Functional relevance of transmembrane domains in membrane fusion

Biological Chemistry

Volumn 393, Issue 11, 2012, Pages 1231-1245

  Nikolaus, Jorg ^a   Herrmann, Andreas ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Hemifusion; Membrane fusion; SNAREs; Stalk; Transmembrane domain; Viral fusogens

Indexed keywords

CHLORPROMAZINE; CHOLESTEROL; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE FUSION PROTEIN; MEMBRANE LIPID; MEMBRANE PROTEIN; SNARE PROTEIN; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; CELL FUSION; CELL MEMBRANE; CHANNEL GATING; CHIMERA; DIMERIZATION; EXOCYTOSIS; HYDROPHOBICITY; MEMBRANE FUSION; MOLECULAR DYNAMICS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

CELL MEMBRANE; HUMANS; MEMBRANE FUSION; MEMBRANE PROTEINS; MODELS, BIOLOGICAL;

EID: 84869394975     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0220     Document Type: Review

References (155)

1. Abdulreda, M.H., Bhalla, A., Chapman, E.R., and Moy, V.T. (2008). Atomic force microscope spectroscopy reveals a hemifusion intermediate during soluble N-ethylmaleimide-sensitive factor attachment protein receptors-mediated membrane fusion. Biophys. J. 94, 648-655.
2. Amatore, C., Arbault, S., Bouret, Y., Guille, M., Lemaitre, F., and Verchier, Y. (2006). Regulation of exocytosis in chromaffin cells by trans -insertion of lysophosphatidylcholine and arachidonic acid into the outer leaflet of the cell membrane. ChemBioChem 7, 1998-2003.
3. Apel, C.L., Deamer, D.W., and Mautner, M.N. (2002). Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. Biochim. Biophys. Acta 1559, 1-9.
4. Armstrong, R.T., Kushnir, A.S., and White, J.M. (2000). The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J. Cell Biol. 151, 425-437.
5. Avinoam, O. and Podbilewicz, B. (2011). Eukaryotic cell-cell fusion families. Curr. Top. Membr. 68, 209-234.
6. Bissonnette, M.L., Donald, J.E., DeGrado, W.F., Jardetzky, T.S., and Lamb, R.A. (2009). Functional analysis of the transmembrane domain in paramyxovirus F protein-mediated membrane fusion. J. Mol. Biol. 386, 14-36.
7. Biswas, S., Yin, S.R., Blank, P.S., and Zimmerberg, J. (2008). Cholesterol promotes hemifusion and pore widening in membrane fusion induced by influenza hemagglutinin. J. Gen. Physiol. 131, 503-513.
8. Bowen, M. and Brunger, A.T. (2006). Conformation of the synaptobrevin transmembrane domain. Proc. Natl. Acad. Sci. USA 103, 8378-8383.
9. Bradshaw, J.P., Darkes, M.J., Harroun, T.A., Katsaras, J., and Epand, R.M. (2000). Oblique membrane insertion of viral fusion peptide probed by neutron diffraction. Biochemistry 39, 6581-6585.
10. Callebaut, I., Tasso, A., Brasseur, R., Burny, A., Portetelle, D., and Mornon, J.P. (1994). Common prevalence of alanine and glycine in mobile reactive centre loops of serpins and viral fusion peptides: do prions possess a fusion peptide? J. Comput. Aided Mol. Des. 8, 175-191.
11. Chang, D.K., Cheng, S.F., Kantchev, E.A., Lin, C.H., and Liu, Y.T. (2008). Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex. BMC Biol. 6, 2.
12. Chernomordik, L.V. and Kozlov, M.M. (2003). Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175-207.
13. Chernomordik, L.V. and Kozlov, M.M. (2005). Membrane hemifusion: crossing a chasm in two leaps. Cell 123, 375-382.
14. Chernomordik, L.V. and Kozlov, M.M. (2008). Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15, 675-683.
15. Chernomordik, L.V., Melikyan, G.B., and Chizmadzhev, Y.A. (1987). Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906, 309-352.
16. Chernomordik, L.V., Vogel, S.S., Sokoloff, A., Onaran, H.O., Leikina, E.A., and Zimmerberg, J. (1993). Lysolipids reversibly inhibit Ca 2 + -, GTP-and pH-dependent fusion of biological membranes. FEBS Lett. 318, 71-76.
17. Chernomordik, L., Chanturiya, A., Green, J., and Zimmerberg, J. (1995). The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys. J. 69, 922-929.
18. Chernomordik, L.V., Frolov, V.A., Leikina, E., Bronk, P., and Zimmerberg, J. (1998). The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. J. Cell Biol. 140, 1369-1382.
19. Chernomordik, L.V., Zimmerberg, J., and Kozlov, M.M. (2006). Membranes of the world unite! J. Cell Biol. 175, 201-207.
20. Churchward, M.A., Rogasevskaia, T., Hofgen, J., Bau, J., and Coorssen, J.R. (2005). Cholesterol facilitates the native mechanism of Ca 2 + -triggered membrane fusion. J. Cell Sci. 118, 4833-4848.
21. Clancy, E.K. and Duncan, R. (2011). Helix-destabilizing, β-branched, and polar residues in the baboon reovirus p15 transmembrane domain influence the modularity of FAST proteins. J. Virol. 85, 4707-4719.
22. Cleverley, D.Z. and Lenard, J. (1998). The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 95, 3425-3430.
23. Cleverley, D.Z., Geller, H.M., and Lenard, J. (1997). Characterization of cholesterol-free insect cells infectible by baculoviruses: effects of cholesterol on VSV fusion and infectivity and on cytotoxicity induced by influenza M2 protein. Exp Cell Res 233, 288-296.
24. Cohen, F.S., Zimmerberg, J., and Finkelstein, A. (1980). Fusion of phospholipid vesicles with planar phospholipid bilayer membranes. II. Incorporation of a vesicular membrane marker into the planar membrane. J. Gen. Physiol. 75, 251-270.
25. Davies, S.M., Kelly, S.M., Price, N.C., and Bradshaw, J.P. (1998). Structural plasticity of the feline leukaemia virus fusion peptide: a circular dichroism study. FEBS Lett. 425, 415-418.
26. Dennison, S.M., Greenfield, N., Lenard, J., and Lentz, B.R. (2002). VSV transmembrane domain (TMD) peptide promotes PEG-mediated fusion of liposomes in a conformationally sensitive fashion. Biochemistry 41, 14925-14934.
27. Dennison, S.M., Bowen, M.E., Brunger, A.T., and Lentz, B.R. (2006). Neuronal SNAREs do not trigger fusion between synthetic membranes but do promote PEG-mediated membrane fusion. Biophys. J. 90, 1661-1675.
28. Domanska, M.K., Kiessling, V., Stein, A., Fasshauer, D., and Tamm, L.K. (2009). Single vesicle millisecond fusion kinetics reveals number of SNARE complexes optimal for fast SNAREmediated membrane fusion. J. Biol. Chem. 284, 32158-32166.
29. Donald, J.E., Zhang, Y., Fiorin, G., Carnevale, V., Slochower, D.R., Gai, F., Klein, M.L., and DeGrado, W.F. (2011). Transmembrane orientation and possible role of the fusogenic peptide from parainfluenza virus 5 (PIV5) in promoting fusion. Proc. Natl. Acad. Sci. USA 108, 3958-3963.
30. Efrat, A., Chernomordik, L.V., and Kozlov, M.M. (2007). Point-like protrusion as a prestalk intermediate in membrane fusion pathway. Biophys. J. 92, L61-L63.
31. Engel, S., Scolari, S., Thaa, B., Krebs, N., Korte, T., Herrmann, A., and Veit, M. (2010). FLIM-FRET and FRAP reveal association of influenza virus haemagglutinin with membrane rafts. Biochem. J. 425, 567-573.
32. 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. USA 95, 15781-15786.
33. Fdez, E., Martinez-Salvador, M., Beard, M., Woodman, P., and Hilfiker, S. (2010). Transmembrane-domain determinants for SNARE-mediated membrane fusion. J. Cell Sci. 123, 2473-2480.
34. Fix, M., Melia, T.J., Jaiswal, J.K., Rappoport, J.Z., You, D., Sollner, T.H., Rothman, J.E., and Simon, S.M. (2004). Imaging single membrane fusion events mediated by SNARE proteins. Proc. Natl. Acad. Sci. USA 101, 7311-7316.
35. Gaudin, Y. (2000). Rabies virus-induced membrane fusion pathway. J. Cell Biol. 150, 601-612.
36. Gibbons, D.L., Vaney, M.C., Roussel, A., Vigouroux, A., Reilly, B., Lepault, J., Kielian, M., and Rey, F.A. (2004). Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427, 320-325.
37. Giraudo, C.G., Hu, C., You, D., Slovic, A.M., Mosharov, E.V., Sulzer, D., Melia, T.J., and Rothman, J.E. (2005). SNAREs can promote complete fusion and hemifusion as alternative outcomes. J. Cell Biol. 170, 249-260.
38. Grafmuller, A., Shillcock, J., and Lipowsky, R. (2007). Pathway of membrane fusion with two tension-dependent energy barriers. Phys. Rev. Lett. 98, 218101.
39. Grafmuller, A., Shillcock, J., and Lipowsky, R. (2009). The fusion of membranes and vesicles: pathway and energy barriers from dissipative particle dynamics. Biophys. J. 96, 2658-2675.
40. Graham, T.R. and Kozlov, M.M. (2010). Interplay of proteins and lipids in generating membrane curvature. Curr. Opin. Cell Biol. 22, 430-436.
41. 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.
42. Han, X., Steinhauer, D.A., Wharton, S.A., and Tamm, L.K. (1999). Interaction of mutant influenza virus hemagglutinin fusion peptides with lipid bilayers: probing the role of hydrophobic residue size in the central region of the fusion peptide. Biochemistry 38, 15052-15059.
43. Harrison, S.C. (2008). Viral membrane fusion. Nat. Struct. Mol. Biol. 15, 690-698.
44. Helfrich, W. (1973). Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C. 28, 693-703.
45. Hess, S.T., Gould, T.J., Gudheti, M.V., Maas, S.A., Mills, K.D., and Zimmerberg, J. (2007). Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc. Natl. Acad. Sci. USA 104, 17370-17375.
46. Hofmann, M.W., Weise, K., Ollesch, J., Agrawal, P., Stalz, H., Stelzer, W., Hulsbergen, F., de Groot, H., Gerwert, K., Reed, J. et al. (2004). De novo design of conformationally flexible transmembrane peptides driving membrane fusion. Proc. Natl. Acad. Sci. USA 101, 14776-14781.
47. 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-tofusion transition. J. Mol. Biol. 364, 1048-1060.
48. Jackson, M.B. and Chapman, E.R. (2006). Fusion pores and fusion machines in Ca 2 + -triggered exocytosis. Annu. Rev. Biophys. Biomol. Struct. 35, 135-160.
49. Jahn, R. and Scheller, R.H. (2006). SNAREs-engines for membrane fusion. Nature reviews. Mol. Cell Biol. 7, 631-643.
50. Jun, Y. and Wickner, W. (2007). Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc. Natl. Acad. Sci. USA 104, 13010-13015.
51. Karatekin, E., Di Giovanni, J., Iborra, C., Coleman, J., O'shaughnessy, B., Seagar, M., and Rothman, J.E. (2010). A fast, single-vesicle fusion assay mimics physiological SNARE requirements. Proc. Natl. Acad. Sci. USA 107, 3517-3521.
52. Kasson, P.M., Kelley, N.W., Singhal, N., Vrljic, M., Brunger, A.T., and Pande, V.S. (2006). Ensemble molecular dynamics yields submillisecond kinetics and intermediates of membrane fusion. Proc. Natl. Acad. Sci. USA 103, 11916-11921.
53. Kasson, P.M., Zomorodian, A., Park, S., Singhal, N., Guibas, L.J., and Pande, V.S. (2007). Persistent voids: a new structural metric for membrane fusion. Bioinformatics 23, 1753-1759.
54. Kasson, P.M., Lindahl, E., and Pande, V.S. (2010). Atomic-resolution simulations predict a transition state for vesicle fusion defined by contact of a few lipid tails. PLoS Comput. Biol. 6, e1000829.
55. Katsov, K., Muller, M., and Schick, M. (2004). Field theoretic study of bilayer membrane fusion. I. Hemifusion mechanism. Biophys. J. 87, 3277-3290.
56. Katsov, K., Muller, M., and Schick, M. (2006). Field theoretic study of bilayer membrane fusion: II. Mechanism of a stalk-hole complex. Biophys. J. 90, 915-926.
57. Kemble, G.W., Danieli, T., and White, J.M. (1994). Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76, 383-391.
58. Kesavan, J., Borisovska, M., and Bruns, D. (2007). v-SNARE actions during Ca 2 + -triggered exocytosis. Cell 131, 351-363.
59. Kinnunen, P.K. (1992). Fusion of lipid bilayers: a model involving mechanistic connection to HII phase forming lipids. Chem. Phys. Lipids 63, 251-258.
60. Knecht, V. and Grubmuller, H. (2003). Mechanical coupling via the membrane fusion SNARE protein syntaxin 1A: a molecular dynamics study. Biophys. J. 84, 1527-1547.
61. Knecht, V. and Marrink, S.J. (2007). Molecular dynamics simulations of lipid vesicle fusion in atomic detail. Biophys. J. 92, 4254-4261.
62. Knecht, V., Mark, A.E., and Marrink, S.J. (2006). Phase behavior of a phospholipid/fatty acid/water mixture studied in atomic detail. J. Am. Chem. Soc. 128, 2030-2034.
63. Koehorst, R.B., Spruijt, R.B., Vergeldt, F.J., and Hemminga, M.A. (2004). Lipid bilayer topology of the transmembrane β-helix of M13 Major coat protein and bilayer polarity profile by site-directed fluorescence spectroscopy. Biophys. J. 87, 1445-1455.
64. Kozerski, C., Ponimaskin, E., Schroth-Diez, B., Schmidt, M.F., and Herrmann, A. (2000). Modification of the cytoplasmic domain of influenza virus hemagglutinin affects enlargement of the fusion pore. J. Virol. 74, 7529-7537.
65. Kozlov, M.M. and Markin, V.S. (1983). Possible mechanism of membrane fusion. Biofizika 28, 242-247.
66. Kozlov, M.M. and Chernomordik, L.V. (1998). A mechanism of protein-mediated fusion: coupling between refolding of the influenza hemagglutinin and lipid rearrangements. Biophys. J. 75, 1384-1396.
67. Kozlov, M.M., McMahon, H.T., and Chernomordik, L.V. (2010). Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35, 699-706.
68. Kozlovsky, Y. and Kozlov, M.M. (2002). Stalk model of membrane fusion: solution of energy crisis. Biophys. J. 82, 882-895.
69. Kozlovsky, Y., Chernomordik, L.V., and Kozlov, M.M. (2002). Lipid intermediates in membrane fusion: formation, structure, and decay of hemifusion diaphragm. Biophys. J. 83, 2634-2651.
70. Kucerka, N., Perlmutter, J.D., Pan, J., Tristram-Nagle, S., Katsaras, J., and Sachs, J.N. (2008). The effect of cholesterol on short-and long-chain monounsaturated lipid bilayers as determined by molecular dynamics simulations and X-ray scattering. Biophys. J. 95, 2792-2805.
71. Kuzmin, P.I., Zimmerberg, J., Chizmadzhev, Y.A., and Cohen, F.S. (2001). A quantitative model for membrane fusion based on low-energy intermediates. Proc. Natl. Acad. Sci. USA 98, 7235-7240.
72. Langosch, D. and Heringa, J. (1998). Interaction of transmembrane helices by a knobs-into-holes packing characteristic of soluble coiled coils. Proteins 31, 150-159.
73. Langosch, D., Brosig, B., and Pipkorn, R. (2001a). Peptide mimics of the vesicular stomatitis virus G-protein transmembrane segment drive membrane fusion in vitro . J. Biol. Chem. 276, 32016-32021.
74. Langosch, D., Crane, J.M., Brosig, B., Hellwig, A., Tamm, L.K., and Reed, J. (2001b). Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. J. Mol. Biol. 311, 709-721.
75. Langosch, D., Hofmann, M., and Ungermann, C. (2007). The role of transmembrane domains in membrane fusion. Cell Mol. Life Sci. 64, 850-864.
76. Lee, J. and Lentz, B.R. (1997). Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusion. Biochemistry 36, 6251-6259.
77. Lee, J.Y. and Schick, M. (2007). Field theoretic study of bilayer membrane fusion III: membranes with leaves of different composition. Biophys. J. 92, 3938-3948.
78. Lei, G. and MacDonald, R.C. (2003). Lipid bilayer vesicle fusion: intermediates captured by high-speed microfluorescence spectroscopy. Biophys. J. 85, 1585-1599.
79. Li, S.C. and Deber, C.M. (1992). Influence of glycine residues on peptide conformation in membrane environments. Int. J. Pept. Protein Res. 40, 243-248.
80. Li, D.W. and Liu, X.Y. (2005). Examination of membrane fusion by dissipative particle dynamics simulation and comparison with continuum elastic models. J. Chem. Phys. 122, 174909.
81. Lindau, M. and Almers, W. (1995). Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Curr. Opin. Cell Biol. 7, 509-517.
82. Liu, T., Wang, T., Chapman, E.R., and Weisshaar, J.C. (2008). Productive hemifusion intermediates in fast vesicle fusion driven by neuronal SNAREs. Biophys. J. 94, 1303-1314.
83. Lu, X., Zhang, F., McNew, J.A., and Shin, Y.K. (2005). Membrane fusion induced by neuronal SNAREs transits through hemifusion. J. Biol. Chem. 280, 30538-30541.
84. Luneberg, J., Martin, I., Nussler, F., Ruysschaert, J.M., and Herrmann, A. (1995). Structure and topology of the influenza virus fusion peptide in lipid bilayers. J. Biol. Chem. 270, 27606-27614.
85. Lygina, A.S., Meyenberg, K., Jahn, R., and Diederichsen, U. (2011). Transmembrane domain peptide/peptide nucleic acid hybrid as a model of a SNARE protein in vesicle fusion. Angew Chem. Int. Ed. 50, 8597-8601.
86. Margittai, M., Otto, H., and Jahn, R. (1999). A stable interaction between syntaxin 1a and synaptobrevin 2 mediated by their transmembrane domains. FEBS Lett. 446, 40-44.
87. Markosyan, R.M., Cohen, F.S., and Melikyan, G.B. (2000). The lipid-anchored ectodomain of influenza virus hemagglutinin (GPI-HA) is capable of inducing nonenlarging fusion pores. Mol. Biol. Cell 11, 1143-1152.
88. Markvoort, A.J. and Marrink, S.J. (2011). Lipid acrobatics in the membrane fusion arena. Curr. Top. Membr. 68, 259-294.
89. Marrink, S.J. and Mark, A.E. (2003). The mechanism of vesicle fusion as revealed by molecular dynamics simulations. J. Am. Chem. Soc. 125, 11144-11145.
90. Marrink, S.J. and Tieleman, D.P. (2002). Molecular dynamics simulation of spontaneous membrane fusion during a cubichexagonal phase transition. Biophys. J. 83, 2386-2392.
91. Marrink, S.J., de Vries, A.H., and Tieleman, D.P. (2009). Lipids on the move: simulations of membrane pores, domains, stalks and curves. Biochim. Biophys. Acta 1788, 149-168.
92. Martin, I., Schaal, H., Scheid, A., and Ruysschaert, J.M. (1996). Lipid membrane fusion induced by the human immunodeficiency virus type 1 gp41 N-terminal extremity is determined by its orientation in the lipid bilayer. J. Virol. 70, 298-304.
93. McNew, J.A., Weber, T., Engelman, D.M., Sollner, 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.
94. McNew, J.A., Weber, T., Parlati, F., Johnston, R.J., Melia, T.J., Sollner, T.H., and Rothman, J.E. (2000). Close is not enough: SNAREdependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150, 105-117.
95. Melikyan, G.B. (2010). Driving a wedge between viral lipids blocks infection. Proc. Natl. Acad. Sci. USA 107, 17069-17070.
96. Melikyan, G.B., White, J.M., and Cohen, F.S. (1995). GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131, 679-691.
97. Melikyan, G.B., Brener, S.A., Ok, D.C., and Cohen, F.S. (1997). Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion. J. Cell Biol. 136, 995-1005.
98. Melikyan, G.B., Lin, S., Roth, M.G., and Cohen, F.S. (1999). Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell 10, 1821-1836.
99. Mirjanian, D., Dickey, A.N., Hoh, J.H., Woolf, T.B., and Stevens, M.J. (2010). Splaying of Aliphatic tails plays a central role in barrier crossing during liposome fusion. J. Phys. Chem. B. 114, 11061-11068.
100. Montecucco, C., Schiavo, G., and Pantano, S. (2005). SNARE complexes and neuroexocytosis: how many, how close? Trends Biochem. Sci. 30, 367-372.
101. Muller, M., Katsov, K., and Schick, M. (2003). A new mechanism of model membrane fusion determined from Monte Carlo simulation. Biophys. J. 85, 1611-1623.
102. Muller, M., Katsov, K., and Schick, M. (2006). Biological and synthetic membranes: what can be learned from a coarsegrained description? Phys. Rep. 434, 113-176.
103. 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.
104. Nikolaus, J., Stockl, M., Langosch, D., Volkmer, R., and Herrmann, A. (2010). Direct visualization of large and protein-free hemifusion diaphragms. Biophys. J. 98, 1192-1199.
105. Nikolaus, J., Warner, J.M., O'shaughnessy, B., and Herrmann, A. (2011). The pathway to membrane fusion through hemifusion. Curr. Top. Membr. 68, 1-32.
106. Noguchi, H. and Takasu, M. (2001). Self-assembly of amphiphiles into vesicles: a Brownian dynamics simulation. Phys. Rev. E. 64, 041913.
107. Nussler, F., Clague, M.J., and Herrmann, A. (1997). Meta-stability of the hemifusion intermediate induced by glycosylphosphatidylinositol-anchored influenza hemagglutinin. Biophys. J. 73, 2280-2291.
108. Ohki, S. (1982). A mechanism of divalent ion-induced phosphatidylserine membrane fusion. Biochim. Biophys. Acta 689, 1-11.
109. Ollesch, J., Poschner, B.C., Nikolaus, J., Hofmann, M.W., Herrmann, A., Gerwert, K., and Langosch, D. (2008). Secondary structure and distribution of fusogenic LV-peptides in lipid membranes. Eur. Biophys. J. 37, 435-445.
110. Oren-Suissa, M. and Podbilewicz, B. (2007). Cell fusion during development. Trends Cell Biol 17, 537-546.
111. Podbilewicz, B., Leikina, E., Sapir, A., Valansi, C., Suissa, M., Shemer, G., and Chernomordik, L.V. (2006). The C. elegans developmental fusogen EFF-1 mediates homotypic fusion in heterologous cells and in vivo . Dev Cell 11, 471-481.
112. Qian, S. and Huang, H.W. (2012). A novel phase of compressed bilayers that models the prestalk transition state of membrane fusion. Biophys. J. 102, 48-55.
113. Rand, R.P. and Parsegian, V.A. (1989). Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta 988, 351-376.
114. Razinkov, V.I., Melikyan, G.B., Epand, R.M., Epand, R.F., and Cohen, F.S. (1998). Effects of spontaneous bilayer curvature on influenza virus-mediated fusion pores. J. Gen. Physiol. 112, 409-422.
115. Reese, C., Heise, F., and Mayer, A. (2005). Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 436, 410-414.
116. Reuven, E.M., Dadon, Y., Viard, M., Manukovsky, N., Blumenthal, R., and Shai, Y. (2012). HIV-1 gp41 transmembrane domain interacts with the fusion peptide: implication in lipid mixing and inhibition of virus-cell fusion. Biochemistry 51, 2867-2878.
117. Risselada, H.J. and Grubmuller, H. (2012). How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr. Opin. Struct. Biol. 22, 187-196.
118. Risselada, H.J., Kutzner, C., and Grubmuller, H. (2011). Caught in the act: visualization of SNARE-mediated fusion events in molecular detail. ChemBioChem 12, 1049-1055.
119. Rizo, J. (2006). Illuminating membrane fusion. Proc. Natl. Acad. Sci. USA 103, 19611-19612.
120. Rogasevskaia, T. and Coorssen, J.R. (2006). Sphingomyelinenriched microdomains define the efficiency of native Ca 2 + -triggered membrane fusion. J. Cell Sci. 119, 2688-2694.
121. Roy, R., Laage, R., and Langosch, D. (2004). Synaptobrevin transmembrane domain dimerization-revisited. Biochemistry 43, 4964-4970.
122. Salzwedel, K., Johnston, P.B., Roberts, S.J., Dubay, J.W., and Hunter, E. (1993). Expression and characterization of glycophospholipid-anchored human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 67, 5279-5288.
123. Sapir, A., Avinoam, O., Podbilewicz, B., and Chernomordik, L.V. (2008). Viral and developmental cell fusion mechanisms: conservation and divergence. Dev. Cell 14, 11-21.
124. Schroth-Diez, B., Ponimaskin, E., Reverey, H., Schmidt, M.F. and Herrmann, A. (1998). Fusion activity of transmembrane and cytoplasmic domain chimeras of the influenza virus glycoprotein hemagglutinin. J. Virol. 72, 133-141.
125. Schuette, C.G., Hatsuzawa, K., Margittai, M., Stein, A., Riedel, D., Kuster, P., Konig, M., Seidel, C., and Jahn, R. (2004). Determinants of liposome fusion mediated by synaptic SNARE proteins. Proc. Natl. Acad. Sci. USA 101, 2858-2863.
126. Scolari, S., Engel, S., Krebs, N., Plazzo, A.P., De Almeida, R.F., Prieto, M., Veit, M., and Herrmann, A. (2009). Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging. J. Biol. Chem. 284, 15708-15716.
127. Shillcock, J.C. and Lipowsky, R. (2005). Tension-induced fusion of bilayer membranes and vesicles. Nat. Mater. 4, 225-228.
128. Shillcock, J.C. and Lipowsky, R. (2006). The computational route from bilayer membranes to vesicle fusion. J. Phys. Condens. Matter 18, S1191-1219.
129. Siddiqui, T.J., Vites, O., Stein, A., Heintzmann, R., Jahn, R., and Fasshauer, D. (2007). Determinants of synaptobrevin regulation in membranes. Mol. Biol. Cell 18, 2037-2046.
130. Skehel, J.J. and Wiley, D.C. (2000). Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69, 531-569.
131. Smeijers, A.F., Markvoort, A.J., Pieterse, K., and Hilbers, P.A. (2006). A detailed look at vesicle fusion. J. Phys. Chem. B 110, 13212-13219.
132. Smirnova, Y.G., Marrink, S.J., Lipowsky, R., and Knecht, V. (2010). Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. J. Am. Chem. Soc. 132, 6710-6718.
133. Smith, E.A. and Weisshaar, J.C. (2011). Docking, not fusion, as the rate-limiting step in a SNARE-driven vesicle fusion assay. Biophys. J. 100, 2141-2150.
134. Smith, E.C., Culler, M.R., Hellman, L.M., Fried, M.G., Creamer, T.P., and Dutch, R.E. (2012). Beyond anchoring: the expanding role of the hendra virus fusion protein transmembrane domain in protein folding, stability, and function. J. Virol. 86, 3003-3013.
135. Sollner, T.H. (2004). Intracellular and viral membrane fusion: a uniting mechanism. Curr. Opin. Cell Biol. 16, 429-435.
136. St Vincent, M.R., Colpitts, C.C., Ustinov, A.V., Muqadas, M., Joyce, M.A., Barsby, N.L., Epand, R.F., Epand, R.M., Khramyshev, S.A., Valueva, O.A., et al. (2010). Rigid amphipathic fusion inhibitors, small molecule antiviral compounds against enveloped viruses. Proc. Natl. Acad. Sci. USA 107, 17339-17344.
137. 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.
138. Stevens, M.J., Hoh, J.H., and Woolf, T.B. (2003). Insights into the molecular mechanism of membrane fusion from simulation: evidence for the association of splayed tails. Phys. Rev. Lett. 91, 188102.
139. Sudhof, T.C. and Rothman, J.E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
140. Tanford, C. (1980) The Hydrophobic Effect. Formation of micelles and biological membranes. (New York, NY: John Wiley and Sons).
141. Tatulian, S.A. and Tamm, L.K. (2000). Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin. Biochemistry 39, 496-507.
142. Thomas, A. and Brasseur, R. (2006). Tilted peptides: the history. Curr. Protein Pept. Sci. 7, 523-527.
143. Tong, S. and Compans, R.W. (2000). Oligomerization, secretion, and biological function of an anchor-free parainfluenza virus type 2 (PI2) fusion protein. Virology 270, 368-376.
144. 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. USA 106, 5141-5146.
145. Wang, Y., Dulubova, I., Rizo, J., and Sudhof, T.C. (2001). Functional analysis of conserved structural elements in yeast syntaxin Vam3p. J. Biol. Chem. 276, 28598-28605.
146. Wang, L., Seeley, E.S., Wickner, W., and Merz, A.J. (2002). Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle. Cell 108, 357-369.
147. Warner, J.M. and O'shaughnessy, B. (2012a). Evolution of the hemifused intermediate on the pathway to membrane fusion. Biophys. J. 103, 1-13.
148. Warner, J.M. and O'shaughnessy, B. (2012b). The hemifused state on the pathway to membrane fusion. Phys. Rev. Lett. 108, 178101.
149. Weise, K. and Reed, J. (2008). Fusion peptides and transmembrane domains of fusion proteins are characterized by different but specific structural properties. ChemBioChem 9, 934-943.
150. Weiss, C.D. and White, J.M. (1993). Characterization of stable Chinese hamster ovary cells expressing wild-type, secreted, and glycosylphosphatidylinositol-anchored human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 67, 7060-7066.
151. Weissenhorn, W., Hinz, A., and Gaudin, Y. (2007). Virus membrane fusion. FEBS Lett 581, 2150-2155.
152. 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.
153. 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.
154. Yang, L. and Huang, H.W. (2002). Observation of a membrane fusion intermediate structure. Science 297, 1877-1879.
155. Yoon, T.Y., Okumus, B., Zhang, F., Shin, Y.K., and Ha, T. (2006). Multiple intermediates in SNARE-induced membrane fusion. Proc. Natl. Acad. Sci. USA 103, 19731-19736.