Home LiteratureArticle Details
PMID: 17651732 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Membrane fusion by VAMP3 and plasma membrane t-SNAREs.

Experimental cell research ·Vol. 313 ·No. 15 ·2007-09-10 ·Pages 3198-209

Hu C, Hardee D, Minnear F

Abstract

Pairing of SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) proteins on vesicles (v-SNAREs) and SNARE proteins on target membranes (t-SNAREs) mediates intracellular membrane fusion. VAMP3/cellubrevin is a v-SNARE that resides in recycling endosomes and endosome-derived transport vesicles. VAMP3 has been implicated in recycling of transferrin receptors, secretion of alpha-granules in platelets, and membrane trafficking during cell migration. Using a cell fusion assay, we examined membrane fusion capacity of the ternary complexes formed by VAMP3 and plasma membrane t-SNAREs syntaxin1, syntaxin4, SNAP-23 and SNAP-25. VAMP3 forms fusogenic pairing with t-SNARE complexes syntaxin1/SNAP-25, syntaxin1/SNAP-23 and syntaxin4/SNAP-25, but not with syntaxin4/SNAP-23. Deletion of the N-terminal domain of syntaxin4 enhanced membrane fusion more than two fold, indicating that the N-terminal domain negatively regulates membrane fusion. Differential membrane fusion capacities of the ternary v-/t-SNARE complexes suggest that transport vesicles containing VAMP3 have distinct membrane fusion kinetics with domains of the plasma membrane that present different t-SNARE proteins.

MeSH Terms
Animals COS Cells Cell Membrane/physiology Chlorocebus aethiops Cloning, Molecular Membrane Fusion/physiology Mice Mutation Qa-SNARE Proteins/genetics,metabolism Qb-SNARE Proteins/genetics,metabolism Qc-SNARE Proteins/genetics,metabolism Synaptosomal-Associated Protein 25/genetics,metabolism Vesicle-Associated Membrane Protein 3/genetics,metabolism
Chemicals
Qa-SNARE Proteins Qb-SNARE Proteins Qc-SNARE Proteins Snap23 protein, mouse Synaptosomal-Associated Protein 25 Vesicle-Associated Membrane Protein 3 vesicle-associated membrane protein 3, mouse
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hu Chuan
Department of Physiology and Pharmacology, West Virginia University Health Sciences Center, Morgantown, WV 26506, USA. [email protected]
Hardee Deborah
Minnear Fred
References (51)
51 references, click to expand
  1. Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12565-70 PMID: 10535962
  2. SNAREs--engines for membrane fusion.
    Nat Rev Mol Cell Biol. 2006 Sep;7(9):631-43 PMID: 16912714
  3. Molecular mechanisms of platelet exocytosis: requirements for alpha-granule release.
    Biochem Biophys Res Commun. 2000 Jan 27;267(3):875-80 PMID: 10673384
  4. Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex.
    Nature. 2000 Mar 23;404(6776):355-62 PMID: 10746715
  5. Membrane fusion and exocytosis.
    Annu Rev Biochem. 1999;68:863-911 PMID: 10872468
  6. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors.
    J Cell Biol. 2000 Jul 10;150(1):105-17 PMID: 10893260
  7. Protein kinase C phosphorylation of syntaxin 4 in thrombin-activated human platelets.
    J Biol Chem. 2000 Aug 18;275(33):25286-91 PMID: 10856305
  8. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins.
    Nature. 2000 Sep 14;407(6801):153-9 PMID: 11001046
  9. A genomic perspective on membrane compartment organization.
    Nature. 2001 Feb 15;409(6822):839-41 PMID: 11237004
  10. VAMP3 null mice display normal constitutive, insulin- and exercise-regulated vesicle trafficking.
    Mol Cell Biol. 2001 Mar;21(5):1573-80 PMID: 11238894
  11. SNARE-mediated membrane fusion.
    Nat Rev Mol Cell Biol. 2001 Feb;2(2):98-106 PMID: 11252968
  12. Syntaxin 1A is delivered to the apical and basolateral domains of epithelial cells: the role of munc-18 proteins.
    J Cell Sci. 2001 Sep;114(Pt 18):3323-32 PMID: 11591820
  13. Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5424-9 PMID: 11959998
  14. Subcellular distribution of 3 functional platelet SNARE proteins: human cellubrevin, SNAP-23, and syntaxin 2.
    Blood. 2002 Jun 1;99(11):4006-14 PMID: 12010801
  15. Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion.
    Blood. 2002 Aug 1;100(3):1081-3 PMID: 12130530
  16. SNARE expression and localization in renal epithelial cells suggest mechanism for variability of trafficking phenotypes.
    Am J Physiol Renal Physiol. 2002 Nov;283(5):F1111-22 PMID: 12372788
  17. Fusion of cells by flipped SNAREs.
    Science. 2003 Jun 13;300(5626):1745-9 PMID: 12805548
  18. A role for Sec1/Munc18 proteins in platelet exocytosis.
    Biochem J. 2003 Aug 15;374(Pt 1):207-17 PMID: 12773094
  19. Control of eukaryotic membrane fusion by N-terminal domains of SNARE proteins.
    Biochim Biophys Acta. 2003 Aug 18;1641(2-3):111-9 PMID: 12914952
  20. Granule stores from cellubrevin/VAMP-3 null mouse platelets exhibit normal stimulus-induced release.
    Blood. 2003 Sep 1;102(5):1716-22 PMID: 12738662
  21. Identification and characterization of Snapin as a ubiquitously expressed SNARE-binding protein that interacts with SNAP23 in non-neuronal cells.
    Biochem J. 2003 Oct 15;375(Pt 2):433-40 PMID: 12877659
  22. A transient N-terminal interaction of SNAP-25 and syntaxin nucleates SNARE assembly.
    J Biol Chem. 2004 Feb 27;279(9):7613-21 PMID: 14665625
  23. Imaging single membrane fusion events mediated by SNARE proteins.
    Proc Natl Acad Sci U S A. 2004 May 11;101(19):7311-6 PMID: 15123811
  24. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes.
    Immunity. 2004 May;20(5):577-88 PMID: 15142526
  25. Inhibitors of the biosynthesis and processing of N-linked oligosaccharides.
    CRC Crit Rev Biochem. 1984;16(1):21-49 PMID: 6232113
  26. SNAP receptors implicated in vesicle targeting and fusion.
    Nature. 1993 Mar 25;362(6418):318-24 PMID: 8455717
  27. Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein.
    Nature. 1993 Jul 22;364(6435):346-9 PMID: 8332193
  28. The syntaxin family of vesicular transport receptors.
    Cell. 1993 Sep 10;74(5):863-73 PMID: 7690687
  29. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion.
    Cell. 1993 Nov 5;75(3):409-18 PMID: 8221884
  30. Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells.
    J Cell Biol. 1994 Jun;125(5):1015-24 PMID: 8195285
  31. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly.
    EMBO J. 1994 Nov 1;13(21):5051-61 PMID: 7957071
  32. Mechanisms of intracellular protein transport.
    Nature. 1994 Nov 3;372(6501):55-63 PMID: 7969419
  33. Cellubrevin and synaptobrevins: similar subcellular localization and biochemical properties in PC12 cells.
    J Cell Biol. 1995 Apr;129(1):219-31 PMID: 7698987
  34. Cellubrevin is a resident protein of insulin-sensitive GLUT4 glucose transporter vesicles in 3T3-L1 adipocytes.
    J Biol Chem. 1995 Apr 7;270(14):8233-40 PMID: 7713930
  35. Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles.
    Cell. 1996 Apr 5;85(1):83-94 PMID: 8620540
  36. Identification of a novel syntaxin- and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues.
    J Biol Chem. 1996 Jun 7;271(23):13300-3 PMID: 8663154
  37. Regulated secretion in platelets: identification of elements of the platelet exocytosis machinery.
    Blood. 1997 Aug 15;90(4):1490-500 PMID: 9269766
  38. SNAREpins: minimal machinery for membrane fusion.
    Cell. 1998 Mar 20;92(6):759-72 PMID: 9529252
  39. Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p.
    Nat Struct Biol. 1998 Sep;5(9):793-802 PMID: 9731774
  40. Three-dimensional structure of an evolutionarily conserved N-terminal domain of syntaxin 1A.
    Cell. 1998 Sep 18;94(6):841-9 PMID: 9753330
  41. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution.
    Nature. 1998 Sep 24;395(6700):347-53 PMID: 9759724
  42. Proteins of the exocytotic core complex mediate platelet alpha-granule secretion. Roles of vesicle-associated membrane protein, SNAP-23, and syntaxin 4.
    J Biol Chem. 1999 Jan 22;274(4):2492-501 PMID: 9891020
  43. Folding intermediates of SNARE complex assembly.
    Nat Struct Biol. 1999 Feb;6(2):117-23 PMID: 10048921
  44. SNARE interactions are not selective. Implications for membrane fusion specificity.
    J Biol Chem. 1999 Feb 26;274(9):5649-53 PMID: 10026182
  45. Human platelets contain SNARE proteins and a Sec1p homologue that interacts with syntaxin 4 and is phosphorylated after thrombin activation: implications for platelet secretion.
    Blood. 1999 Apr 15;93(8):2617-26 PMID: 10194441
  46. Phosphorylation of SNAP-23 regulates exocytosis from mast cells.
    J Biol Chem. 2005 Feb 25;280(8):6610-20 PMID: 15611044
  47. Inhibition of SNARE-mediated membrane traffic impairs cell migration.
    Exp Cell Res. 2005 Apr 15;305(1):63-73 PMID: 15777788
  48. Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion.
    Proc Natl Acad Sci U S A. 2005 May 3;102(18):6362-7 PMID: 15851685
  49. v-SNAREs control exocytosis of vesicles from priming to fusion.
    EMBO J. 2005 Jun 15;24(12):2114-26 PMID: 15920476
  50. A role for the phagosome in cytokine secretion.
    Science. 2005 Dec 2;310(5753):1492-5 PMID: 16282525
  51. nSec1 binds a closed conformation of syntaxin1A.
    J Cell Biol. 2000 Jan 24;148(2):247-52 PMID: 10648557
Article Info
Journal
Experimental cell research
Abbr.
Exp Cell Res
ISSN
0014-4827
DOI
10.1016/j.yexcr.2007.06.008
Email
[email protected]
Published
2007-09-10
Epub
2007-00-27
Pages
3198-209
Language
English
Region
United States
NLM ID
0373226
PMCID
PMC2696983
Subset
IM
Grants
NHLBI NIH HHS · R01 HL068079 · United States
NHLBI NIH HHS · R01 HL068079-01A1 · United States
NHLBI NIH HHS · HL-68079 · United States
External Links
PubMed source DOI: 10.1016/j.yexcr.2007.06.008 PMC Full Text View journal details
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: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2