Vacuole membrane fusion: V0 functions after trans-SNARE pairing and is coupled to the Ca2+-releasing channel

Journal of Cell Biology

Volumn 162, Issue 2, 2003, Pages 211-222

  Bayer, Martin J ^a   Reese, Christoph ^a   Bühler, Susanne ^a   Peters, Christopher ^a   Mayer, Andreas ^a  

^a FRIEDRICH MIESCHER LABORATORY OF THE MAX PLANCK SOCIETY   (Germany)

Author keywords

Calcium; Membrane fusion; SNAREs; V ATPase; Vacuoles

Indexed keywords

ANTIBODY; CALCIUM; CALCIUM CHANNEL; MEMBRANE LIPID; MEMBRANE PROTEIN; PROTEIN SUBUNIT; PROTEOLIPID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SNARE PROTEIN; UNCLASSIFIED DRUG; VPH1P PROTEIN;

ARTICLE; CALCIUM TRANSPORT; CELL VACUOLE; CONFORMATION; MEMBRANE FUSION; MODEL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; YEAST;

ACRIDINE ORANGE; CALCIUM; FLUORESCENT DYES; KINETICS; MEMBRANE FUSION; MEMBRANE PROTEINS; MUTATION; PROTON-TRANSLOCATING ATPASES; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

FUNGI;

EID: 0043174011     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200212004     Document Type: Article

References (94)

1. Adachi, I., K. Puopolo, N. Marquez-Sterling, H. Arai, and M. Forgac. 1990. Dissociation, cross-linking, and glycosylation of the coated vesicle proton pump. J. Biol. Chem. 265:967-973.
2. Adamo, J.E., G. Rossi, and P. Brennwald. 1999. The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol. Biol. Cell. 10:4121-4133.
3. Adamo, J.E., J.J. Moskow, A.S. Gladfelter, D. Viterbo, D.J. Lew, and P.J. Brennwald. 2001. Yeast Cdc42 functions at a late step in exocytosis, specifically during polarized growth of the emerging bud. J. Cell Biol. 155:581-592.
4. Adler, E.M., G.J. Augustine, S.N. Duffy, and M.P. Charlton. 1991. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11:1496-1507.
5. Arai, H., S. Pink, and M. Forgac. 1989. Interaction of anions and ATP with the coated vesicle proton pump. Biochemistry. 28:3075-3082.
6. Boeddinghaus, C., A.J. Merz, R. Laage, and C. Ungermann. 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. 157:79-90.
7. Chapman, E.R. 2002. Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat. Rev. Mol. Cell Biol. 3:498-508.
8. Cheever, M.L., T.K. Sato, T. de Beer, T.G. Kutateladze, S.D. Emr, and M. Overduin. 2001. Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3:613-618.
9. Chen, Y.A., and R.H. Scheller. 2001. SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2:98-106.
10. Conchon, S., X. Cao, C. Barlowe, and H.R. Pelham. 1999. Got1p and Sft2p: membrane proteins involved in traffic to the Golgi complex. EMBO J. 18:3934-3946.
11. Conradt, B., J. Shaw, T. Vida, S. Emr, and W. Wickner. 1992. In vitro reactions of vacuole inheritance in Saccharomyces cerevisiae. J. Cell Biol. 119:1469-1479.
12. Conradt, B., A. Haas, and W. Wickner. 1994. Determination of four biochemically distinct, sequential stages during vacuole inheritance in vitro. J. Cell Biol. 126:99-110.
13. Cunningham, K.W., and G.R. Fink. 1994. Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases. J. Cell Biol. 124:351-363.
14. Drose, S., and K. Altendorf. 1997. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 200:1-8.
15. Eitzen, G., N. Thorngren, and W. Wickner. 2001. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking. EMBO J. 20:5650-5656.
16. Eitzen, G., L. Wang, N. Thorngren, and W. Wickner. 2002. Remodeling of organelle-bound actin is required for yeast vacuole fusion. J. Cell Biol. 158:669-679.
17. Fernandez-Chacon, R., and T.C. Sudhof. 2000. Novel SCAMPs lacking NPF repeats: ubiquitous and synaptic vesicle-specific forms implicate SCAMPs in multiple membrane-trafficking functions. J. Neurosci. 20:7941-7950.
18. Fernandez-Chacon, R., M. Achiriloaie, R. Janz, J.P. Albanesi, and T.C. Sudhof. 2000. SCAMP1 function in endocytosis. J. Biol. Chem. 275:12752-12756.
19. Fernandez-Chacon, R., A. Konigstorfer, S.H. Gerber, J. Garcia, M.F. Matos, C.F. Stevens, N. Brose, J. Rizo, C. Rosenmund, and T.C. Sudhof. 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature. 410:41-49.
20. 2+ homeostasis is a constitutive function of the V-ATPase in Saccharomyces cerevisiae. J. Biol. Chem. 275:38245-38253.
21. Gluck, S., S. Kelly, and Q. Al-Awqati. 1982. The proton translocating ATPase responsible for urinary acidification. J. Biol. Chem. 257:9230-9233.
22. Gotte, M., T. Lazar, J.S. Yoo, D. Scheglmann, and D. Gallwitz. 2000. The full complement of yeast Ypt/Rab-GTPases and their involvement in exo- and endocytic trafficking. Subcell. Biochem. 34:133-173.
23. Guldener, U., S. Heck, T. Fielder, J. Beinhauer, and J.H. Hegemann. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24:2519-2524.
24. Guo, W., F. Tamanoi, and P. Novick. 2001. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 3:353-360.
25. Guo, Z., L. Liu, D. Cafiso, and D. Castle. 2002. Perturbation of a very late step of regulated exocytosis by a secretory carrier membrane protein (SCAMP2)-derived peptide. J. Biol. Chem. 277:35357-35363.
26. Haas, A., and W. Wickner. 1996. Homotypic vacuole fusion requires Sec17p (yeast alpha-SNAP) and Sec18p (yeast NSF). EMBO J. 15:3296-3305.
27. Haas, A., B. Conradt, and W. Wickner. 1994. G-protein ligands inhibit in vitro reactions of vacuole inheritance. J. Cell Biol. 126:87-97.
28. Haas, A., D. Scheglmann, T. Lazar, D. Gallwitz, and W. Wickner. 1995. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. EMBO J. 14:5258-5270.
29. Hirata, R., L.A. Graham, A. Takatsuki, T.H. Stevens, and Y. Anraku. 1997. VMA11 and VMA16 encode second and third proteolipid subunits of the Saccharomyces cerevisiae vacuolar membrane H+-ATPase. J. Biol. Chem. 272:4795-4803.
30. Kane, P.M. 1999. Biosynthesis and regulation of the yeast vacuolar H+-ATPase. J. Bioenerg. Biomembr. 31:49-56.
31. Kane, P.M., and K.J. Parra. 2000. Assembly and regulation of the yeast vacuolar H(+)-ATPase. J. Exp. Biol. 203:81-87.
32. Kane, P.M., C.T. Yamashiro, and T.H. Stevens. 1989. Biochemical characterization of the yeast vacuolar H(+)-ATPase. J. Biol. Chem. 264:19236-19244.
33. Kato, M., and W. Wickner. 2001. Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. EMBO J. 20:4035-4040.
34. Kawasaki-Nishi, S., K. Bowers, T. Nishi, M. Forgac, and T.H. Stevens. 2001a. The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 276:47411-47420.
35. Kawasaki-Nishi, S., T. Nishi, and M. Forgac. 2001b. Yeast V-ATPase complexes containing different isoforms of the 100-kDa a-subunit differ in coupling efficiency and in vivo dissociation. J. Biol. Chem. 276:17941-17948.
36. Klionsky, D.J., P.K. Herman, and S.D. Emr. 1990. The fungal vacuole: composition, function, and biogenesis. Microbiol. Rev. 54:266-292.
37. Laage, R., and C. Ungermann. 2001. The N-terminal domain of the t-SNARE Vam3p coordinates priming and docking in yeast vacuole fusion. Mol. Biol. Cell. 12:3375-3385.
38. Leveque, C., O. el Far, N. Martin-Moutot, K. Sato, R. Kato, M. Takahashi, and M.J. Seagar. 1994. Purification of the N-type calcium channel associated with syntaxin and synaptotagmin. A complex implicated in synaptic vesicle exocytosis. J. Biol. Chem. 269:6306-6312.
39. Lindau, M., and W. Almers. 1995. Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Curr. Opin. Cell Biol. 7:509-517.
40. Mahal, L.K., S.M. Sequeira, J.M. Gureasko, and T.H. Sollner. 2002. Calciumin-dependent stimulation of membrane fusion and SNAREpin formation by synaptotagmin I.J. CellBiol. 158:273-282.
41. Manolson, M.F., B. Wu, D. Proteau, B.E. Taillon, B.T. Roberts, M.A. Hoyt, and E.W. Jones. 1994. STV1 gene encodes functional homologue of 95-kDa yeast vacuolar H(+)- ATPase subunit Vph1p. J. Biol. Chem. 269:14064-14074.
42. Mayer, A. 2001. What drives membrane fusion in eukaryotes? Trends Biochem. Sci. 26:717-723.
43. Mayer, A., and W. Wickner. 1997. Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). J. Cell Biol. 136:307-317.
44. Mayer, A., W. Wickner, and A. Haas. 1996. Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell. 85:83-94.
45. Mayer, A., D. Scheglmann, S. Dove, A. Glatz, W. Wickner, and A. Haas. 2000. Phospharidylinositol 4,5-bisphosphate regulates two steps of homotypic vacuole fusion. Mol. Biol. Cell. 11:807-817.
46. Moriyama, Y., and N. Nelson. 1989. Cold inactivation of vacuolar proton-ATPases. J. Biol. Chem. 264:3577-3582.
47. Muller, O., D.I. Johnson, and A. Mayer. 2001. Cdc42p functions at the docking stage of yeast vacuole membrane fusion. EMBO J. 20:5657-5665.
48. 0 trans-complex formation. EMBO J. 21:259-269.
49. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron. 20:389-399.
50. Nichols, B.J., C. Ungermann, H.R. Pelham, W.T. Wickner, and A. Haas. 1997. Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature. 387:199-202.
51. Ohsumi, Y., and Y. Anraku. 1981. Active transport of basic amino acids driven by a proton motive force in vacuolar membrane vesicles of Saccharomyces cerevisiae. J. Biol. Chem. 256:2079-2082.
52. Ohsumi, Y., and Y. Anraku. 1983. Calcium transport driven by a proton motive force in vacuolar membrane vesicles of Saccharomyces cerevisiae. J. Biol. Chem. 258:5614-5617.
53. Parlati, F., T. Weber, J.A. McNew, B. Westermann, T.H. Sollner, and J.E. Rothman. 1999. 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. USA. 96:12565-12570.
54. Parra, K.J., and P.M. Kane. 1998. Reversible association between the V1 and V0 domains of yeast vacuolar H+-ATPase is an unconventional glucose-induced effect. Mol. Cell. Biol. 18:7064-7074.
55. Pelham, H.R. 2001. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 11:99-101.
56. Perzov, N., V. Padler-Karavani, H. Nelson, and N. Nelson. 2002. Characterization of yeast V-ATPase mutants lacking Vphlp or Srvlp and the effect on endocytosis. J. Exp. Biol. 205:1209-1219.
57. 2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature. 396:575-580.
58. Peters, C., P.D. Andrews, M.J. Stark, S. Cesaro-Tadic, A. Glatz, A. Podtelejnikov, M. Mann, and A. Mayer. 1999. Control of the terminal step of intracellular membrane fusion by protein phosphatase 1. Science. 285:1084-1087.
59. Peters, C., M.J. Bayer, S. Buhler, J.S. Andersen, M. Mann, and A. Mayer. 2001. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature. 409:581-588.
60. Powell, B., L.A. Graham, and T.H. Stevens. 2000. Molecular characterization of the yeast vacuolar H+-ATPase proton pore. J. Biol. Chem. 275:23654-23660.
61. Price, A., D. Seals, W. Wickner, and C. Ungermann. 2000a. The docking stage of yeast vacuole fusion requires the transfer of proteins from a cis-SNARE complex to a Rab/Ypt protein. J. Cell Biol. 148:1231-1238.
62. Price, A., W. Wickner, and C. Ungermann. 2000b. Proteins needed for vesicle budding from the Golgi complex are also required for the docking step of homotypic vacuole fusion. J. Cell Biol. 148:1223-1229.
63. Raymond, C.K., I. Howald-Stevenson, C.A. Vater, and T.H. Stevens. 1992. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a ptevacuolat compartment in class E vps mutants. Mol. Biol. Cell. 3:1389-1402.
64. Rohde, J., L. Dietrich, D. Langosch, and C. Ungermann. 2003. The transmembrane domain of Vam3 affects the composition of cis- and trans-SNARE complexes to promote homotypic vacuole fusion. J. Biol. Chem. 278:1656-1662.
65. Rothman, J.E. 1994. Mechanisms of intracellular protein transport. Nature. 372:55-63.
66. Sato, T., Y. Ohsumi, and Y. Anraku. 1984. Substrate specificities of active transport systems for amino acids in vacuolar-membrane vesicles of Saccharomyces cerevisiae. Evidence of seven independent proton/amino acid antiport systems. J. Biol. Chem. 259:11505-11508.
67. Sato, T.K., P. Rehling, M.R. Peterson, and S.D. Emr. 2000. Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Mol. Cell. 6:661-671.
68. Seals, D.F., G. Eitzen, N. Margolis, W.T. Wickner, and A. Price. 2000. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. USA. 97:9402-9407.
69. Seeley, E.S., M. Kato, N. Margolis, W. Wickner, and G. Eitzen. 2002. Genomic analysis of homotypic vacuole fusion. Mol. Biol. Cell. 13:782-794.
70. Sheng, Z.H., J. Rettig, M. Takahashi, and W.A. Catterall. 1994. Identification of a syntaxin-binding site on N-type calcium channels. Neuron. 13:1303-1313.
71. Shimomura, O., B. Musicki, Y. Kishi, and S. Inouye. 1993. Light-emitting properties of recombinant semi-synthetic aequorins and recombinant fluorescein-conjugated aequorin for measuring cellular calcium. Cell Calcium. 14:373-378.
72. Singleton, D.R., T.T. Wu, and J.D. Castle. 1997. Three mammalian SCAMPs (secretory carrier membrane proteins) are highly related products of distinct genes having similar subcellular distributions. J. Cell Sci. 110:2099-2107.
73. Slusarewicz, P., Z. Xu, K. Seefeld, A. Haas, and W.T. Wickner. 1997. 12B is a small cytosolic protein that participates in vacuole fusion. Proc. Natl. Acad. Sci. USA. 94:5582-5587.
74. Sollner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324.
75. Stevens, T.H., and M. Forgac. 1997. Structure, function and regulation of the vacuolar (H+)-ATPase. Annu. Rev. Cell Dev. Biol. 13:779-808.
76. Ungermann, C., B.J. Nichols, H.R. Pelham, and W. Wickner. 1998a. 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.
77. Ungermann, C., K. Sato, and W. Wickner. 1998b. Defining the functions of trans-SNARE pairs. Nature. 396:543-548.
78. Ungermann, C., G.F. von Mollard, O.N. Jensen, N. Margolis, T.H. Stevens, and W. Wickner. 1999a. Three v-SNAREs and two t-SNAREs, present in a pentameric cis-SNARE complex on isolated vacuoles, are essential for homotypic fusion. J. Cell Biol. 145:1435-1442.
79. Ungermann, C., W. Wickner, and Z. Xu. 1999b. Vacuole acidification is required for trans-SNARE pairing, LMA1 release, and homotypic fusion. Proc. Natl. Acad Sci. USA. 96:11194-11199.
80. Veit, M., R. Laage, L. Dietrich, L. Wang, and C. Ungermann. 2001. Vac8p release from the SNARE complex and its palmitoylation are coupled and essential for vacuole fusion. EMBO J. 20:3145-3155.
81. Wada, Y., and Y. Anraku. 1994. Chemiosmotic coupling of ion transport in the yeast vacuole: its role in acidification inside organelles. J. Bioenerg. Biomembr. 26:631-637.
82. Wada, Y., Y. Ohsumi, and Y. Anraku. 1992a. Chloride transport of yeast vacuolar membrane vesicles: a study of in vitro vacuolar acidification. Biochim. Biophys. Acta. 1101:296-302.
83. Wada, Y., Y. Ohsumi, and Y. Anraku. 1992b. Genes for directing vacuolar morphogenesis in Saccharomyces cerevisiae. I. Isolation and characterization of two classes of vam mutants. J. Biol. Chem. 267:18665-18670.
84. Wang, L., C. Ungermann, and W. Wickner. 2000. The docking of primed vacuoles can be reversibly arrested by excess Sec17p (alpha-SNAP). J. Biol. Chem. 275:22862-22867.
85. Wang, L., E.S. Seeley, W. Wickner, and A.J. Merz. 2002. Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle. Cell. 108:357-369.
86. Wang, Y., I. Dulubova, J. Rizo, and T.C. Sudhof. 2001a. Functional analysis of conserved structural elements in yeast syntaxin Vam3p. J. Biol. Chem. 276:28598-28605.
87. Wang, Y.X., E.J. Kauffman, J.E. Duex, and L.S. Weisman. 2001b. Fusion of docked membranes requires the armadillo repeat protein Vac8p. J. Biol. Chem. 276:35133-35140.
88. Weber, T., B.V. Zemelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Sollner, and J.E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772.
89. Wurmser, A.E., T.K. Sato, and S.D. Emr. 2000. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151:551-562.
90. Xu, Z., and W. Wickner. 1996. Thioredoxin is required for vacuole inheritance in Saccharomyces cerevisiae. J. Cell Biol. 132:787-794.
91. Xu, Z., A. Mayer, E. Muller, and W. Wickner. 1997. A heterodimer of thioredoxin and I(B)2 cooperates with Sec18p (NSF) to promote yeast vacuole inheritance. J. Cell Biol. 136:299-306.
92. Xu, Z., K. Sato, and W. Wickner. 1998. LMA1 binds to vacuoles at Sec18p (NSF), transfers upon ATP hydrolysis to a t-SNARE (Vam3p) complex, and is released during fusion. Cell. 93:1125-1134.
93. Zhang, X., E. Bi, P. Novick, L. Du, K.G. Kozminski, J.H. Lipschutz, and W. Guo. 2001. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 276:46745-46750.
94. Zimmerberg, J. 2001. How can proteolipids be central players in membrane fusion? Trends Cell Biol. 11:233-235.