Membranes linked by trans-SNARE complexes require lipids prone to non-bilayer structure for progression to fusion

eLife

Volumn 2014, Issue 3, 2014, Pages

  Zick, Michael ^a   Stroupe, Christopher ^b,c   Orr, Amy ^a   Douville, Deborah ^a   Wickner, William T ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; ERGOSTEROL; PHOSPHATIDYLETHANOLAMINE; PROTEOLIPOSOME; RAB PROTEIN; SNARE PROTEIN; ADENOSINE TRIPHOSPHATASE; ARTIFICIAL MEMBRANE; MEMBRANE LIPID; PROTEIN BINDING; PROTEOLIPID; PROTEOLIPOSOMES; Q SNARE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SEC17 PROTEIN, S CEREVISIAE; SEC18 PROTEIN, S CEREVISIAE; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; SYNAPTOBREVIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CELL VACUOLE; EXTRACTION; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOBLOTTING; LYSOSOME; MEMBRANE FUSION; POLYACRYLAMIDE GEL ELECTROPHORESIS; ARTIFICIAL MEMBRANE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; TIME FACTOR;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; MEMBRANE FUSION; MEMBRANE LIPIDS; MEMBRANES, ARTIFICIAL; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEOLIPIDS; Q-SNARE PROTEINS; R-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS; TIME FACTORS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 84898767505     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01879     Document Type: Article

References (56)

1. Araç D, Chen X, Khant HA, Ubach J, Ludtke SJ, Kikkawa M, Johnson AE, Chiu W, Südhof TC, Rizo J. 2006. Close membrane-membrane proximity induced by Ca(2+)-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nature Structure Molecular Biology 13:209-217. doi: 10.1038/nsmb1056.
2. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37:911-917. doi: 10.1139/o59-099.
3. Chapman ER, Davis AF. 1998. Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. Journal of Biological Chemistry 273:13995-14001. doi: 10.1074/jbc.273.22.13995.
4. Cheever ML, Sato TK, de Beer T, Kutateladze TG, Emr SD, Overduin M. 2001. Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nature Cell Biology 3:613-618. doi: 10.1038/35083000.
5. Chernomordik LV, Frolov VA, Leikina E, Bronk P, Zimmerberg J. 1998. The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. The Journal of Cell Biology 140:1369-1382. doi: 10.1083/jcb.140.6.1369.
6. Collins KM, Wickner W. 2007. Trans-SNARE complex assembly and yeast vacuole membrane fusion. Proceedings of the National Academy of Sciences of the United States of America 104:8755-8760. doi: 10.1073/pnas.0702290104.
7. Diao J, Grob P, Cipriano DJ, Kyoung M, Zhang Y, Shah S, Nguyen A, Padolina M, Srivastava A, Vrljic M, Shah A, Nogales E, Chu S, Brunger AT. 2012. Synaptic proteins promote calcium-triggered fast transition from point contact to full fusion. Elife 1:e00109. doi: 10.7554/eLife.00109.
8. Domanska MK, Kiessling V, Tamm LK. 2010. Docking and fast fusion of synaptobrevin vesicles depends on the lipid compositions of the vesicle and the acceptor SNARE complex-containing target membrane. Biophysical Journal 99:2936-2946. doi: 10.1016/j.bpj.2010.09.011.
9. Fasshauer D, Sutton RB, Brunger AT, Jahn R. 1998. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs. Proceedings of the National Academy of Sciences of the United States of America 95:15781-15786. doi: 10.1073/pnas.95.26.15781.
10. Fratti RA, Jun Y, Merz AJ, Margolis N, Wickner W. 2004. Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. The Journal of Cell Biology 167:1087-1098. doi: 10.1083/jcb.200409068.
11. Fukuda R, McNew JA, Weber T, Parlati F, Engel T, Nickel W, Rothman JE, Söllner TH. 2000. Functional architecture of an intracellular membrane t-SNARE. Nature 407:198-202. doi: 10.1038/35025084.
12. Gaudin Y. 2000. Rabies virus-induced membrane fusion pathway. The Journal of Cell Biology 150:601-612. doi: 10.1083/jcb.150.3.601.
13. Grosshans BL, Ortiz D, Novick P. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proceedings of the National Academy of Sciences of the United States of America 103:11821-11827. doi: 10.1073/pnas.0601617103.
14. Haas A. 1995. A quantitative assay to measure homotypic vacuole fusion in vitro. Methods in Cell Science 17:283-294. doi: 10.1007/BF00986234.
15. Haas A, Wickner W. 1996. Homotypic vacuole fusion requires Sec17p (yeast alpha-SNAP) and Sec18p (yeast NSF). The EMBO Journal 15:3296-3305.
16. Hickey CM, Stroupe C, Wickner W. 2009. The major role of the Rab Ypt7p in vacuole fusion is supporting HOPS membrane association. Journal of Biological Chemistry 284:16118-16125. doi: 10.1074/jbc.M109.000737.
17. Hickey C, Wickner W. 2010. HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Molecular Biology of the Cell 21:2297-2305. doi: 10.1091/mbc.E10-01-0044.
18. Jahn R, Scheller RH. 2006. SNAREs-engines for membrane fusion. Nature Reviews Molecular Cell Biology 7:631-643. doi: 10.1038/nrm2002.
19. Jun Y, Fratti RA, Wickner W. 2004. Diacylglycerol and its formation by phospholipase C regulate Rab-and SNARE-dependent yeast vacuole fusion. Journal of Biological Chemistry 279:53186-53195. doi: 10.1074/jbc.M411363200.
20. Jun Y, Xu H, Thorngren N, Wickner W. 2007. Sec18p and Vam7p remodel trans-SNARE complexes to permit a lipid-anchored R-SNARE to support yeast vacuole fusion. The EMBO Journal 26:4935-4945. doi: 10.1038/sj.emboj.7601915.
21. Karunakaran V, Wickner W. 2013. Fusion proteins and select lipids cooperate as membrane receptors for the soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) Vam7p. Journal of Biological Chemistry 288:28557-28566. doi: 10.1074/jbc.A113.484410.
22. Kato M, Wickner W. 2001. Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. The EMBO Journal 20:4035-4040. doi: 10.1093/emboj/20.15.4035.
23. Kyoung M, Srivastava A, Zhang Y, Diao J, Vrljic M, Grob P, Nogales E, Chu S, Brunger AT. 2011. In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proceedings of the National Academy of Sciences of the United States of America 108:E304-E313. doi: 10.1073/pnas.1107900108.
24. Lee SA, Kovacs J, Stahelin RV, Cheever ML, Overduin M, Setty TG, Burd CG, Cho W, Kutateladze TG. 2006. Molecular mechanism of membrane docking by the Vam7p PX domain. Journal of Biological Chemistry 281:37091-37101. doi: 10.1074/jbc.M608610200.
25. Li F, Pincet F, Perez E, Eng WS, Melia TJ, Rothman JE, Tareste D. 2007. Energetics and dynamics of SNAREpin folding across lipid bilayers. Nature Structural & Molecular Biology 14:890-896. doi: 10.1038/nsmb1310.
26. Mayer A, Scheglmann D, Dove S, Glatz A, Wickner W, Haas A. 2000. Phosphatidylinositol 4,5-bisphosphate regulates two steps of homotypic vacuole fusion. Molecular Biology of the Cell 11:807-817. doi: 10.1091/mbc.11.3.807.
27. Mayer A, Wickner W, Haas A. 1996. Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85:83-94. doi: 10.1016/S0092-8674(00)81084-3.
28. McNew JA, Weber T, Engelman DM, Söllner TH, Rothman JE. 1999. The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion. Molecular Cell 4:415-421. doi: 10.1016/S1097-2765(00)80343-3.
29. Merz AJ, Wickner W. 2004. Trans-SNARE interactions elicit Ca2+ efflux from the yeast vacuole lumen. The Journal of Cell Biology 164:195-206. doi: 10.1083/jcb.200310105.
30. Mima J, Wickner W. 2009. Phosphoinositides and SNARE chaperones synergistically assemble and remodel SNARE complexes for membrane fusion. Proceedings of the National Academy of Sciences of the United States of America 106:16191-16196. doi: 10.1073/pnas.0908694106.
31. Mima J, Hickey CM, Xu H, Jun Y, Wickner W. 2008. Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones. The EMBO Journal 27:2031-2042. doi: 10.1038/emboj.2008.139.
32. Nichols BJ, Ungermann C, Pelham HR, Wickner WT, Haas A. 1997. Homotypic vacuolar fusion mediated by t-and v-SNAREs. Nature 387:199-202. doi: 10.1038/387199a0.
33. Pécheur E-I, Martin I, Maier O, Bakowsky U, Ruysschaert J-M, Hoekstra D. 2002. Phospholipid species act as modulators in p97/p47-mediated fusion of Golgi membranes. Biochemistry 41:9813-9823. doi: 10.1021/bi0259195.
34. Schneiter R, Brugger B, Sandhoff R, Zellnig G, Leber A, Lampl M, Athenstaedt K, Hrastnik C, Eder S, Daum G, Paltauf F, Wieland FT, Kohlwein SD. 1999. Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species in route to the plasma membrane. The Journal of Cell Biology 146:741-754. doi: 10.1083/jcb.146.4.741.
35. Schwartz ML, Merz AJ. 2009. Capture and release of partially zipped trans-SNARE complexes on intact organelles. The Journal of Cell Biology 185:535-549. doi: 10.1083/jcb.200811082.
36. Seals DF, Eitzen G, Margolis N, Wickner WT, Price A. 2000. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proceedings of the National Academy of Sciences of the United States of America 97:9402-9407. doi: 10.1073/pnas.97.17.9402.
37. Seeley ES, Kato M, Margolis N, Wickner W, Eitzen G. 2002. Genomic analysis of homotypic vacuole fusion. Molecular Biology of the Cell 13:782-794. doi: 10.1091/mbc.01-10-0512.
38. Starai VJ, Jun Y, Wickner W. 2007. Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proceedings of the National Academy of Sciences of the United States of America 104:13551-13558. doi: 10.1073/pnas.0704741104.
39. Stroupe C, Collins KM, Fratti RA, Wickner W. 2006. Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. The EMBO Journal 25:1579-1589. doi: 10.1038/sj.emboj.7601051.
40. Stroupe C, Hickey CM, Mima J, Burfeind AS, Wickner W. 2009. Minimal membrane docking requirements revealed by reconstitution of Rab GTPase-dependent membrane fusion from purified components. Proceedings of the National Academy of Sciences of the United States of America 106:17626-17633. doi: 10.1073/pnas.0903801106.
41. Wada Y, Ohsumi Y, Anraku Y. 1992. Genes for directing vacuolar morphogenesis in Saccharomyces cerevisiae. I. Isolation and characterization of two classes of vam mutants. Journal of Biological Chemistry 267:18665-18670.
42. Wang L, Merz AJ, Collins KM, Wickner W. 2003. Hierarchy of protein assembly at the vertex ring domain for yeast vacuole docking and fusion. The Journal of Cell Biology 160:365-374. doi: 10.1083/jcb.200209095.
43. Wang L, Seeley ES, Wickner W, Merz AJ. 2002. Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle. Cell 108:357-369. doi: 10.1016/S0092-8674(02)00632-3.
44. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Söllner TH, Rothman JE. 1998. SNAREpins: minimal machinery for membrane fusion. Cell 92:759-772. doi: 10.1016/S0092-8674(00)81404-X.
45. White J, Helenius A. 1980. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proceedings of the National Academy of Sciences of the United States of America 77:3273-3277. doi: 10.1073/pnas.77.6.3273.
46. Wickner W, Schekman R. 2008. Membrane fusion. Nature Structural & Molecular Biology 15:658-664. doi: 10.1038/nsmb.1451.
47. Wickner W. 2010. Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. The Annual Review of Cell and Developmental Biology 26:115-136. doi: 10.1146/annurev-cellbio-100109-104131.
48. Wurmser AE, Sato TK, Emr SD. 2000. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. The Journal of Cell Biology 151:551-562. doi: 10.1083/jcb.151.3.551.
49. Xu H, Wickner W. 2010. Phosphoinositides function asymmetrically for membrane fusion, promoting tethering and 3Q-SNARE subcomplex assembly. Journal of Biological Chemistry 285:39359-39365. doi: 10.1074/jbc.M110.183111.
50. Xu H, Zick M, Wickner WT, Jun Y. 2011. A lipid-anchored SNARE supports membrane fusion. Proceedings of the Montana Academy of Sciences 108:17325-17330. doi: 10.1073/pnas.1113888108.
51. Xue M, Ma C, Craig TK, Rosenmund C, Rizo J. 2008. The Janus-faced nature of the C(2)B domain is fundamental for synaptotagmin-1 function. Nature Structural & Molecular Biology 15:1160-1168. doi: 10.1038/nsmb.1508.
52. Zhang X, Rizo J, Südhof TC. 1998. Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I. Biochemistry 37:12395-12403. doi: 10.1021/bi9807512.
53. Zhou P, Bacaj T, Yang X, Pang ZP, Südhof TC. 2013. Lipid-anchored SNAREs lacking transmembrane regions fully support membrane fusion during neurotransmitter release. Neuron 80:470-483. doi: 10.1016/j.neuron.2013.09.010.
54. Zick M, Wickner W. 2013. The tethering complex HOPS catalyzes assembly of the soluble SNARE Vam7 into fusogenic trans-SNARE complexes. Molecular Biology of the Cell 24:3746-3753. doi: 10.1091/mbc.E13-07-0419.
55. Zinser E, Sperka-Gottlieb CD, Fasch EV, Kohlwein SD, Paltauf F, Daum G. 1991. Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. Journal of Bacteriology 173:2026-2034.
56. Zucchi PC, Zick M. 2011. Membrane fusion catalyzed by a Rab, SNAREs, and SNARE chaperones is accompanied by enhanced permeability to small molecules and by lysis. Molecular Biology of the Cell 22:4635-4646. doi: 10.1091/mbc.E11-08-0680.