain - structure and function.
    Traffic. 2004 Feb;5(2):79-88 PMID: 14690497
  34. Arf GAPs: multifunctional proteins that regulate membrane traffic and actin remodelling.
    Cell Signal. 2004 Apr;16(4):401-13 PMID: 14709330
  35. The ArfGAP Glo3 is required for the generation of COPI vesicles.
    Mol Biol Cell. 2004 Sep;15(9):4064-72 PMID: 15254269
  36. A general procedure for the preparation of highly active eukaryotic ribosomes and ribosomal subunits.
    Methods Enzymol. 1974;30:368-87 PMID: 4850210
  37. Purification and properties of a new clathrin assembly protein.
    EMBO J. 1986 Dec 1;5(12):3143-9 PMID: 3816757
  38. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane.
    EMBO J. 1988 Apr;7(4):919-29 PMID: 3402440
  39. Subunit interaction and function of clathrin-coated vesicle adaptors from the Golgi and the plasma membrane.
    J Biol Chem. 1991 Apr 25;266(12):7910-8 PMID: 1902231
  40. Hydrolysis of bound GTP by ARF protein triggers uncoating of Golgi-derived COP-coated vesicles.
    J Cell Biol. 1993 Dec;123(6 Pt 1):1365-71 PMID: 8253837
  41. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling.
    Cell. 1994 Sep 9;78(5):751-60 PMID: 8087843
  42. Myristoylation of ADP-ribosylation factor 1 facilitates nucleotide exchange at physiological Mg2+ levels.
    J Biol Chem. 1995 Jan 20;270(3):1337-41 PMID: 7836400
  43. Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment.
    J Biol Chem. 1995 Mar 3;270(9):4933-42 PMID: 7876268
  44. Role of auxilin in uncoating clathrin-coated vesicles.
    Nature. 1995 Dec 7;378(6557):632-5 PMID: 8524399
  45. The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization.
    Science. 1995 Dec 22;270(5244):1999-2002 PMID: 8533093
  46. In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting.
    EMBO J. 1996 Jun 3;15(11):2893-9 PMID: 8654387
  47. Comparative activity of ADP-ribosylation factor family members in the early steps of coated vesicle formation on rat liver Golgi membranes.
    J Biol Chem. 1997 Feb 14;272(7):4141-8 PMID: 9020126
  48. The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1.
    EMBO J. 1997 Dec 15;16(24):7305-16 PMID: 9405360
  49. Reversible dissociation of coatomer: functional characterization of a beta/delta-coat protein subcomplex.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2140-5 PMID: 9482852
  50. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes.
    Cell. 1998 Apr 17;93(2):263-75 PMID: 9568718
  51. A function for the AP3 coat complex in synaptic vesicle formation from endosomes.
    Cell. 1998 May 1;93(3):423-32 PMID: 9590176
  52. ADP-ribosylation factor 1 transiently activates high-affinity adaptor protein complex AP-1 binding sites on Golgi membranes.
    Mol Biol Cell. 1998 Jun;9(6):1323-37 PMID: 9614177
  53. Requirement for both the amino-terminal catalytic domain and a noncatalytic domain for in vivo activity of ADP-ribosylation factor GTPase-activating protein.
    J Biol Chem. 1998 Sep 18;273(38):24786-91 PMID: 9733781
  54. Coatomer, Arf1p, and nucleotide are required to bud coat protein complex I-coated vesicles from large synthetic liposomes.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11199-204 PMID: 9736713
  55. Uptake by COPI-coated vesicles of both anterograde and retrograde cargo is inhibited by GTPgammaS in vitro.
    J Cell Sci. 1998 Oct;111 ( Pt 20):3081-90 PMID: 9739081
  56. Neuroendocrine synaptic vesicles are formed in vitro by both clathrin-dependent and clathrin-independent pathways.
    J Cell Biol. 1998 Nov 16;143(4):947-55 PMID: 9817753
  57. Coat assembly directs v-SNARE concentration into synthetic COPII vesicles.
    Mol Cell. 1998 Nov;2(5):703-8 PMID: 9844642
  58. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors.
    Cell. 1999 Feb 19;96(4):495-506 PMID: 10052452
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2005-10-00
Epub
2005-00-10
Pages
4745-54
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1237080
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com