title: HOPS prevents the disassembly of trans-SNARE complexes by Sec17p/Sec18p during membrane fusion.
abstract: SNARE-dependent membrane fusion requires the disassembly of cis-SNARE complexes (formed by SNAREs anchored to one membrane) followed by the assembly of trans-SNARE complexes (SNAREs anchored to two apposed membranes). Although SNARE complex disassembly and assembly might be thought to be opposing reactions, the proteins promoting disassembly (Sec17p/Sec18p) and assembly (the HOPS complex) work synergistically to support fusion. We now report that trans-SNARE complexes formed during vacuole fusion are largely associated with Sec17p. Using a reconstituted proteoliposome fusion system, we show that trans-SNARE complex, like cis-SNARE complex, is sensitive to Sec17p/Sec18p mediated disassembly. Strikingly, HOPS inhibits the disassembly of SNARE complexes in the trans-, but not in the cis-, configuration. This selective HOPS preservation of trans-SNARE complexes requires HOPS:SNARE recognition and is lost when the apposed bilayers are dissolved in Triton X-100; it is also observed during fusion of isolated vacuoles. HOPS thus directs the Sec17p/Sec18p chaperone system to maximize functional trans-SNARE complex for membrane fusion, a new role of tethering factors during membrane traffic.
authors.affiliation: Department of Biochemistry, Dartmouth Medical School, Hanover, NH, USA.
authors.forename: Hao
authors.initials: H
authors.lastname: Xu
authors.forename: Youngsoo
authors.initials: Y
authors.lastname: Jun
authors.forename: James
authors.initials: J
authors.lastname: Thompson
authors.forename: John
authors.initials: J
authors.lastname: Yates
authors.forename: William
authors.initials: W
authors.lastname: Wickner
mesh_terms: D000251:Adenosine Triphosphatases / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism*; D008561:Membrane Fusion; D008954:Models, Biological; D050600:SNARE Proteins / Q000378:metabolism*; D012441:Saccharomyces cerevisiae / Q000502:physiology*; D029701:Saccharomyces cerevisiae Proteins / Q000378:metabolism*; D052067:Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins / Q000378:metabolism*; D014617:Vacuoles / Q000378:metabolism; D033921:Vesicular Transport Proteins / Q000378:metabolism*
chemical_list: C075137:SEC17 protein, S cerevisiae; D050600:SNARE Proteins; D029701:Saccharomyces cerevisiae Proteins; D052067:Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins; D033921:Vesicular Transport Proteins; D000251:Adenosine Triphosphatases; C064404:SEC18 protein, S cerevisiae
references.citation: J Cell Biol. 2009 Mar 9;184(5):751-64
references.pmid: 19255244
references.citation: Dev Cell. 2007 May;12(5):739-50
references.pmid: 17488625
references.citation: Mol Biol Cell. 2006 Apr;17(4):1845-58
references.pmid: 16452633
references.citation: J Cell Biol. 2000 Mar 20;148(6):1223-29
references.pmid: 10725335
references.citation: J Cell Biol. 2003 Feb 3;160(3):365-74
references.pmid: 12566429
references.citation: Nat Genet. 2004 Apr;36(4):400-4
references.pmid: 15052268
references.citation: J Cell Biol. 1998 Jan 12;140(1):61-9
references.pmid: 9425154
references.citation: J Biol Chem. 1998 Dec 11;273(50):33667-73
references.pmid: 9837952
references.citation: J Cell Biol. 2000 May 29;149(5):1063-72
references.pmid: 10831610
references.citation: EMBO J. 2007 Dec 12;26(24):4935-45
references.pmid: 18007597
references.citation: J Proteome Res. 2003 Jan-Feb;2(1):43-50
references.pmid: 12643542
references.citation: J Cell Sci. 2005 Aug 15;118(Pt 16):3663-73
references.pmid: 16046475
references.citation: Mol Biol Cell. 2010 Jul 1;21(13):2297-305
references.pmid: 20462954
references.citation: Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17626-33
references.pmid: 19826089
references.citation: Proc Natl Acad Sci U S A. 1997 May 27;94(11):5582-7
references.pmid: 9159115
references.citation: J Cell Biol. 2002 May 13;157(4):631-43
references.pmid: 12011112
references.citation: EMBO J. 2008 Aug 6;27(15):2031-42
references.pmid: 18650938
references.citation: J Cell Biol. 2009 May 4;185(3):535-49
references.pmid: 19414611
references.citation: Nucleic Acids Res. 2005 Jan 1;33(Database issue):D378-82
references.pmid: 15608220
references.citation: J Am Soc Mass Spectrom. 1994 Nov;5(11):976-89
references.pmid: 24226387
references.citation: Mol Cell. 1999 Jun;3(6):805-11
references.pmid: 10394369
references.citation: EMBO J. 2002 Mar 15;21(6):1241-7
references.pmid: 11889030
references.citation: Cell. 2007 Jan 12;128(1):183-95
references.pmid: 17218264
references.citation: J Cell Biol. 2002 Apr 1;157(1):79-89
references.pmid: 11916982
references.citation: Chem Rev. 2008 May;108(5):1669-86
references.pmid: 18419164
references.citation: EMBO J. 1996 Jul 1;15(13):3296-305
references.pmid: 8670830
references.citation: Bioinformatics. 2004 Aug 4;20 Suppl 1:i49-54
references.pmid: 15262780
references.citation: EMBO J. 2005 May 18;24(10):1775-86
references.pmid: 15889152
references.citation: Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):1146-50
references.pmid: 12538872
references.citation: J Cell Biol. 2000 Oct 30;151(3):551-62
references.pmid: 11062257
references.citation: J Cell Biol. 1994 Jul;126(1):87-97
references.pmid: 8027189
references.citation: Nat Cell Biol. 2001 Jul;3(7):613-8
references.pmid: 11433291
references.citation: EMBO J. 2004 Jul 21;23(14):2765-76
references.pmid: 15241469
references.citation: Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13551-8
references.pmid: 17699614
references.citation: EMBO J. 1998 May 1;17(9):2494-503
references.pmid: 9564032
references.citation: EMBO J. 2009 Jul 22;28(14):2006-17
references.pmid: 19536132
references.citation: Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9402-7
references.pmid: 10944212
references.citation: Nat Biotechnol. 2001 Mar;19(3):242-7
references.pmid: 11231557
references.citation: Mol Biol Cell. 2008 Jun;19(6):2500-8
references.pmid: 18385512
references.citation: Nat Struct Mol Biol. 2008 Jul;15(7):658-64
references.pmid: 18618939
references.citation: Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):11821-7
references.pmid: 16882731
references.citation: EMBO J. 2006 Apr 19;25(8):1579-89
references.pmid: 16601699
references.citation: Proc Natl Acad Sci U S A. 2007 May 22;104(21):8755-60
references.pmid: 17502611
references.citation: J Biol Chem. 1992 Sep 15;267(26):18665-70
references.pmid: 1526998
references.citation: Cell. 1996 Apr 5;85(1):83-94
references.pmid: 8620540
references.citation: Mol Biol Cell. 2003 Feb;14(2):361-9
references.pmid: 12589039
references.citation: Nature. 1998 Dec 10;396(6711):543-8
references.pmid: 9859990
references.citation: Nature. 2009 Jun 25;459(7250):1091-7
references.pmid: 19458617
references.citation: J Biol Chem. 2002 Dec 13;277(50):48318-24
references.pmid: 12377769
references.citation: Science. 2009 Jan 23;323(5913):474-7
references.pmid: 19164740
references.citation: Curr Protoc Bioinformatics. 2007 Jan;Chapter 13:Unit 13.4
references.pmid: 18428785
references.citation: J Proteome Res. 2002 May-Jun;1(3):211-5
references.pmid: 12645897
references.citation: J Cell Biol. 2004 Dec 20;167(6):1087-98
references.pmid: 15611334
references.citation: Cell Mol Life Sci. 2008 Sep;65(18):2814-32
references.pmid: 18726177
references.citation: J Biol Chem. 2001 Feb 16;276(7):5012-9
references.pmid: 11053422
references.citation: J Proteome Res. 2002 Jan-Feb;1(1):21-6
references.pmid: 12643522
references.citation: EMBO J. 2000 Sep 1;19(17):4577-88
references.pmid: 10970851
references.citation: Mol Biol Cell. 2008 Mar;19(3):776-84
references.pmid: 18094056
references.citation: EMBO J. 1999 Feb 15;18(4):1071-80
references.pmid: 10022848
references.citation: Cell. 1998 Mar 20;92(6):759-72
references.pmid: 9529252
references.citation: J Cell Biol. 2007 Dec 17;179(6):1179-92
references.pmid: 18086915
references.citation: Mol Cell. 1998 Jul;2(1):157-62
references.pmid: 9702203
references.citation: EMBO J. 2001 Oct 15;20(20):5650-6
references.pmid: 11598008
references.citation: FEBS Lett. 2007 May 22;581(11):2125-30
references.pmid: 17316615