V-SNARE transmembrane domains function as catalysts for vesicle fusion

eLife

Volumn 5, Issue JUN2016, 2016, Pages

  Dhara, Madhurima ^a   Yarzagaray, Antonio ^a   Makke, Mazen ^a   Schindeldecker, Barbara ^a   Schwarz, Yvonne ^a   Shaaban, Ahmed ^a   Sharma, Satyan ^b   Böckmann, Rainer A ^c   Lindau, Manfred ^b   Mohrmann, Ralf ^a   Bruns, Dieter ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ISOLEUCINE; LEUCINE; SNARE PROTEIN; SYNAPTOBREVIN 2; VALINE; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; EMBRYO; EPIFLUORESCENCE MICROSCOPY; GENE MUTATION; IMMUNOCYTOCHEMISTRY; MEMBRANE FUSION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN STABILITY; SEQUENCE ANALYSIS; X RAY CRYSTALLOGRAPHY; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CHEMISTRY; DNA MUTATIONAL ANALYSIS; EXOCYTOSIS; GENETICS; METABOLISM; PROTEIN CONFORMATION; SECRETORY VESICLE;

ANIMALS; CELLS, CULTURED; DNA MUTATIONAL ANALYSIS; EXOCYTOSIS; MEMBRANE FUSION; MICE; MODELS, BIOLOGICAL; MUTANT PROTEINS; PROTEIN CONFORMATION; SECRETORY VESICLES; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84981240726     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.17571.001     Document Type: Article

References (91)

1. Agrawal P, Kiihne S, Hollander J, Hulsbergen F, Hofmann M, Langosch D, de Groot H. 2007. Solid state NMR investigation of the interaction between biomimetic lipid bilayers and de novo designed fusogenic peptides. ChemBioChem 8:493-496. doi: 10.1002/cbic.200600518
2. Agrawal P, Kiihne S, Hollander J, Hofmann M, Langosch D, de Groot H. 2010. A solid-state NMR study of changes in lipid phase induced by membrane-fusogenic LV-peptides. Biochimica Et Biophysica Acta (BBA) -Biomembranes 1798:202-209. doi: 10.1016/j.bbamem.2009.10.015
3. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez de Toledo G, Lindau M. 1997. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389:509-512. doi: 10.1038/39081
4. Alvarez de Toledo G, Fernández-Chacón R, Fernández JM. 1993. Release of secretory products during transient vesicle fusion. Nature 363:554-558. doi: 10.1038/363554a0
5. Ashery U, Betz A, Xu T, Brose N, Rettig J. 1999. An efficient method for infection of adrenal chromaffin cells using the semliki forest virus gene expression system. European Journal of Cell Biology 78:525-532. doi: 10.1016/S0171-9335(99)80017-X
6. Bao H, Goldschen-Ohm M, Jeggle P, Chanda B, Edwardson JM, Chapman ER. 2016. Exocytotic fusion pores are composed of both lipids and proteins. Nature Structural & Molecular Biology 23:67-73. doi: 10.1038/nsmb.3141
7. Bekkers JM, Stevens CF. 1991. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. PNAS 88:7834-7838. doi: 10.1073/pnas.88.17.7834
8. Bolte S, Cordelières FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. Journal of Microscopy 224:213-232. doi: 10.1111/j.1365-2818.2006.01706.x
9. Borisovska M, Zhao Y, Tsytsyura Y, Glyvuk N, Takamori S, Matti U, Rettig J, Südhof T, Bruns D. 2005. v-SNAREs control exocytosis of vesicles from priming to fusion. The EMBO Journal 24:2114-2126. doi: 10.1038/sj.emboj.7600696
10. Borisovska M, Schwarz YN, Dhara M, Yarzagaray A, Hugo S, Narzi D, Siu SW, Kesavan J, Mohrmann R, Böckmann RA, Bruns D. 2012. Membrane-proximal tryptophans of synaptobrevin II stabilize priming of secretory vesicles. Journal of Neuroscience 32:15983-15997. doi: 10.1523/JNEUROSCI.6282-11.2012
11. Bruns D. 1998. Serotonin transport in cultured leech neurons. Methods in Enzymology 296:593-607. doi: 10.1016/s0076-6879(98)96042-6
12. Bruns D. 2004. Detection of transmitter release with carbon fiber electrodes. Methods 33:312-321. doi: 10.1016/j.ymeth.2004.01.004
13. Bruns D, Jahn R. 1995. Real-time measurement of transmitter release from single synaptic vesicles. Nature 377: 62-65. doi: 10.1038/377062a0
14. Chang CW, Chiang CW, Gaffaney JD, Chapman ER, Jackson MB. 2016. Lipid-anchored synaptobrevin provides little or no support for exocytosis or liposome fusion. Journal of Biological Chemistry 291:2848-2857. doi: 10.1074/jbc.M115.701169
15. Chang CW, Hui E, Bai J, Bruns D, Chapman ER, Jackson MB. 2015. A structural role for the synaptobrevin 2 transmembrane domain in dense-core vesicle fusion pores. Journal of Neuroscience 35:5772-5780. doi: 10.1523/JNEUROSCI.3983-14.2015
16. Chizmadzhev YA, Cohen FS, Shcherbakov A, Zimmerberg J. 1995. Membrane mechanics can account for fusion pore dilation in stages. Biophysical Journal 69:2489-2500. doi: 10.1016/S0006-3495(95)80119-0
17. Chow RH, von Rüden L, Neher E. 1992. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60-63. doi: 10.1038/356060a0
18. Deá k F, Schoch S, Liu X, Südhof TC, Kavalali ET. 2004. Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nature Cell Biology 6:1102-1108. doi: 10.1038/ncb1185
19. Dhara M, Yarzagaray A, Schwarz Y, Dutta S, Grabner C, Moghadam PK, Bost A, Schirra C, Rettig J, Reim K, Brose N, Mohrmann R, Bruns D. 2014. Complexin synchronizes primed vesicle exocytosis and regulates fusion pore dynamics. Journal of Cell Biology 204:1123-1140. doi: 10.1083/jcb.201311085
20. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. 1995. A smooth particle mesh Ewald method. Journal of Chemical Physics 103:8577-8593. doi: 10.1063/1.470117
21. Fang Q, Lindau M. 2014. How could SNARE proteins open a fusion pore? Physiology 29:278-285. doi: 10.1152/physiol.00026.2013
22. Fava E, Dehghany J, Ouwendijk J, Müller A, Niederlein A, Verkade P, Meyer-Hermann M, Solimena M. 2012. Novel standards in the measurement of rat insulin granules combining electron microscopy, high-content image analysis and in silico modelling. Diabetologia 55:1013-1023. doi: 10.1007/s00125-011-2438-4
23. Fdez E, Martínez-Salvador M, Beard M, Woodman P, Hilfiker S. 2010. Transmembrane-domain determinants for SNARE-mediated membrane fusion. Journal of Cell Science 123:2473-2480. doi: 10.1242/jcs.061325
24. Follenzi A, Ailles LE, Bakovic S, Geuna M, Naldini L. 2000. Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nature Genetics 25:217-222. doi: 10.1038/76095
25. Follenzi A, Sabatino G, Lombardo A, Boccaccio C, Naldini L. 2002. Efficient gene delivery and targeted expression to hepatocytes in vivo by improved lentiviral vectors. Human Gene Therapy 13:243-260. doi: 10.1089/10430340252769770
26. Giraudo CG, Hu C, You D, Slovic AM, Mosharov EV, Sulzer D, Melia TJ, Rothman JE. 2005. SNAREs can promote complete fusion and hemifusion as alternative outcomes. Journal of Cell Biology 170:249-260. doi: 10.1083/jcb.200501093
27. Grote E, Baba M, Ohsumi Y, Novick PJ. 2000. Geranylgeranylated SNAREs are dominant inhibitors of membrane fusion. Journal of Cell Biology 151:453-466. doi: 10.1083/jcb.151.2.453
28. Guzman RE, Schwarz YN, Rettig J, Bruns D. 2010. SNARE force synchronizes synaptic vesicle fusion and controls the kinetics of quantal synaptic transmission. Journal of Neuroscience 30:10272-10281. doi: 10.1523/JNEUROSCI.1551-10.2010
29. Han X, Jackson MB. 2005. Electrostatic interactions between the syntaxin membrane anchor and neurotransmitter passing through the fusion pore. Biophysical Journal 88:L20-22. doi: 10.1529/biophysj.104.056739
30. Han J, Pluhackova K, Bruns D, Böckmann RA. 2016. Synaptobrevin transmembrane domain determines the structure and dynamics of the SNARE motif and the linker region. Biochimica Et Biophysica Acta 1858:855-865. doi: 10.1016/j.bbamem.2016.01.030
31. Higuchi R, Krummel B, Saiki RK. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Research 16:7351-7367. doi: 10.1093/nar/16.15.7351
32. Hofmann MW, Peplowska K, Rohde J, Poschner BC, Ungermann C, Langosch D. 2006. Self-interaction of a SNARE transmembrane domain promotes the hemifusion-to-fusion transition. Journal of Molecular Biology 364:1048-1060. doi: 10.1016/j.jmb.2006.09.077
33. Hoover WG. 1985. Canonical dynamics: Equilibrium phase-space distributions. Physical Review A 31:1695-1697. doi: 10.1103/PhysRevA.31.1695
34. Hui E, Johnson CP, Yao J, Dunning FM, Chapman ER. 2009. Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2+)-regulated fusion. Cell 138:709-721. doi: 10.1016/j.cell.2009.05.049
35. Jahn R, Fasshauer D. 2012. Molecular machines governing exocytosis of synaptic vesicles. Nature 490:201-207. doi: 10.1038/nature11320
36. Jämbeck JP, Lyubartsev AP. 2012. An extension and further validation of an all-atomistic force field for biological membranes. Journal of Chemical Theory and Computation 8:2938-2948. doi: 10.1021/ct300342n
37. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics 79:926-935. doi: 10.1063/1.445869
38. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637. doi: 10.1002/bip.360221211
39. Kasson PM, Lindahl E, Pande VS. 2010. Atomic-resolution simulations predict a transition state for vesicle fusion defined by contact of a few lipid tails. PLoS Computational Biology 6:e1000829. doi: 10.1371/journal.pcbi.1000829
40. Kesavan J, Borisovska M, Bruns D. 2007. v-SNARE actions during Ca(2+)-triggered exocytosis. Cell 131:351-363. doi: 10.1016/j.cell.2007.09.025
41. Kozlov MM, McMahon HT, Chernomordik LV. 2010. Protein-driven membrane stresses in fusion and fission. Trends in Biochemical Sciences 35:699-706. doi: 10.1016/j.tibs.2010.06.003
42. Krzewski K, Gil-Krzewska A, Watts J, Stern JN, Strominger JL. 2011. VAMP4-and VAMP7-expressing vesicles are both required for cytotoxic granule exocytosis in NK cells. European Journal of Immunology 41:3323-3329. doi: 10.1002/eji.201141582
43. Laage R, Langosch D. 1997. Dimerization of the synaptic vesicle protein synaptobrevin (vesicle-associated membrane protein) II depends on specific residues within the transmembrane segment. European Journal of Biochemistry 249:540-546. doi: 10.1111/j.1432-1033.1997.00540.x
44. Lacroix E, Viguera AR, Serrano L. 1998. Elucidating the folding problem of alpha-helices: local motifs, long-range electrostatics, ionic-strength dependence and prediction of NMR parameters. Journal of Molecular Biology 284:173-191. doi: 10.1006/jmbi.1998.2145
45. Langosch D, Crane JM, Brosig B, Hellwig A, Tamm LK, Reed J. 2001. Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. Journal of Molecular Biology 311:709-721. doi: 10.1006/jmbi.2001.4889
46. Langosch D, Hofmann M, Ungermann C. 2007. The role of transmembrane domains in membrane fusion. Cellular and Molecular Life Sciences 64:850-864. doi: 10.1007/s00018-007-6439-x
47. Li JY, Edelmann L, Jahn R, Dahlström A. 1996. Axonal transport and distribution of synaptobrevin I and II in the rat peripheral nervous system. Journal of Neuroscience 16:137-147.
48. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE. 2010. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins: Structure, Function, and Bioinformatics 78: 1950-1958. doi: 10.1002/prot.22711
49. Lippert U, Ferrari DM, Jahn R. 2007. Endobrevin/VAMP8 mediates exocytotic release of hexosaminidase from rat basophilic leukaemia cells. FEBS Letters 581:3479-3484. doi: 10.1016/j.febslet.2007.06.057
50. 2+-triggered neurotransmitter release at the mouse neuromuscular junction. Journal of Physiology 589:1603-1618. doi: 10.1113/jphysiol.2010.201939
51. Lu X, Zhang Y, Shin YK. 2008. Supramolecular SNARE assembly precedes hemifusion in SNARE-mediated membrane fusion. Nature Structural & Molecular Biology 15:700-706. doi: 10.1038/nsmb.1433
52. Manders EMM, Verbeek FJ, Aten JA. 1993. Measurement of co-localization of objects in dual-colour confocal images. Journal of Microscopy 169:375-382. doi: 10.1111/j.1365-2818.1993.tb03313.x
53. Markvoort AJ, Marrink SJ. 2011. Lipid acrobatics in the membrane fusion arena. Current Topics in Membranes 68:259-294. doi: 10.1016/B978-0-12-385891-7.00011-8
54. Martens S, Kozlov MM, McMahon HT. 2007. How synaptotagmin promotes membrane fusion. Science 316: 1205-1208. doi: 10.1126/science.1142614
55. Matti U, Pattu V, Halimani M, Schirra C, Krause E, Liu Y, Weins L, Chang HF, Guzman R, Olausson J, Freichel M, Schmitz F, Pasche M, Becherer U, Bruns D, Rettig J. 2013. Synaptobrevin2 is the v-SNARE required for cytotoxic T-lymphocyte lytic granule fusion. Nature Communications 4:1439. doi: 10.1038/ncomms2467
56. McNew JA, Weber T, Parlati F, Johnston RJ, Melia TJ, Söllner TH, Rothman JE. 2000. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. Journal of Cell Biology 150:105-117. doi: 10.1083/jcb.150.1.105
57. Ming M, Schirra C, Becherer U, Stevens DR, Rettig J. 2015. Behavior and properties of mature lytic granules at the immunological synapse of human cytotoxic T lymphocytes. PLoS One 10:e0135994. doi: 10.1371/journal.pone.0135994
58. Miyamoto S, Kollman PA. 1992. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. Journal of Computational Chemistry 13:952-962. doi: 10.1002/jcc.540130805
59. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, Marrink SJ. 2008. The MARTINI coarse-grained force field: extension to proteins. Journal of Chemical Theory and Computation 4:819-834. doi: 10.1021/ct700324x
60. Nadelhaft I. 1973. Measurement of the size distribution of zymogen granules from rat pancreas. Biophysical Journal 13:1014-1029. doi: 10.1016/S0006-3495(73)86042-4
61. Neumann S, Langosch D. 2011. Conserved conformational dynamics of membrane fusion protein transmembrane domains and flanking regions indicated by sequence statistics. Proteins: Structure, Function, and Bioinformatics 79:2418-2427. doi: 10.1002/prot.23063
62. Ngatchou AN, Kisler K, Fang Q, Walter AM, Zhao Y, Bruns D, Sørensen JB, Lindau M. 2010. Role of the synaptobrevin C terminus in fusion pore formation. PNAS 107:18463-18468. doi: 10.1073/pnas.1006727107
63. Nosè S. 1984. A unified formulation of the constant temperature molecular dynamics methods. The Journal of Chemical Physics 81:511-519. doi: 10.1063/1.447334
64. Parrinello M, Rahman A. 1981. Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics 52:7182-7190. doi: 10.1063/1.328693
65. Pieren M, Desfougères Y, Michaillat L, Schmidt A, Mayer A. 2015. Vacuolar SNARE protein transmembrane domains serve as nonspecific membrane anchors with unequal roles in lipid mixing. Journal of Biological Chemistry 290:12821-12832. doi: 10.1074/jbc.M115.647776
66. Pronk S, Pá ll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, Shirts MR, Smith JC, Kasson PM, van der Spoel D, Hess B, Lindahl E. 2013. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29:845-854. doi: 10.1093/bioinformatics/btt055
67. Quint S, Widmaier S, Minde D, Hornburg D, Langosch D, Scharnagl C. 2010. Residue-specific side-chain packing determines the backbone dynamics of transmembrane model helices. Biophysical Journal 99:2541-2549. doi: 10.1016/j.bpj.2010.08.031
68. Rajappa R, Gauthier-Kemper A, Böning D, Hüve J, Klingauf J, Huve J. 2016. Synaptophysin 1 clears synaptobrevin 2 from the presynaptic active zone to prevent short-term depression. Cell Reports 14:1369-1381. doi: 10.1016/j.celrep.2016.01.031
69. Rettig J, Neher E. 2002. Emerging roles of presynaptic proteins in Ca++-triggered exocytosis. Science 298:781-785. doi: 10.1126/science.1075375
70. Risselada HJ, Kutzner C, Grubmüller H. 2011. Caught in the act: visualization of SNARE-mediated fusion events in molecular detail. ChemBioChem 12:1049-1055. doi: 10.1002/cbic.201100020
71. Rohde J, Dietrich L, Langosch D, Ungermann C. 2003. The transmembrane domain of Vam3 affects the composition of cis-and trans-SNARE complexes to promote homotypic vacuole fusion. Journal of Biological Chemistry 278:1656-1662. doi: 10.1074/jbc.M209522200
72. Roy R, Laage R, Langosch D. 2004. Synaptobrevin transmembrane domain dimerization-revisited. Biochemistry 43:4964-4970. doi: 10.1021/bi0362875
73. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology 234:779-815. doi: 10.1006/jmbi.1993.1626
74. Schoch S, Deá k F, Königstorfer A, Mozhayeva M, Sara Y, Südhof TC, Kavalali ET. 2001. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294:1117-1122. doi: 10.1126/science.1064335
75. Sharma S, Kim BN, Stansfeld PJ, Sansom MS, Lindau M. 2015. A coarse grained model for a lipid membrane with physiological composition and leaflet asymmetry. PLoS One 10:e0144814. doi: 10.1371/journal.pone.0144814
76. Shi L, Shen QT, Kiel A, Wang J, Wang HW, Melia TJ, Rothman JE, Pincet F. 2012. SNARE proteins: one to fuse and three to keep the nascent fusion pore open. Science 335:1355-1359. doi: 10.1126/science.1214984
77. Smirnova YG, Marrink SJ, Lipowsky R, Knecht V. 2010. Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. Journal of the American Chemical Society 132:6710-6718. doi: 10.1021/ja910050x
78. Sørensen JB. 2009. Conflicting views on the membrane fusion machinery and the fusion pore. Annual Review of Cell and Developmental Biology 25:513-537. doi: 10.1146/annurev.cellbio.24.110707.175239
79. Stein A, Weber G, Wahl MC, Jahn R. 2009. Helical extension of the neuronal SNARE complex into the membrane. Nature 460:525-528. doi: 10.1038/nature08156
80. Stelzer W, Poschner BC, Stalz H, Heck AJ, Langosch D. 2008. Sequence-specific conformational flexibility of SNARE transmembrane helices probed by hydrogen/deuterium exchange. Biophysical Journal 95:1326-1335. doi: 10.1529/biophysj.108.132928
81. Stevens CF, Wesseling JF. 1999. Augmentation is a potentiation of the exocytotic process. Neuron 22:139-146. doi: 10.1016/S0896-6273(00)80685-6
82. Südhof TC, Rothman JE. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323:474-477. doi: 10.1126/science.1161748
83. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Müller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmüller H, Heuser J, et al. 2006. Molecular anatomy of a trafficking organelle. Cell 127:831-846. doi: 10.1016/j.cell.2006.10.030
84. Tamm LK, Crane J, Kiessling V. 2003. Membrane fusion: a structural perspective on the interplay of lipids and proteins. Current Opinion in Structural Biology 13:453-466. doi: 10.1016/S0959-440X(03)00107-6
85. Tarafdar PK, Chakraborty H, Bruno MJ, Lentz BR. 2015. Phosphatidylserine-dependent catalysis of stalk and pore formation by synaptobrevin JMR-TMD peptide. Biophysical Journal 109:1863-1872. doi: 10.1016/j.bpj.2015.08.051
86. Tong J, Borbat PP, Freed JH, Shin Y-K. 2009. A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. PNAS 106:5141-5146. doi: 10.1073/pnas.0813138106
87. Wang CC, Ng CP, Lu L, Atlashkin V, Zhang W, Seet LF, Hong W. 2004. A role of VAMP8/endobrevin in regulated exocytosis of pancreatic acinar cells. Developmental Cell 7:359-371. doi: 10.1016/j.devcel.2004.08.002
88. Wassenaar TA, Pluhackova K, Böckmann RA, Marrink SJ, Tieleman DP. 2014. Going backward: A flexible geometric approach to reverse transformation from coarse grained to atomistic models. Journal of Chemical Theory and Computation 10:676-690. doi: 10.1021/ct400617g
89. Xu J, Luo F, Zhang Z, Xue L, Wu XS, Chiang HC, Shin W, Wu LG. 2013. SNARE proteins synaptobrevin, SNAP-25, and syntaxin are involved in rapid and slow endocytosis at synapses. Cell Reports 3:1414-1421. doi: 10.1016/j.celrep.2013.03.010
90. Zhang Z, Jackson MB. 2010. Membrane bending energy and fusion pore kinetics in Ca(2+)-triggered exocytosis. Biophysical Journal 98:2524-2534. doi: 10.1016/j.bpj.2010.02.043
91. 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