Vesicles and vesicle fusion: Coarse-grained simulations

Methods in Molecular Biology

Volumn 924, Issue , 2013, Pages 659-697

  Shillcock, Julian C ^a  

^a NONE

Author keywords

Bilayer; Coarse grained simulation; Dissipative particle dynamics; Membrane; Phospholipid; Vesicle; Vesicle fusion

Indexed keywords

EID: 84934444294     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-62703-17-5_26     Document Type: Article

References (175)

1. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1989) Molecular biology of the cell, 2nd edn. Garland Publishing, New York
2. Israelachvili J (1992) Intermolecular and surface forces, 2nd edn. Academic, press London
3. Jahn R, Grubmuller H (2002) Membrane fusion. Curr Op Cell Biol 14:488-495
4. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474-477
5. Jones RAL (2002) Soft condensed matter. Oxford University Press, Oxford, UK
6. Sprong H, van der Sluijs P, van Meer G (2001) How proteins move lipids and lipids move proteins. Nat Mol Cell Biol 2:504-513
7. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Mol Cell Biol 1:31-39
8. Thompson MP, Chien M-P, Ku T-H, Rush AM, Gianneschi NC (2010) Smart lipids for programmable nanomaterials. Nanoletters 10:2690-2693
9. Hadorn M, Hotz PE (2010) DNA-mediated self-Assembly of artificial vesicles. PLoS One 5:e9886
10. Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622-629
11. Jiang W, Kim BYS, Rutka JT, Chan WCW (2008) Nanoparticle-mediated cellular response is size-dependent. Nat Nanotechnol 3:145-150
12. Zhang S, Li J, Lykotrafitis G, Bao G, Suresh S (2009) Size-dependent endocytosis of nanoparticles. Adv Mater 21:419-424
13. Mailander V, Landfester K (2009) Interaction of nanoparicles with cells. Biomacromolecules 10:2379-2400
14. Mitragotri S, Lahann J (2009) Physical approaches to biomaterial design. Nat Mater 8:15-23
15. Nel AE, Madler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Understanding biophysicochemical interactions at the nanobio interface. Nat Mater 8:543-557
16. Heimburg T (2009) Membrane biophysics. Soft Matter 5:3129-3364
17. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720-731
18. Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438:578-580
19. Castorph S, Riedel D, Arleth L, Sztucki M, Jahn R, Holt M, Salditt T (2010) Structure parameters of synaptic vesicles quantified by small-Angle X-ray scattering. Biophys J 98:1200-1208
20. Rosoff M (1996) Vesicles. Surfactant science series. Marcel Dekker, New York
21. Dobereiner H-G (2000) Fluctuating vesicle shapes. In: Luisi PL, Walde P (eds) Giant vesicles. John Wiley and Sons Ltd, New York
22. Evans E,RawiczW(1990) Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys Rev Lett 64:2094-2097
23. Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328-339
24. Canham PB (1970) The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J Theor Biol 26:61-81
25. Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforschung c 28:693-703
26. Seifert U (1997) Configurations of fluid membranes and vesicles. Adv Phys 46:13-137
27. Seifert U, Shillcock J, Nelson P (1996) Role of bilayer tilt difference in equilibrium membrane shapes. Phys Rev Lett 77:5237-5240
28. Gompper G, KrollDM(1997) Network models of fluid, hexatic and polymerized membranes. J Phys Condens Matter 9:8795-8834
29. Noguchi H (2009) Membrane simulation models from nanometer to micrometer scale. J Phys Soc Japan 78:041007-1-041007-9
30. Julicher F, Lipowsky R (1993) Domaininduced budding of vesicles. Phys Rev Lett 70:2964-2967
31. Seifert U (1993) Curvature-induced lateral phase segregation in two-component vesicles. Phys Rev Lett 70:1335-1338
32. Taniguchi T (1996) Shape deformation and phase separation dynamics of two-component vesicles. Phys Rev Lett 76:4444-4447
33. Ramakrishnan N, Sunil Kumar PB, Ipsen JH (2010) Monte Carlo simulations of fluid vesicles with in plane orientational ordering. Phys Rev E 81:041922-1-041922-9
34. Gruner SM (1989) Stability of lyotropic phases with curved interfaces. J Phys Chem 93:7562-7570
35. Jones RAL (2004) Soft Machines Nanotechnology and Life. Oxford University Press, Oxford, UK
36. Arkhipov A, Yin Y, Schulten K (2008) Fourscale description of membrane sculpting by BAR domains. Biophys J 95:2806-2821
37. Campelo F, Fabrikant G, McMahon HT, Kozlov MM (2009) Modeling membrane shaping by proteins: focus on EHD2 and N-BAR domains. FEBS Lett 584:1830-1839
38. Shillcock JC (2008) Insight or illusion? seeing inside the cell with mesoscopic simulations. HFSP J 2:1-6
39. Ayton G, Smondyrev AM, Bardenhagen SG, McMurtry P, Voth GA (2002) Interfacing molecular dynamics and macro-scale simulations for lipid bilayer vesicles. Biophys J 83:1026-1038
40. Delgado-Buscalioni R, Kremer K, Prapotnik M (2008) Concurrent triple-scale simulation of molecular liquids. J Chem Phys 128:114110-1-114110-9
41. Ayton GS, Voth GA (2009) Hybrid coarsegraining approach for lipid bilayers at large length and time scales. J Phys Chem B 113:4413-4424
42. Peter C, Kremer K (2009) Multiscale simulation of soft matter systems -from the atomistic to the coarse-grained level and back. Soft Matter 5:4357-4366
43. Murtola T, Bunker A, Vattulainen IV, Deserno M, Karttunen M (2009) Multiscale modeling of emergent materials: biological and soft matter. Phys Chem Chem Phys 11:1869-1892
44. Bennun SV, Hoopes MI, Xing C, Faller R (2009) Coarse-grained modeling of lipids. Chem Phys Lipids 159:59-66
45. Berendsen HJC (2009) Concluding remarks. Faraday Discuss 144:467-481
46. Marrink SJ, de Vries AH, Tieleman DP (2009) Lipids on the move: simulations of membrane pores, domains, stalks, and curves. Biochim Biophys Acta 1788:149-168
47. Goetz R, Lipowsky R (1998) Computer simulations of bilayer membranes: selfassembly and interfacial tension. J Chem Phys 108:7397-7409
48. Wu R, Deng M, Kong B, Yang X (2009) Coarse-grained molecular dynamics simulation of ammonium surfactant self-Assemblies: micelles and vesicles. J Phys Chem B 113:15010-15016
49. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH (2007) The MARTINI force field: coarse-grained model for biomolecular simulations. J Phys Chem B 111:7812-7824
50. Markvoort AJ, Smeijers AF, Pieterse K, van Santen RA, Hilbers PAJ (2007) Lipid-based mechanisms for vesicle fission. J Phys Chem B 111:5719-5725
51. Noguchi H, Takasu M (2001) Self-Assembly of amphiphiles into vesicles: a Brownian dynamics simulation. Phys Rev E 64:041913-1-041913-7
52. Farago O (2003) "Water-free" computer model for fluid bilayer membranes. J Chem Phys 119:596-605
53. Brannigan G, Brown FLH (2004) Solventfree simulations of fluid membrane bilayers. J Chem Phys 120:1059-1071
54. Cooke IR, Kremer K, Deserno M (2005) Tunable generic model for fluid bilayer membranes. Phys Rev E 72:011506-1-011506-4
55. Wang Z-J, Deserno M (2010) A systematically coarse-grained solvent-free model for quantitative phospholipid bilayer simulations. J Phys Chem B 114:11207-11220
56. Hoogerbrugge PJ, Koelman JMVA (1992) Simulating microscopic hydrodynamic phenomena with Dissipative Particle Dynamics. Europhys Lett 19:155-160
57. Espagnol P, Warren PB (1995) Statistical properties of Dissipative Particle Dynamics. Europhys Lett 30:191-196
58. Groot RD, Warren PB (1997) Dissipative Particle Dynamics: bridging the gap between atomistic and mesoscopic simulation. J Chem Phys 107:4423-4435
59. Venturoli M, Smit B (1999) Simulating the self-Assembly of model membranes. Phys Chem Commun 10:1-10
60. Shillcock JC, Lipowsky R (2002) Equilibrium structure and lateral stress distribution of amphiphilic bilayers from Dissipative Particle Dynamics simulations. J Chem Phys 117:5048-5061
61. Shillcock JC, Lipowsky R (2006) The computational route from bilayer membranes to vesicle fusion. J Phys Condens Matter 18: S1191-S1219
62. Schmid F (2009) Toy amphiphiles on the computer: what can we learn from generic models? Macromol Rapid Commun 30:741-751
63. Venturoli M, Sperotto MM, Kranenburg M, Smit B (2006) Mesoscopic models of biological membranes. Physics Reports 437:1-54
64. Muller M, Katsov K, Schick M (2006) Biological and synthetic membranes: what can be learned from a coarse-grained description? Physics Reports 434:113-176
65. Fuchslin RM, Maeke T, McCaskill JS (2009) Spatially resolved simulations of membrane reactions and dynamics: multipolar reaction DPD. Eur Phys J E 29:431-448
66. Laughlin RB, Pines D, Schmalian J, Stojkovic BP, Wolynes P (2000) The middle way. PNAS 97:32-37
67. Lipowsky R, Leibler S (1986) Unbinding transitions of interacting membranes. Phys Rev Lett 56:2541-2544
68. Safinya CR, Roux D, Smith GS, Sinha SK, Dimon P, Clark NA, Bellocq AM (1986) Steric interactions in a model multimembrane system: a synchrotron X-ray study. Phys Rev Lett 57:2718-2721
69. Jakobsen AF, Mouritsen OG, Besold G (2005) Artifacts in dynamical simulations of coarse-grained lipid bilayers. J Chem Phys 122:204901-1-204901-11
70. Allen MP (2006) Configurational temperature in membrane simulations using dissipative particle Dynamics. J Phys Chem B 110:3823-3830
71. Larson RG (1989) Self-Assembly of surfactant liquid crystalline phases by Monte Carlo simulation J Chem Phys 91:2479-2488
72. Drouffe J-M, Maggs AC, Leibler S (1991) Computer simulations of self-Assembled membranes. Science 254:1353-1356
73. Smit B, Hilbers PAJ, Esselink K, Rupert LAM, van Os NM, Schlijper AG (1990) Computer simulations of a water/oil interface in the presences of micelles. Nature 348:624-625
74. Tieleman DP, van der Spoel D, Berendsen HJC (2000) Molecular dynamics simulations of dodecylphosphocholine micelles at three different aggregate sizes: micellar structure and chain relaxation. J Phys Chem B 104:6380-6388
75. Marrink SJ, Lindahl E, Edholm O, Mark AE (2001) Simulation of the spontaneous aggregation of phospholipids into bilayers. JACS 123:8638-8639
76. Nielsen M, Miao L, Ipsen JH, Zuckermann MJ, Mouritsen OG (1999) Off-lattice model for the phase behavior of lipid-cholesterol bilayers. Phys Rev E 59:5790-5803
77. Marrink SJ, Mark AE (2003) Molecular dynamics simulation of the formation, structure and dynamics of small phospholipid vesicles. JACS 125:15233-15242
78. de Vries AH, Mark AM, Marrink SJ (2004) Molecular dynamics simulation of the spontaneous formation of a small DPPC vesicle in water in atomistic detail. JACS 126:4488-4489
79. Risselada HJ, Mark AE, Marrink SJ (2008) Application of mean field boundary potentials in simulations of lipid vesicles. J Phys Chem B 112:7438-7447
80. Bernardes AT (1996) Computer simulations of spontaneous vesicle formation. Langmuir 12:5763-5767
81. Huang J, Wang Y, Qian C (2009) Simulation study on the formation of vesicle and influence of solvent. J Chem Phys 131:234902-1-234902-5
82. Sevink GJA, Zvelindovsky AV (2005) Self-Assembly of complex vesicles. Macromolecules 38:7502-7513
83. He X, Schmid F (2006) Dynamics of spontaneous vesicle formation in dilute solutions of amphiphilic diblock copolymers. Macromolecules 39:2654-2662
84. Pogodin S, Baulin VA (2010) Coarse-grained models of biological membranes within the single chain mean field theory. Soft Matter 6:1-12
85. Yamamoto S, Maruyama Y, Hyodo S (2002) Dissipative Particle Dynamics study of spontaneous vesicle formation of amphiphilic molecules. J Chem Phys 116:5842-5849
86. Grafmuller A, Shillcock J, Lipowsky R (2009) The fusion of membranes and vesicles: pathway and energy barriers from Dissipative Particle Dynamics. Biophys J 96:2658-2675
87. Discher BM, Won YY, Ege DS, Lee JCM, Bates FS, Discher DE, Hammer DA (1999) Polymersomes: tough vesicles made from diblock copolymers. Science 284:1143-1146
88. Yu S, Azzam T, Rouiller I, Eisenberg A (2009) Breathing vesicles. JACS 131:10557-10566
89. Ortiz V, Nielsen SO, Discher DE, Klein ML, Lipowsky R, Shillcock J (2005) Dissipative Particle Dynamics simulations of polymersomes. J Phys Chem B 109:17708-17714
90. Srinivas G, Discher DE, Klein ML (2004) Self-Assembly and properties of diblock copolymers by coarse-grained molecular dynamics. Nat Mater 3:638-644
91. Meleard P, Gerbeaud C, Pott T, Fernandez-Puente L, Bivas I, Mitov MD, Dufourcq J, Bothore P (1997) Bending elasticities of model membranes: influences of temperature and sterol content. Biophys J 72:2616-2629
92. Illya G, Lipowsky R, Shillcock JC (2005) Effect of chain length and asymmetry on material properties of bilayer membranes. J Chem Phys 122:244901-1-224901-6
93. Schofield P, Henderson JR (1982) Statistical mechanics of inhomogeneous fluids. Proc R Soc London A 379:231-246
94. Templer RH, Castle SJ, Curran AR, Rumbles G, Klug DR (1998) Seeing isothermal changes in the lateral pressure in model membanes using di-pyrenyl phosphatidylcholine. Faraday Disc 111:41-53
95. Cantor RS (1999) Lipid composition and the lateral pressure profile in bilayers. Biophys J 76:2625-2639
96. Cantor RS (2001) Breaking the Meyer-Overton rule: predicted effects of varying stiffness and interfacial activity on the intrinsic potency of anesthetics. Biophys J 80:2284-2297
97. Sonne J, Hansen FY, Peters GH (2005) Methodological problems in pressure profile calculations for lipid bilayers. J Chem Phys 122:124903-1-124903-9
98. Cantor RS (2002) Size distribution of barrelstave aggregates of membrane peptides: influence of the bilayer lateral pressure profile. Biophys J 82:2520-2525
99. Lindahl E, Edholm O (2000) Spatial and energetic-entropic decomposition of surface tension in lipid bilayers from Molecular Dynamics simulations. J Chem Phys 113:3882-3893
100. Gullingsrud J, Schulten K (2004) Lipid bilayer pressure profiles and mechanosensitive channel gating. Biophys J 86:3496-3509
101. Ollila OHS, Risselada HJ, Louhivuori M, Lindahl E, Vattulainen I, Marrink SJ (2009) 3D pressure field in lipid membranes and membrane-protein complexes. Phys Rev Lett 102:078101-1-078101-4
102. Jørgensen K, Mouritsen OG (1995) Phase separation dynamics and lateral organization of two-component lipid membranes. Biophys J 69:942-954
103. Wu SH, McConnell HM (1975) Phase separations in phospholipid membranes. Biochemistry 14:847-854
104. Wilkinson DA, Nagle JF (1979) Dilatometric study of binary mixtures of phosphatidylcholines. Biochemistry 18:4244-4249
105. Bagatolli LA, Gratton E (2000) A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: a two-photon fluorescence microscopy study. Biophys J 79:434-447
106. Illya G, Lipowsky R, Shillcock JC (2006) Two-component membrane material properties and domain formation from Dissipative Particle Dynamics. J Chem Phys 125:114710-1-114710-9
107. Yamamoto S, Hyodo S (2003) Budding and fission dynamics of two-component vesicles. J Chem Phys 118:7937-7943
108. Laradji M, Sunil Kumar PB (2005) Domain growth, budding, and fission in phaseseparating self-Assembled fluid bilayers. J Chem Phys 123:224902-1-224902- 10
109. Venturoli M, Smit B, Sperotto MM (2005) Simulation studies of protein-induced bilayer deformations, and lipid-induced protein tilting, on a mesoscopic model for lipid bilayers with embedded proteins. Biophys J 88:1778-1798
110. Schmidt U, Guigas G, Weiss M (2008) Cluster formation of transmembrane proteins due to hydrophobic mismatching. Phys Rev Lett 101:128104-1-128104-4
111. Li L, Davande H, Bedrov D, Smith GD (2007) A molecular dynamics simulation study of C60 fullerenes inside a dimyristoylphosphatidylcholine lipid bilayer. J Phys Chem B 111:4067-4072
112. Monticelli L, Salonen E, Ke PC, Vattulainen I (2009) Effects of carbon nanoparticles on lipid membranes: a molecular simulation perspective. Soft Matter 5:4433-4445
113. Wong-Ekkabut J, Baoukina S, Triampo W, Tang I-M, Tieleman DP, Monticelli L (2008) Computer simulation study of fullerene translocation through lipid membranes. Nat Nanotechnol 3:363-368
114. Chiu CC, deVane R, Klein ML, Shinoda W, Moore PB, Nielsen SO (2010) Coarsegrained potential models for phenyl-based molecules: II. application to fullerenes. J Phys Chem B 114:6394-6400
115. Smith KA, Jasnow D, Balazs AC (2007) Designing synthetic vesicles that engulf nanoscopic particles. J Chem Phys 127:084703-1-084703-10
116. Yang K, Ma Y-Q (2010) Computer simulation of the translocation of nanoparticles with different shapes across a lipid bilayer. Nature Nantechnology 5:579-583
117. Graham TR, Kozlov MM (2010) Interplay of proteins and lipids in generating membrane curvature. Curr Op Cell Biology 22:430-436
118. Wu S, Guo H (2009) Simulation study of protein-mediated vesicle fusion. J Phys Chem B 113:589-591
119. Reynwar BJ, Illya G, Harmandaris VA,Muller MM, Kremer K, DesernoM(2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447:461-464
120. Chanturiya A, Chernomordik LV, Zimmerberg J (1997) Flickering fusion pores comparable with initial exocytotic pores occur in protein-free phospholipid bilayers. PNAS 94:14423-14428
121. Lentz BR, Lee J (1999) Poly(ethylene glycol) (PEG)-mediated fusion between pure lipid bilayers: a mechanism in common with viral fusion and secretory vesicle release? Mol Membrane Biol 16:279-296
122. Safran SA, Kuhl TL, Israelachvili JN (2001) Polymer-induced membrane contraction, phase separation, and fusion via Marangoni flow. Biophys J 81:659-666
123. Bentz J, Alford D, Cohen J, Duzgunes N (1988) La3+ induced fusion of phosphatidylserine liposomes. Biophys J 53:593-607
124. Haluska CK, Riske KA, Marchi-Artzner V, Lehn J-M, Lipowsky R, Dimova R (2006) Time scales of membrane fusion revealed by direct imaging of vesicle fusion with high temporal resolution. PNAS 103:15841-15846
125. Sunami T, Caschera F, Morita Y, Toyota T, Nishimura K, Matsuura T, Suzuki H, Hanczyc MM, Yomo T (2010) Detection of association and fusion of giant vesicles using a fluorescence-Activated cell sorter. Langmuir. 26:15098-15103
126. Dimova R, Bezlyepkina N, Jordo MD, Knorr RL, Riske KA, Staykova M, Vlahovska PM, Yamamoto T, Yang P, Lipowsky R (2009) Vesicles in electric fields: some novel aspects of membrane behavior. Soft Matter 5:3201-3212
127. Hu C, Ahmed M, Melia TJ, Sollner TH, Mayer T, Rothman JE (2003) Fusion of cells by flipped SNAREs. Science 300:1745-1748
128. Yang L, Huang HW (2002) Observation of a membrane fusion intermediate structure. Science 297:1877-1879
129. McNew JA (2008) Regulation of SNAREmediated membrane fusion during exocytosis. Chem Rev 108:1669-1686
130. Thorley JA, McKeating JA, Rappoport JZ (2010) Mechanisms of viral entry: sneaking in the front door. Protoplasma 244:15-24
131. St. Vincent MR, Colpitts CC, Ustinov AV, Muqadas M, Joyce MA, Barsby NL, Epand RF, Epand RM, Khramyshev SA, Valueva OA, Korshun VA, Tyrrell DLJ, Schang LM (2010) Rigid amphipathic fusion inhibitors, small molecule antiviral compounds against enveloped viruses. PNAS 107:17339-17344
132. Jahn R, Lang T, Sudhof TC (2003) Membrane fusion. Cell 112:519-533
133. Yang Y, Kurteva S, Ren X, Lee S, Sodroski J (2005) Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1. J of Virology 79:12132-12147
134. Mohrmann R, de Wit H, Verhage M, Neher E, Sørensen JB (2010) Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 330:502-505
135. Tamm LK, Crane J, Kiessling V (2003) Membrane fusion: a structural perspective on the interplay of lipids and proteins. Curr Op Struct Biol 13:453-466
136. Chernomordik LV, Zimmerberg J, KozlovMM (2006) Membranes of the world unite. J Cell Biology 175:201-207
137. Lindau M, de Toledo GA (2003) The fusion pore. Biochim Biophys Acta 1641:167-173
138. Han X, Wang C-T, Bai J, Chapman ER, Jackson MB (2004) Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science 304:289-292
139. Szule JA, Coorssen JR (2004) Comment on Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science 306:813b
140. Han X, Jackson MB (2004) Response to comment on Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science 306:813c
141. Carr CM, Rizo J (2010) At the junction of SNARE and SM protein function. Curr Op Cell Biol 22:488-495
142. Coorssen JR, Blank PS, Albertorio F, Bezrukov L, Kolosova I, Chen X, Backlund PS Jr., Zimmerberg J (2003) Regulared secretion: SNARE density, vesicle fusion and calcium dependence. J Cell Science 116:2087-2096
143. Kozlov MM, Markin VS (1983) Possible mechanism of membrane fusion. Biofizika 28:243-247
144. Chernomordik LV, Melikyan GB, Chizmadzhev YA (1987) Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim Biophys Acta 906:309-352
145. Siegel DP (1993) Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophys J 65:2124-2140
146. Kozlovsky Y, KozlovMM(2002) Stalk model of membrane fusion: solution of energy crisis. Biophys J 82:882-895
147. Markin VS, Albanesi JP (2002) Membrane fusion: stalk model revisited. Biophys J 82:693-712
148. Tajparast M, Glavinović MI (2009) Forces and stresses acting on fusion pore membrane during secretion. Biochim Biophys Acta 1788:1009-1023
149. Chernomordik LV, Kozlov MM (2005) Membrane hemifusion: crossing a chasm in two leaps. Cell 123:375-382
150. Efrat A, Chernomordik L, Kozlov MM (2007) Point-like protrusion as a pre-stalk intermediate in membrane fusion pathway. Biophys J 92:L61-L63
151. Lipowsky R, Grotehans S (1993) Hydration vs protrusion forces between lipid bilayers. Europhys Lett 23:599-604
152. Woodbury DJ (1989) Pure lipid vesicles can induce channel-like conductances in planar bilayers. J Membrane Biol 109:145-150
153. Heimburg T (2010) Lipid ion channels. Biophys Chem 150:2-22
154. Marrink SJ,MarkAE(2003)Themechanismof vesicle fusion as revealed bymolecular dynamics simulations. JACS 125:11144-11145
155. Stevens MJ, Hoh JH, Woolf TB (2003) Insights into the molecular mechanism of membrane fusion from simulation: evidence for the association of splayed tails. Phys Rev Lett 91:188102-1-188102-4
156. 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 Comput Biol 6: e1000829
157. Smirnova YG, Marrink SJ, Lipowsky R, Knecht V (2009) Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. JACS 132:6710-6718
158. Mirjanian D, Dickey AN, Hoh JH, Woolf TB, Stevens MJ (2010) Splaying of aliphatic tails plays a central role in barrier crossing during liposome fusion. J Phys Chem B 114:11061-11068
159. Noguchi H, Takasu M (2001) Fusion pathways of vesicles: a Brownian dynamics simulation. J Chem Phys 115:9547-9551
160. Shillcock JC, Lipowsky R (2005) Tensioninduced fusion of bilayer membranes and vesicles. Nat Mater 4:225-228
161. Gao L, Lipowsky R, Shillcock JC (2008) Tension-induced vesicle fusion: pathways and pore dynamics. Soft Matter 4:1208-1214
162. Liu Y-T, Zhao Y, Liu H, Liu Y-H, Lu Z-Y (2009) Spontaneous fusion between the vesicles formed by A2n(B2)n type comb-like block copolymers with a semiflexible hydrophobic backbone. J Phys Chem B 113:15256-15262
163. Li X, Liu Y, Wang L, Deng M, Liang H (2009) Fusion and fission pathways of vesicles from amphiphilic triblock copolymers: a dissipative particle dynamics simulation study. Phys Chem Chem Phys 11:4051-4059
164. Muller M, Katsov K, Schick M (2003) A new mechanism of model membrane fusion determined from Monte Carlo simulation. Biophys J 85:1611-1623
165. Schick M, Katsov K, Muller M (2005) The central role of line tension in the fusion of biological membranes. Mol Phys 103:3055-3059
166. Kinnunen PKJ (1992) Fusion of lipid bilayers: a model involving mechanistic connection to HII phase forming lipids. Chem Phys Lipids 63:251-258
167. Holopainen JM, Lehtonen JYA, Kinnunen PKJ (1999) Evidence for the extended phospholipid conformation in membrane fusion and hemifusion. Biophys J 76:2111-2120
168. Kinnunen PKJ, Holopainen JM (2000) Mechanisms of initiation of membrane fusion: role of lipids. Biosci Rep 20:465-482
169. Stein A, Weber G, Wahl MC, Jahn R (2009) Helical extension of the neuronal SNARE complex into the membrane. Nature 460:525-528
170. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachi M, Parlati F, Sollner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759-772
171. Pang ZP, Sudhof TC (2010) Cell biology of Ca2+-triggered exocytosis. Curr Op Cell Biology 22:496-505
172. Knecht V, Grubmuller H (2003) Mechanical coupling via the membrane fusion SNARE protein Syntaxin 1A: a molecular dynamics study. Biophys J 84:1527-1547
173. McNew JA, Weber T, Parlati F, Johnston RJ, Melia TJ, Sollner TH, Rothman JE (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
174. Yersin A, Hirling H, Steiner P, Magnin S, Regazzi R, Huni B, Huguenot P, de Los RP, Dietler G, Catsicas S, Kasas S (2003) Interactions between synaptic vesicle fusion proteins explored by atomic force microscopy. PNAS 100:8736-8741
175. Abdulreda MH, Bhalla A, Rico F, Berggren PO, Chapman ER, Moy VT (2009) Pulling force generated by interacting SNAREs facilitates membrane hemifusion. Integr Biol 1:301-310