Membrane fusion: Five lipids, four SNAREs, three chaperones, two nucleotides, and a rab, all dancing in a ring on yeast vacuoles

Annual Review of Cell and Developmental Biology

Volumn 26, Issue , 2010, Pages 115-136

  Wickner, William ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

docking; membrane microdomain; priming

Indexed keywords

CHAPERONE; LIPID; NUCLEOTIDE; RAB PROTEIN; SNARE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

CELL VACUOLE; COLORIMETRY; MEMBRANE FUSION; MOLECULAR DOCKING; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; YEAST CELL; CYTOLOGY; ENDOSOME; LIPID METABOLISM; METABOLISM; SACCHAROMYCES CEREVISIAE;

ENDOSOMES; LIPID METABOLISM; MEMBRANE FUSION; MOLECULAR CHAPERONES; NUCLEOTIDES; RAB GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; VACUOLES;

EID: 77957020175     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-100109-104131     Document Type: Review

References (104)

1. Angers CG, MerzA.2009. HOPS interacts with Apl5atthe vacuole membrane andisrequired for consumptionof AP-3 transport vesicles. Mol. Biol. Cell 20:4563-74
2. 2+-releasing channel. J. Cell Biol. 162:211-22
3. Boeddinghaus C, Merz AJ, Laage R, Ungermann C. 2002. A cycle of Vam7p release from and PtdIns 3-P-dependent rebinding to the yeast vacuole is required for homotypic vacuole fusion. J. Cell Biol. 157:79-89
4. Bowen M, Brunger AT. 2006. Conformation of the synaptobrevin transmembrane domain. Proc. Natl. Acad. Sci. USA 103:8378-83
5. Boya P, Kroemer G. 2008. Lysosomal membrane permeabilization in cell death. Oncogene 27:6434-51
6. Brandhorst D, Zwilling D, Rizzoli SO, Lippert U, Lang T, Jahn R. 2006. Homotypic fusion of early endosomes:SNAREs do not determine fusion specificity. Proc. Natl. Acad. Sci. USA 103:2701-6
7. Brett CL, Plemel RL, Lobinger BT, Vignali M, Fields S, Merz AJ. 2008. Efficient termination of vacuolar RabGTPase signaling requires coordinated action by a GAP and a protein kinase. J. Cell Biol. 182:1141-51
8. Cabrera M, Ostrowicz CW, Mari M, LaGrassa TJ, Reggiori F, Ungermann C. 2009. Vps41 phosphorylationand the Rab Ypt7 control the targeting of the HOPS complex to endosome-vacuole fusion sites. Mol. Biol. Cell 20:1937-48
9. Chan Y-HM, van Lengerich B, Boxer SG. 2009. Effects of linker sequences on vesicle fusion mediated bylipid-anchored oligonucleotides. Proc. Natl. Acad. Sci. USA 106:979-84
10. Chang J, Kim S-A, Lu X, Su Z, Kim SK, Shin Y-K. 2009. Fusion step-specific influence of cholesterol onSNARE-mediated membrane fusion. Biophys. J. 96:1839-46
11. Cheever ML, Sato TK, de Beer T, Kutateladze TG, Emr SD, Overduin M. 2001. Phox domain interactionwith PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3:613-18
12. Collins KM, Thorngren NL, Fratti RA, Wickner WT. 2005. Vacuole SNAREs form distinct complexeswith Sec17p or HOPS to mediate SNARE complex disruption or their assembly for fusion. EMBO J.24:1775-86
13. Collins KM, Wickner WT. 2007. Trans-SNARE complex assembly and yeast vacuole membrane fusion. Proc. Natl. Acad. Sci. USA 104:8755-60
14. Conradt B, Shaw J, Vida T, Emr S, Wickner W. 1992. In vitro reactions of vacuole inheritance in Saccharomycescerevisiae. J. Cell Biol. 119:1469-79
15. Dascher C, Ossig R, Gallwitz D, Schmitt HD. 1991. Identification and structure of four yeast genes (SLY)that are able to suppress the functional loss of YPT1, a member of the RAS superfamily. Mol. Cell Biol.11:872-85
16. Decker B, Wickner W. 2006. Enolase activates homotypic vacuole fusion and protein transport to the vacuolein yeast. J. Biol. Chem. 281:14523-28
17. Dennison SM, Bowen ME, Brunger AT, Lentz BR. 2006. Neuronal SNAREs do not trigger fusion betweensynthetic membranes but do promote PEG-mediated membrane fusion. Biophys. J. 90:1661-75
18. Edsall JT. 1947. The plasma proteins and their fractionation. In Advances in Protein Chemistry, ed. ML Anso,JT Edsall, 9:383-479 . New York: Academic
19. Eitzen G, Thorngren N, Wickner W. 2001. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking. EMBO J. 20:5650-56
20. Eitzen G, Wang L, Thorngren N, Wickner W. 2002. Remodeling of organelle-bound actin is required foryeast vacuole fusion. J. Cell Biol. 158:669-79
21. Eitzen G, Will E, Gallwitz D, Haas A, Wickner W. 2000. Sequential action of two GTPases to promotevacuole docking and fusion. EMBO J. 19:6713-20
22. Engel A, Walter P. 2008. Membrane lysis during biological membrane fusion: collateral damage by misregu-lated fusion machines. J. Cell Biol. 183:181-86
23. Fasshauer D, Sutton RB, Brunger AT, Jahn R. 1998. Conserved structural features of the synaptic fusioncomplex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. USA 95:15781-86
24. Fratti R, Collins KM, Hickey CM, Wickner W. 2007. Stringent 3Q:1R composition of the SNARE 0-layercan be bypassed for fusion by compensatory SNARE mutation or by lipid bilayer modification. J. Biol. Chem. 282:14861-67
25. Fratti R, Jun Y, Merz AJ, Margolis N, Wickner W. 2004. Interdependent assembly of specific "regulatory"lipids and membrane fusion proteins into the vertex ring domainofdocked vacuoles. J. Cell Biol. 167:1087-98
26. Fratti R, Wickner W. 2007. Distinct targeting and fusion functions of the PX- and SNARE-domains of yeastvacuolar Vam7p. J. Biol. Chem. 282:13133-38
27. Fukuda R, McNew JA, Weber T, Parlati F, Engel T, et al. 2000. Functional architecture of an intracellularmembrane t-SNARE. Nature 407:198-202
28. Haas A, Conradt B, Wickner W. 1994. G-protein ligands inhibit in vitro reactions of vacuole inheritance. J. Cell Biol. 126:87-97
29. Haas A, Scheglmann D, Lazar T, Gallwitz D, Wickner W. 1995. The GTPase Ypt7p of Saccharomyces cerevisiaeis required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. EMBO J.14:5258-70
30. Haas A, Wickner W. 1996. Homotypic vacuole fusion requires Sec17p (yeast a-SNAP) and Sec18p (yeastNSF). EMBO J. 15:3296-305
31. Hickey CM, Sroupe C, Wickner W. 2009. The major role of the Rab Ypt7p in vacuole fusion is supportingHOPS membrane association. J. Biol. Chem. 284:16118-25
32. Hickey CM, Wickner W. 2010. HOPS initiates vacuole docking by tethering membranes prior to trans-SNARE pairing. EMBO J. In press
33. Hofmann MW, Peplowska K, Rohde J, Poschner BC, Ungermann C, Langosch D. 2006. Self-interaction of aSNARE transmembrane domain promotes the hemifusion-to-fusion transition. J. Mol. Biol. 364:1048-60
34. James DJ, Khodthong C, Kowalchyk JA, Martin TFJ. 2008. Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J. Cell Biol. 182:355-66
35. Jun Y, Fratti RA, Wickner W. 2004. Diacylglycerol and its formation by phospholipase C regulate Rab- and SNARE-dependent yeast vacuole fusion. J. Biol. Chem. 279:53186-95
36. Jun Y, Thorngren N, Starai V, Fratti R, Collins K, Wickner W. 2006. Reversible, cooperative reactions of yeast vacuole docking. EMBO J. 25:5260-69
37. Jun Y, Wickner W. 2007. Assays of vacuole fusion resolve the stages of docking, lipid mixing, and contentmixing. Proc. Natl. Acad. Sci. USA 104:13010-15
38. Jun Y, Xu H, Thorngren N, Wickner W. 2007. Sec18p and Vam7p remodel trans-SNARE complexes topermit a lipid-anchored R-SNARE to support yeast vacuole fusion. EMBO J. 26:4935-45
39. Kato M, Wickner W. 2001. Ergosterol is required for the Sec18/ATP-dependent priming step of homotypicvacuole fusion. EMBO J. 20:2035-40
40. Kato M, Wickner W. 2003. Vam10p defines a Sec18p-independent step of priming that allows yeast vacuoletethering. Proc. Natl. Acad. Sci. USA 100:6398-403
41. Kleijnen MF, Kirkpatrick DS, Gygi SP. 2007. The ubiquitin-proteasome system regulates membrane fusionof yeast vacuoles. EMBO J. 26:275-87
42. Laage R, Ungermann C. 2001. The N-terminal domain of the t-SNARE Vam3p coordinates priming anddocking in yeast vacuole fusion. Mol. Biol. Cell 12:3375-85
43. La Grassa TJ, Ungermann C. 2005. The vacuolar kinase Yck3 maintains organelle fragmentation by regulatingthe HOPS tethering complex. J. Cell Biol. 168:401-14
44. Lam AD, Tryoen-Toth P, Tsai B, Vitale N, Stuenkel EL. 2008. SNARE-catalyzed fusion events are regulatedby Syntaxin 1A-lipid interactions. Mol. Biol. Cell 19:485-97
45. Laufman O, Kedan A, Hong W, Lev S. 2009. Direct interaction between the COG complex and the SMprotein, Sly1, is required for Golgi SNARE pairing. EMBO J. 28:2006-17
46. Liu S, Wilson KA, Rice-Stitt T, Neiman AM, McNew JA. 2007. In vitro fusion catalyzed by the sporulation-specific t-SNARE light-chain Spo20p is stimulated by phosphatidic acid. Traffic 8:1630-43
47. Mayer A, Scheglmann D, Dove S, Glatz A, Wickner W, Haas A. 2000. Phosphatidylinositol-(4,5)-bisphosphateregulates two steps of homotypic vacuole fusion. Mol. Biol. Cell 11:807-17
48. Mayer A, Wickner W, Haas A. 1996. Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede dockingand fusion of yeast vacuoles. Cell 85:83-94
49. Mayer A, Wickner W. 1997. Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p aftersymmetric priming by Sec18p (NSF). J. Cell Biol. 136:307-17
50. McNew JA, Weber T, Parlati F, Johnston RJ, Melia TJ, et al. 2000. Close is not enough: SNARE-dependentmembrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol.150:105-17
51. Merz AJ, Wickner W. 2004a. Resolution of organelle docking and fusion kinetics in a cell-free assay. Proc. Natl. Acad. Sci. USA 101:11548-53
52. 2+ efflux from the yeast vacuole lumen. J. Cell Biol. 164:195-206
53. Mima J, Hickey C, Xu H, Jun Y, Wickner W. 2008. Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones. EMBO J. 27:2031-42
54. Mima J, Wickner W. 2009a. Multiple roles of phosphoinositides in membrane fusion. Proc. Natl. Acad. Sci. USA 106:16191-96
55. Mima J, Wickner W. 2009b. Complex lipid requirements for SNARE- and SNARE chaperone-dependentmembrane fusion. J. Biol. Chem. 284:27114-22
56. 0 trans-complex formation. EMBO J. 21:259-69
57. Müller O, Johnson DI, Mayer A. 2001. Cdc42p functions at the docking stage of yeast vacuole membranefusion. EMBO J. 20:5657-65
58. Müller O, Neumann H, Bayer MJ, Mayer A. 2003. Role of the Vtc proteins in V-ATPase stability andmembrane trafficking. J. Cell Sci. 116:1107-15
59. NakanishiH,Morishita M, Schwartz CL, ColuccioA,EngebrechtJ,Neiman AM. 2006. PhospholipaseDandthe SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast. J. Cell Sci. 119:1406-15
60. Nichols BJ, Ungermann C, Pelham HRB, Wickner WT, Haas A. 1997. Homotypic vacuolar fusion mediatedby t- and v-SNAREs. Nature 387:199-202
61. Nieva J-L, Goni FM, Alonso A. 1989. Liposome fusion catalytically induced by phospholipase C. Biochemistry 28:7364-67
62. Ohya T, Miaczynska M, Coskun U, Lommer B, Runge A, et al 2009 Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459 1091-97
63. PeplowskaK,Markgraf DF,OstrowiczCW,BangeG,UngermannC.2007.TheCORVET tetheringcomplex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev. Cell 12:739-50
64. Peters C, Andrews PD, Stark MJR, Cesaro-Tadic S, Glatz A, et al. 1999. Control of the terminal step of intracellular membrane fusion by protein phosphatase 1. Science 285:1084-87
65. Peters C, Baars TL, Bühler S, Mayer A. 2004. Mutual control of membrane fission and fusion proteins. Cell 119:667-78
66. Peters C, Bayer MJ, Bühler S, Anderson JS, Mann M, Mayer A. 2001. Trans-complex formation by proteolipidchannels in the terminal phase of membrane fusion. Nature 409:581-88
67. 2+/calmodulin signals the completion of docking and triggers a late step of vacuolefusion. Nature 396:575-80
68. Predescu SA, Predescu DN, Shimizu K, Klein IK, Malik AB. 2005. Cholesterol-dependent syntaxin-4 andSNAP-23 clustering reglates caveolar fusion with the endothelial plasma membrane. J. Biol. Chem.280:37130-38
69. Price A, Seals D, Wickner W, Ungermann C. 2000a. The docking stage of yeast vacuole fusion requires thetransfer of proteins from a cis-SNARE complex to a Rab/Ypt protein. J. Cell Biol. 148:1231-38
70. Price A, Wickner W, Ungermann C. 2000b. Vacuole protein sorting (VPS) proteins needed for transportvesicle budding from the Golgi are also required for the docking step of homotypic vacuole fusion. J. CellBiol. 148:1223-30
71. Reese C, Heise F, Mayer A. 2005. Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 436:410-14
72. Rohde J, Dietrich L, Langosch D, Ungermann C. 2003. The transmembrane domain of Vam3 affects thecomposition of cis- and trans-SNARE complexes to promote homotypic vacuole fusion. J. Biol. Chem.278:1656-62
73. Sato K, WicknerW. 1998. Functional reconstitution of Ypt7p GTPase and a purified vacuole SNARE complex. Science 281:700-2
74. Schwartz ML, Merz A. 2009. Capture and release of partially zipped trans-SNARE complexes on intactorganelles. J. Cell Biol. 185:535-49
75. Seals D, Eitzen G, Margolis N, Wickner W, Price A. 2000. A Ypt/Rab effector complex containing the Sec1homolog Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. USA 97:9402-7
76. Seeley ES, Kato M, Margolis N, Wickner W, Eitzen G. 2002. The genomics of homotypic vacuole fusion. Mol. Biol. Cell 13:782-94
77. Starai V, Jun Y, Wickner W. 2007. Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proc. Natl. Acad. Sci USA 104:13551-58
78. Starai VJ, Thorngren N, Fratti RA, Wickner W. 2005. Ion regulation of homotypic vacuole fusion in Saccha-romyces cerevisiae. J. Biol. Chem. 280:16754-62
79. Starai VJ, Wickner W. 2008. HOPS proofreads the trans-SNARE complex for yeast vacuole fusion. Mol. Biol. Cell 19:2500-8
80. Stroupe C, Collins KM, Fratti RA, Wickner WT. 2006. Purification of active HOPS complex reveals itsaffinities for phosphoinositides and the SNARE Vam7p. EMBO J. 25:1579-89
81. Stroupe C, Hickey CM, Mima J, Burfeind AS, Wickner W. 2009. Minimal membrane docking requirementsrevealed by reconstitution of Rab GTPase-dependent membrane fusion from purified components. Proc. Natl. Acad. Sci. USA 106:17626-33
82. Struck DK, Hoekstra D, Paganoo RE. 1981. Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20:4093-99
83. Thorngren N, Collins K, Fratti R, Wickner W, Merz AJ. 2004. A soluble SNARE drives rapid docking, bypassing ATP and Sec17/18p for vacuole fusion. EMBO J. 23:2765-76
84. Tong J, Borbat PP, Freed JH, Shin Y-K. 2009. A scissors mechanism for stimulation of SNARE-mediatedlipid mixing by cholesterol. Proc. Natl. Acad. Sci. USA 106:5141-46
85. Ungermann C, Nichols BJ, Pelham HRB, Wickner W. 1998. A vacuolar v-t-SNARE complex, the predominant form in vivo and on isolated vacuoles, is disassembled and activated for docking and fusion. J. Cell Biol. 140:61-69
86. Ungermann C, Price A, Wickner W. 2000. A new role for a SNARE protein as a regulator of the Ypt7/Rab-dependent stage of docking. Proc. Natl. Acad. Sci. USA 97:8889-91
87. Ungermann C, Sato K, Wickner W. 1998. Defining the functions of trans-SNARE pairs. Nature 396:543-48
88. Ungermann C, von Mollard GF, Jensen ON, Margolis N, Stevens T, Wickner W. 1999. Three v-SNAREsand two t-SNAREs, present in a pentameric cis-SNARE complex on isolated vacuoles, are essential forhomotypic fusion. J. Cell Biol. 145:1435-42
89. Ungermann C, Wickner W. 1998. Vam7p, a vacuolar SNAP-25 homolog, is required for SNARE complexintegrity and vacuole docking and fusion. EMBO J. 17:3269-76
90. Valdez-Taubas J, Pelham HRB. 2003. Slow diffusion of proteins in the yeast plasma membrane allows polarityto be maintained by endocytic cycling. Curr. Biol. 13:1636-40
91. Vicogne J, Vollenweider D, Smith JR, Huang P, Frohman RA, Pessin JE. 2006. Asymmetric phospholipiddistribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc. Natl. Acad. Sci. USA103:14761-66
92. Villar A-V, Alonso A, Goni FM. 2000. Leaky vesicle fusion induced by phosphatidylinositol-specific phos-pholipase C: observation of mixing of vesicular inner monolayers. Biochemistry 39:14012-18
93. Wada Y, Ohsumi Y, Anraku Y. 1992. Genes for directing vacuolar morphogenesis in Saccharomyces cerevisiae. Isolation and characterization of two classes of vam mutants. J. Biol. Chem. 267:18665-70
94. Wang C-W, Stromhaug PE, Kauffman EJ, Weisman LS, Klionsky DJ. 2003a. Yeast homotypic vacuole fusionrequires the Ccz1-Mon1 complex during the tethering/docking stage. J. Cell Biol. 163:973-85
95. Wang L, Merz A, Collins K, Wickner W. 2003b. Hierarchy of protein assembly at the vertex ring domain foryeast vacuole docking and fusion. J. Cell Biol. 160:365-74
96. Wang L, Seeley S, Wickner W, Merz A. 2002. Vacuole fusion at a ring of vertex docking sites leaves membrane fragments with in the organelle. Cell 108:357-69
97. Wang T, Smith EA, Chapman ER, Weisshaar JC. 2009. Lipid mixing and content release in single-vesicle, SNARE-driven fusion assay with 1-5 ms resolution. Biophys. J. 96:4122-31
98. Wang Y, Dulubova I, Rizo J, Südhof T. 2001. Functional analysis of conserved structural elements in yeastsyntaxin Vam3p. J. Biol. Chem. 276:28598-605
99. WeberT,ZemelmanBV,McNewJA,WestermannB,GmachlM,etal 1998 SNAREpins:minimalmachineryfor membrane fusion. Cell 92 759-72
100. Wichmann H, Hengst L, Gallwitz D. 1992. Endocytosis in yeast: evidence for the involement of a smallGTP-binding protein (Ypt7p). Cell 71:1131-42
101. Wurmser AE, Sato TK, Emr SD. 2000. New component of the vacuolar class C-Vps complex couples nu-cleotide exchange on the Ypt7p GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151:551-62
102. Xu H, Wickner W. 2006. Bem1p is a positive regulator of the homotypic fusion of yeast vacuoles. J. Biol. Chem. 281:27158-66
103. Xu H, Jun Y, Thompson J, Yates J, Wickner W. 2010. HOPS prevents the disassembly of trans-SNAREcomplexes by Sec17p/Sec18p during membrane fusion. EMBO J. 29:1948-60
104. Xu Z, Sato K, Wickner W. 1998. LMA1 binds to vacuoles at Sec18p (NSF), transfers upon ATP hydrolysisto a t-SNARE (Vam3p) complex, and is released during fusion. Cell 93:1125-34