Home LiteratureArticle Details
PMID: 9425154 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A vacuolar v-t-SNARE complex, the predominant form in vivo and on isolated vacuoles, is disassembled and activated for docking and fusion.

The Journal of cell biology ·Vol. 140 ·No. 1 ·1998-01-12 ·Pages 61-9

Ungermann C, Nichols BJ, Pelham HR, Wickner W

Abstract

Homotypic vacuole fusion in yeast requires Sec18p (N-ethylmaleimide-sensitive fusion protein [NSF]), Sec17p (soluble NSF attachment protein [alpha-SNAP]), and typical vesicle (v) and target membrane (t) SNAP receptors (SNAREs). We now report that vacuolar v- and t-SNAREs are mainly found with Sec17p as v-t-SNARE complexes in vivo and on purified vacuoles rather than only transiently forming such complexes during docking, and disrupting them upon fusion. In the priming reaction, Sec18p and ATP dissociate this v-t-SNARE complex, accompanied by the release of Sec17p. SNARE complex structure governs each functional aspect of priming, as the v-SNARE regulates the rate of Sec17p release and, in turn, Sec17p-dependent SNARE complex disassembly is required for independent function of the two SNAREs. Sec17p physically and functionally interacts largely with the t-SNARE. (a) Antibodies to the t-SNARE, but not the v-SNARE, block Sec17p release. (b) Sec17p is associated with the t-SNARE in the absence of v-SNARE, but is not bound to the v-SNARE without t-SNARE. (c) Vacuoles with t-SNARE but no v-SNARE still require Sec17p/Sec18p priming, whereas their fusion partners with v-SNARE but no t-SNARE do not. Sec18p thus acts, upon ATP hydrolysis, to disassemble the v-t-SNARE complex, prime the t-SNARE, and release the Sec17p to allow SNARE participation in docking and fusion. These studies suggest that the analogous ATP-dependent disassembly of the 20-S complex of NSF, alpha-SNAP, and v- and t-SNAREs, which has been studied in detergent extracts, corresponds to the priming of SNAREs for docking rather than to the fusion of docked membranes.

MeSH Terms
Adenosine Triphosphatases Alkaline Phosphatase/metabolism Antibodies Carrier Proteins/isolation & purification,metabolism Fungal Proteins/isolation & purification,metabolism Kinetics Membrane Fusion Membrane Proteins/isolation & purification,metabolism Models, Biological Protein Binding Qb-SNARE Proteins Saccharomyces cerevisiae/physiology,ultrastructure Saccharomyces cerevisiae Proteins Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins Vacuoles/physiology,ultrastructure Vesicle-Associated Membrane Protein 3 Vesicular Transport Proteins
Chemicals
Antibodies Carrier Proteins Fungal Proteins Membrane Proteins Qb-SNARE Proteins SEC17 protein, S cerevisiae Saccharomyces cerevisiae Proteins Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins VTI1 protein, S cerevisiae Vesicle-Associated Membrane Protein 3 Vesicular Transport Proteins Alkaline Phosphatase Adenosine Triphosphatases SEC18 protein, S cerevisiae
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ungermann C
Department of Biochemistry, Dartmouth Medical School, Hanover, New Hampshire 03755-3844, USA.
Nichols B J
Pelham H R
Wickner W
References (52)
52 references, click to expand
  1. Distinct biochemical requirements for the budding, targeting, and fusion of ER-derived transport vesicles.
    J Cell Biol. 1991 Jul;114(2):219-29 PMID: 1649197
  2. The formation of Golgi stacks from vesiculated Golgi membranes requires two distinct fusion events.
    Cell. 1995 Sep 22;82(6):895-904 PMID: 7553850
  3. Intervacuole exchange in the yeast zygote: a new pathway in organelle communication.
    Science. 1988 Jul 29;241(4865):589-91 PMID: 3041591
  4. ERS-24, a mammalian v-SNARE implicated in vesicle traffic between the ER and the Golgi.
    J Cell Biol. 1997 Jun 2;137(5):1017-28 PMID: 9166403
  5. Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes.
    Cell. 1995 Sep 22;82(6):885-93 PMID: 7553849
  6. SNAP receptors implicated in vesicle targeting and fusion.
    Nature. 1993 Mar 25;362(6418):318-24 PMID: 8455717
  7. Disassembly of the reconstituted synaptic vesicle membrane fusion complex in vitro.
    EMBO J. 1995 May 15;14(10):2317-25 PMID: 7774590
  8. The activity of Golgi transport vesicles depends on the presence of the N-ethylmaleimide-sensitive factor (NSF) and a soluble NSF attachment protein (alpha SNAP) during vesicle formation.
    J Cell Biol. 1992 Sep;118(6):1321-32 PMID: 1522110
  9. High expression of the yeast syntaxin-related Vam3 protein suppresses the protein transport defects of a pep12 null mutant.
    FEBS Lett. 1997 Jul 7;411(1):48-52 PMID: 9247140
  10. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance.
    EMBO J. 1995 Nov 1;14(21):5258-70 PMID: 7489715
  11. Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF).
    J Cell Biol. 1997 Jan 27;136(2):307-17 PMID: 9015302
  12. I2B is a small cytosolic protein that participates in vacuole fusion.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5582-7 PMID: 9159115
  13. The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria.
    Science. 1994 Nov 18;266(5188):1250-3 PMID: 7973708
  14. Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6197-201 PMID: 9177194
  15. SNAREs and NSF in targeted membrane fusion.
    Curr Opin Cell Biol. 1997 Aug;9(4):505-12 PMID: 9261050
  16. An NSF-like ATPase, p97, and NSF mediate cisternal regrowth from mitotic Golgi fragments.
    Cell. 1995 Sep 22;82(6):905-14 PMID: 7553851
  17. Transport vesicle docking: SNAREs and associates.
    Annu Rev Cell Dev Biol. 1996;12:441-61 PMID: 8970734
  18. A possible predocking attachment site for N-ethylmaleimide-sensitive fusion protein. Insights from in vitro endosome fusion.
    J Biol Chem. 1996 Aug 2;271(31):18810-6 PMID: 8702539
  19. Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis.
    J Cell Biol. 1995 Sep;130(5):1063-70 PMID: 7657692
  20. A heterodimer of thioredoxin and I(B)2 cooperates with Sec18p (NSF) to promote yeast vacuole inheritance.
    J Cell Biol. 1997 Jan 27;136(2):299-306 PMID: 9015301
  21. Vacuolar segregation to the bud of Saccharomyces cerevisiae: an analysis of morphology and timing in the cell cycle.
    J Gen Microbiol. 1991 Oct;137(10):2447-54 PMID: 1770360
  22. Biogenesis of the vacuole in Saccharomyces cerevisiae.
    Int Rev Cytol. 1992;139:59-120 PMID: 1428679
  23. The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling.
    J Cell Biol. 1995 Feb;128(4):637-45 PMID: 7860636
  24. A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles.
    Cell. 1994 Sep 23;78(6):937-48 PMID: 7923363
  25. Protein sorting by transport vesicles.
    Science. 1996 Apr 12;272(5259):227-34 PMID: 8602507
  26. t-SNARE activation through transient interaction with a rab-like guanosine triphosphatase.
    Science. 1997 May 23;276(5316):1255-8 PMID: 9157884
  27. A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole.
    J Cell Biol. 1997 Aug 11;138(3):517-29 PMID: 9245783
  28. Coupled ER to Golgi transport reconstituted with purified cytosolic proteins.
    J Cell Biol. 1997 Dec 1;139(5):1097-108 PMID: 9382859
  29. Stages of regulated exocytosis.
    Trends Cell Biol. 1997 Jul;7(7):271-6 PMID: 17708959
  30. Homotypic vacuole fusion requires Sec17p (yeast alpha-SNAP) and Sec18p (yeast NSF).
    EMBO J. 1996 Jul 1;15(13):3296-305 PMID: 8670830
  31. Assembly of the ER to Golgi SNARE complex requires Uso1p.
    J Cell Biol. 1996 Mar;132(5):755-67 PMID: 8603910
  32. G-protein ligands inhibit in vitro reactions of vacuole inheritance.
    J Cell Biol. 1994 Jul;126(1):87-97 PMID: 8027189
  33. 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
  34. Homotypic vacuolar fusion mediated by t- and v-SNAREs.
    Nature. 1997 May 8;387(6629):199-202 PMID: 9144293
  35. N-Ethylmaleimide-sensitive factor acts at a prefusion ATP-dependent step in Ca2+-activated exocytosis.
    J Biol Chem. 1996 Aug 23;271(34):20223-6 PMID: 8702750
  36. 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
  37. Thioredoxin is required for vacuole inheritance in Saccharomyces cerevisiae.
    J Cell Biol. 1996 Mar;132(5):787-94 PMID: 8603912
  38. Vesicle fusion from yeast to man.
    Nature. 1994 Jul 21;370(6486):191-3 PMID: 8028665
  39. MgATP-independent and MgATP-dependent exocytosis. Evidence that MgATP primes adrenal chromaffin cells to undergo exocytosis.
    J Biol Chem. 1989 Apr 5;264(10):5412-9 PMID: 2784433
  40. Synaptic core complex of synaptobrevin, syntaxin, and SNAP25 forms high affinity alpha-SNAP binding site.
    J Biol Chem. 1995 Feb 3;270(5):2213-7 PMID: 7836452
  41. The N-ethylmaleimide-sensitive fusion protein and alpha-SNAP induce a conformational change in syntaxin.
    J Biol Chem. 1995 Jul 14;270(28):16955-61 PMID: 7622514
  42. In vitro reactions of vacuole inheritance in Saccharomyces cerevisiae.
    J Cell Biol. 1992 Dec;119(6):1469-79 PMID: 1334958
  43. Is NSF a fusion protein?
    Trends Cell Biol. 1995 Sep;5(9):335-9 PMID: 14732068
  44. Compartmental organization of Golgi-specific protein modification and vacuolar protein sorting events defined in a yeast sec18 (NSF) mutant.
    J Cell Biol. 1991 Jul;114(2):207-18 PMID: 2071670
  45. Vam3p, a new member of syntaxin related protein, is required for vacuolar assembly in the yeast Saccharomyces cerevisiae.
    J Cell Sci. 1997 Jun;110 ( Pt 11):1299-306 PMID: 9202390
  46. A novel SNARE complex implicated in vesicle fusion with the endoplasmic reticulum.
    EMBO J. 1997 Jun 2;16(11):3017-24 PMID: 9214619
  47. Mechanisms of intracellular protein transport.
    Nature. 1994 Nov 3;372(6501):55-63 PMID: 7969419
  48. Structural changes are associated with soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation.
    J Biol Chem. 1997 Oct 31;272(44):28036-41 PMID: 9346956
  49. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly.
    EMBO J. 1994 Nov 1;13(21):5051-61 PMID: 7957071
  50. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells.
    Cell. 1995 May 19;81(4):571-80 PMID: 7758111
  51. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy.
    Cell. 1997 Aug 8;90(3):523-35 PMID: 9267032
  52. Vesicle fusion in protein transport through the Golgi in vitro does not involve long-lived prefusion intermediates. A reassessment of the kinetics of transport as measured by glycosylation.
    Biochemistry. 1992 Jul 7;31(26):6111-8 PMID: 1320928
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1998-01-12
Pages
61-9
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2132603
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: [email protected]