Vacuolar SNARE protein transmembrane domains serve as nonspecific membrane anchors with unequal roles in lipid mixing

Journal of Biological Chemistry

Volumn 290, Issue 20, 2015, Pages 12821-12832

  Pieren, Michel ^a   Desfougères, Yann ^a   Michaillat, Lydie ^a   Schmidt, Andrea ^a   Mayer, Andreas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; AMINO ACIDS; ANCHORS; CELL MEMBRANES; MACHINERY; PROTEINS;

CONFORMATIONAL TRANSITIONS; LIPID STRUCTURES; MECHANICAL FORCE; MEMBRANE ANCHORS; PAIR-WISE EXCHANGES; PRIMARY SEQUENCES; STRUCTURAL STUDIES; TRANS-MEMBRANE DOMAINS;

MEMBRANES;

LEUCINE; MEMBRANE FUSION PROTEIN; SNARE PROTEIN; VALINE; MEMBRANE LIPID; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BASE PAIRING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVATION; LIPID BILAYER; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; CELL VACUOLE; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

MEMBRANE FUSION; MEMBRANE LIPIDS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; VACUOLES;

EID: 84929378454     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.647776     Document Type: Article

References (67)

1. Ostrowicz, C. W., Meiringer, C. T., and Ungermann, C. (2008) Yeast vacuole fusion: a model system for eukaryotic endomembrane dynamics. Autophagy 4, 5-19
2. Wickner, W. (2002) Yeast vacuoles and membrane fusion pathways. EMBO J. 21, 1241-1247
3. Haas, A., Conradt, B., and Wickner, W. (1994) G-protein ligands inhibit in vitro reactions of vacuole inheritance. J. Cell Biol. 126, 87-97
4. Reese, C., Heise, F., and Mayer, A. (2005) Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 436, 410-414
5. Mayer, A., and Wickner, W. (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
6. Ungermann, C., and Wickner, W. (1998) Vam7p, a vacuolar SNAP-25 homolog, is required for SNARE complex integrity and vacuole docking and fusion. EMBO J. 17, 3269-3276
7. Hickey, C. M., and Wickner, W. (2010) HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Mol. Biol. Cell 21, 2297-2305
8. Fasshauer, D., Sutton, R. B., Brunger, A. T., and Jahn, R. (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs. Proc. Natl. Acad. Sci. U.S.A. 95, 15781-15786
9. Collins, K. M., and Wickner, W. T. (2007) Trans-SNARE complex assembly and yeast vacuole membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 104, 8755-8760
10. Schwartz, M. L., and Merz, A. J. (2009) Capture and release of partially zipped trans-SNARE complexes on intact organelles. J. Cell Biol. 185, 535-549
11. Dietrich, L. E., Gurezka, R., Veit, M., and Ungermann, C. (2004) The SNARE Ykt6 mediates protein palmitoylation during an early stage of homotypic vacuole fusion. EMBO J. 23, 45-53
12. Wickner, W. (2010) Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu. Rev. Cell Dev. Biol. 26, 115-136
13. Mayer, A., Wickner, W., and Haas, A. (1996) Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85, 83-94
14. Wang, L., Ungermann, C., and Wickner, W. (2000) The docking of primed vacuoles can be reversibly arrested by excess Sec17p (α-SNAP). J. Biol. Chem. 275, 22862-22867
15. Grote, E., Baba, M., Ohsumi, Y., and Novick, P. J. (2000) Geranylgeranylated SNAREs are dominant inhibitors of membrane fusion. J. Cell Biol. 151, 453-466
16. Rohde, J., Dietrich, L., Langosch, D., and Ungermann, C. (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
17. Jun, Y., Xu, H., Thorngren, N., and Wickner, W. (2007) Sec18p and Vam7p remodel trans-SNARE complexes to permit a lipid-anchored RSNARE to support yeast vacuole fusion. EMBO J. 26, 4935-4945
18. McNew, J. A., Weber, T., Parlati, F., Johnston, R. J., Melia, T. J., Söllner, T. H., and Rothman, J. E. (2000) Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150, 105-117
19. Xu, H., Zick, M., Wickner, W. T., and Jun, Y. (2011) A lipid-anchored SNARE supports membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 108, 17325-17330
20. Xu, Y., Zhang, F., Su, Z., McNew, J. A., and Shin, Y. K. (2005) Hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12, 417-422
21. Zhou, P., Bacaj, T., Yang, X., Pang, Z. P., and Südhof, T. C. (2013) Lipidanchored SNAREs lacking transmembrane regions fully support membrane fusion during neurotransmitter release. Neuron 80, 470-483
22. Langosch, D., Crane, J. M., Brosig, B., Hellwig, A., Tamm, L. K., and Reed, J. (2001) Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. J. Mol. Biol. 311, 709-721
23. Hofmann, M. W., Weise, K., Ollesch, J., Agrawal, P., Stalz, H., Stelzer, W., Hulsbergen, F., de Groot, H., Gerwert, K., Reed, J., and Langosch, D. (2004) De novo design of conformationally flexible transmembrane peptides driving membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 101, 14776-14781
24. Poschner, B. C., Quint, S., Hofmann, M. W., and Langosch, D. (2009) Sequence-specific conformational dynamics of model transmembrane domains determines their membrane fusogenic function. J. Mol. Biol. 386, 733-741
25. Poschner, B. C., Fischer, K., Herrmann, J. R., Hofmann, M. W., and Langosch, D. (2010) Structural features of fusogenic model transmembrane domains that differentially regulate inner and outer leaflet mixing in membrane fusion. Mol. Membr. Biol. 27, 1-10
26. Fdez, E., Martínez-Salvador, M., Beard, M., Woodman, P., and Hilfiker, S. (2010) Transmembrane-domain determinants for SNARE-mediated membrane fusion. J. Cell Sci. 123, 2473-2480
27. Tong, J., Borbat, P. P., Freed, J. H., and Shin, Y. K. (2009) A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. Proc. Natl. Acad. Sci. U.S.A. 106, 5141-5146
28. Hofmann, M. W., Peplowska, K., Rohde, J., Poschner, B. C., Ungermann, C., and Langosch, D. (2006) Self-interaction of a SNARE transmembrane domain promotes the hemifusion-to-fusion transition. J. Mol. Biol. 364, 1048-1060
29. Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353
30. Stein, A., Weber, G., Wahl, M. C., and Jahn, R. (2009) Helical extension of the neuronal SNARE complex into the membrane. Nature 460, 525-528
31. Pieren, M., Schmidt, A., and Mayer, A. (2010) The SM protein Vps33 and the t-SNARE H(abc) domain promote fusion pore opening. Nat. Struct. Mol. Biol. 17, 710-717
32. Haas, A., and Wickner, W. (1996) Homotypic vacuole fusion requires Sec17p (yeast α-SNAP) and Sec18p (yeast NSF). EMBO J. 15, 3296-3305
33. Thorngren, N., Collins, K. M., Fratti, R. A., Wickner, W., and Merz, A. J. (2004) A soluble SNARE drives rapid docking, bypassing ATP and Sec17/18p for vacuole fusion. EMBO J. 23, 2765-2776
34. Kunkel, T. A., Roberts, J. D., and Zakour, R. A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382
35. Nichols, B. J., Ungermann, C., Pelham, H. R., Wickner, W. T., and Haas, A. (1997) Homotypic vacuolar fusion mediated by t-and v-SNAREs. Nature 387, 199-202
36. Boeke, J. D., Trueheart, J., Natsoulis, G., and Fink, G. R. (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154, 164-175
37. Scott, J. H., and Schekman, R. (1980) Lyticase: endoglucanase and protease activities that act together in yeast cell lysis. J. Bacteriol. 142, 414-423
38. Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., and Rothman, J. E. (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772
39. Chernomordik, L. V., and Kozlov, M. M. (2003) Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175-207
40. Cheever, M. L., Sato, T. K., de Beer, T., Kutateladze, T. G., Emr, S. D., and Overduin, M. (2001) Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3, 613-618
41. Gao, J., Liao, J., and Yang, G. Y. (2009) CAAX-box protein, prenylation process and carcinogenesis. Am. J. Transl. Res. 1, 312-325
42. Ungermann, C., Nichols, B. J., Pelham, H. R., and 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
43. Sharpe, H. J., Stevens, T. J., and Munro, S. (2010) A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158-169
44. Cordes, F. S., Bright, J. N., and Sansom, M. S. (2002) Proline-induced distortions of transmembrane helices. J. Mol. Biol. 323, 951-960
45. Orzáez, M., Salgado, J., Giménez-Giner, A., Pérez-Payá, E., and Mingarro, I. (2004) Influence of proline residues in transmembrane helix packing. J. Mol. Biol. 335, 631-640
46. Milovanovic, D., Honigmann, A., Koike, S., Göttfert, F., Pähler, G., Junius, M., Müllar, S., Diederichsen, U., Janshoff, A., Grubmüller, H., Risselada, H. J., Eggeling, C., Hell, S. W., van den Bogaart, G., and Jahn, R. (2015) Hydrophobic mismatch sorts SNARE proteins into distinct membrane domains. Nat. Commun. 6, 5984
47. McNew, J. A., Weber, T., Engelman, D. M., Söllner, T. H., and Rothman, J. E. (1999) The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion. Mol. Cell 4, 415-421
48. Wang, Y., Dulubova, I., Rizo, J., and Südhof, T. C. (2001) Functional analysis of conserved structural elements in yeast syntaxin Vam3p. J. Biol. Chem. 276, 28598-28605
49. Kee, Y., and Scheller, R. H. (1996) Localization of synaptotagmin-binding domains on syntaxin. J. Neurosci. 16, 1975-1981
50. Yassine, W., Taib, N., Federman, S., Milochau, A., Castano, S., Sbi, W., Manigand, C., Laguerre, M., Desbat, B., Oda, R., and Lang, J. (2009) Reversible transition between α-helix and β-sheet conformation of a trans-membrane domain. Biochim. Biophys. Acta 1788, 1722-1730
51. Ngatchou, A. N., Kisler, K., Fang, Q., Walter, A. M., Zhao, Y., Bruns, D., Sørensen, J. B., and Lindau, M. (2010) Role of the synaptobrevinCterminus in fusion pore formation. Proc. Natl. Acad. Sci. U.S.A. 107, 18463-18468
52. Conradt, B., Haas, A., and Wickner, W. (1994) Determination of four biochemically distinct, sequential stages during vacuole inheritance in vitro. J. Cell Biol. 126, 99-110
53. Collins, K. M., Thorngren, N. L., Fratti, R. A., and Wickner, W. T. (2005) Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J. 24, 1775-1786
54. Parlati, F., McNew, J. A., Fukuda, R., Miller, R., Söllner, T. H., and Rothman, J. E. (2000) Topological restriction of SNARE-dependent membrane fusion. Nature 407, 194-198
55. Alpadi, K., Kulkarni, A., Comte, V., Reinhardt, M., Schmidt, A., Namjoshi, S., Mayer, A., and Peters, C. (2012) Sequential analysis of trans-SNARE formation in intracellular membrane fusion. PLoS Biol. 10, e1001243
56. Chernomordik, L. V., and Kozlov, M. M. (2008) Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15, 675-683
57. Jahn, R., Lang, T., and Südhof, T. C. (2003) Membrane fusion. Cell 112, 519-533
58. Risselada, H. J., and Grubmüller, H. (2012) How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr. Opin. Struct. Biol. 22, 187-196
59. Langosch, D., Brosig, B., and Pipkorn, R. (2001) Peptide mimics of the vesicular stomatitis virus G-protein transmembrane segment drive membrane fusion in vitro. J. Biol. Chem. 276, 32016-32021
60. Neumann, S., and Langosch, D. (2011) Conserved conformational dynamics of membrane fusion protein transmembrane domains and flanking regions indicated by sequence statistics. Proteins 79, 2418-2427
61. Jahn, R., and Südhof, T. C. (1999) Membrane fusion and exocytosis. Annu. Rev. Biochem. 68, 863-911
62. Kesavan, J., Borisovska, M., and Bruns, D. (2007) v-SNARE actions during Ca2+-triggered exocytosis. Cell 131, 351-363
63. Van Komen, J. S., Bai, X., Rodkey, T. L., Schaub, J., and McNew, J. A. (2005) The polybasic juxtamembrane region of Sso1p is required for SNARE function in vivo. Eukaryot. Cell 4, 2017-2028
64. Südhof, T. C. (2013) Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675-690
65. Choi, U. B., Strop, P., Vrljic, M., Chu, S., Brunger, A. T., and Weninger, K. R. (2010) Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex. Nat. Struct. Mol. Biol. 17, 318-324
66. Kim, J. Y., Choi, B. K., Choi, M. G., Kim, S. A., Lai, Y., Shin, Y. K., and Lee, N. K. (2012) Solution single-vesicle assay reveals PIP2-mediated sequential actions of synaptotagmin-1 on SNAREs. EMBO J. 31, 2144-2155
67. Jones, E. W., Zubenko, G. S., and Parker, R. R. (1982) PEP4 gene function is required for expression of several vacuolar hydrolases in Saccharomyces cerevisiae. Genetics 102, 665-677