Membrane fusion: A structural perspective on the interplay of lipids and proteins

Current Opinion in Structural Biology

Volumn 13, Issue 4, 2003, Pages 453-466

  Tamm, Lukas K ^a   Crane, Jonathan ^a   Kiessling, Volker ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; LIPID; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; INTRACELLULAR MEMBRANE; LIPID MEMBRANE; MEMBRANE FUSION; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; REVIEW; X RAY CRYSTALLOGRAPHY;

EID: 0041428123     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00107-6     Document Type: Review

References (125)

1. Skehel J.J., Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev. Biochem. 69:2000;531-569.
2. Eckert D.M., Kim P.S. Mechanisms of viral membrane fusion and its inhibition. Annu Rev. Biochem. 70:2001;777-810 An excellent review of the structural biology of helical bundle (class I) viral fusion proteins.
3. Brunger A.T. Structural insights into the molecular mechanism of calcium-dependent vesicle-membrane fusion. Curr. Opin. Struct. Biol. 11:2001;163-173 An excellent review of the structural biology of proteins involved in intracellular fusion.
4. Bullough P.A., Hughson F.M., Skehel J.J., Wiley D.C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 371:1994;37-43.
5. Helm C.A., Israelachvili J.N., McGuiggan P.M. Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers. Science. 246:1989;919-922.
6. Helm C.A., Israelachvili J.N., McGuiggan P.M. Role of hydrophobic forces in bilayer adhesion and fusion. Biochemistry. 31:1992;1794-1805.
7. Chernomordik L.V., Melikyan G.B., Chizmadzhev Y.A. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906:1987;309-352.
8. Gingell D, Ginsberg I: Problems in the physical interpretation of membrane interaction and fusion. In Membrane Fusion. Edited by Poste G, Nicolson GL: Elsevier; 1978:791-833.
9. Hui S.E., Stewart T.P., Boni L.T., Yeagle P.L. Membrane fusion through point defects in bilayers. Science. 212:1981;921-923.
10. Markin V.S., Kozlov M.M., Borovjagin V.L. On the theory of membrane fusion: the stalk mechanism. Gen. Physiol. Biophys. 3:1984;361-377.
11. Siegel D.P. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophys. J. 65:1993;2124-2140.
12. Siegel D.P. The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusion. Biophys. J. 76:1999;291-313.
13. Markin V.S., Albanesi J.P. Membrane fusion: stalk model revisited. Biophys. J. 82:2002;693-712 Calculation of the optimized shape of a stress-free' stalk. The energy of the transition from hemifusion to complete fusion is calculated to be of the order of 40-50 kT in this model.
14. Kuzmin P.I., Zimmerberg J., Chizmadzhev Y.A., Cohen F.S. A quantitative model for membrane fusion based on low-energy intermediates. Proc. Natl. Acad. Sci. U.S.A. 98:2001;7235-7240 Calculation of the energy of a modified stalk with tilted lipids in the contacting monolayers of the stalk. This geometry reduces the volume of 'hydrophobic voids' and thus the energy of the stalk intermediate. The hemifusion to prepore transition energy is of the order of 40 kT in this model.
15. •] and is even negative for some lipids.
16. Kozlovsky Y., Chernomordik L.V., Kozlov M.M. Lipid intermediates in membrane fusion: formation, structure, and decay of the hemifusion diaphragm. Biophys. J. 83:2002;2634-2651.
17. •] (see Figure 1).
18. ••], rhombohedral phases resembling lipid stalks are observed in mixtures of DOPC and DOPE at relative humidities of about 50-75%.
19. Lee J., Lentz B.R. Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusion. Biochemistry. 36:1997;6251-6259.
20. Evans K.O., Lentz B.R. Kinetics of lipid rearrangements during poly(ethylene glycol)-mediated fusion of highly curved unilamellar vesicles. Biochemistry. 41:2002;1241-1249.
21. Haque M.E., McIntosh T.J., Lentz B.R. Influence of lipid composition on physical properties and PEG-mediated fusion of curved and uncurved model membrane vesicles: 'nature's own' fusogenic lipid bilayer. Biochemistry. 40:2001;4340-4348 A systematic study of the fusogenic properties of pure lipid bilayers composed of a large variety of different lipids. Lipid compositions close to those found in secretory vesicles are found to best support nonleaky fusion.
22. Malinin V., Frederik P., Lentz B.R. Osmotic and curvature stress affect PEG-induced fusion of lipid vesicles but not mixing of their lipids. Biophys. J. 82:2002;2090-2100.
23. Malinin V., Lentz B.R. Pyrene cholesterol reports the transient appearance of nonlamellar intermediate structures during fusion of model membranes. Biochemistry. 41:2002;5913-5919.
24. Chernomordik L., Kozlov M.M., Zimmerberg J. Lipids in biological membrane fusion. J. Membr. Biol. 146:1995;1-14.
25. Kemble G.W., Danieli T., White J.M. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell. 76:1994;383-391.
26. Melikyan G.B., Brener S.A., Ok D.C., Cohen F.S. Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion. J. Cell Biol. 136:1997;995-1005.
27. Chernomordik L.V., Frolov V.A., Leikina E., Bronk P., Zimmerberg J. The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion and lipidic fusion pore formation. J. Cell Biol. 140:1998;1369-1382.
28. Leikina E., Chernomordik L.V. Reversible merger of membranes at the early stage of influenza hemagglutinin-mediated fusion. Mol. Biol. Cell. 11:2000;2359-2371.
29. Markosyan R.M., Melikyan G.B., Cohen F.S. Evolution of intermediates of influenza virus hemagglutinin-mediated fusion revealed by kinetic measurements of pore formation. Biophys. J. 80:2001;812-821.
30. Wilson I.A., Skehel J.J., Wiley D.C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature. 289:1981;366-373.
31. Chen J., Lee K.H., Steinhauer D.A., Stevens D.J., Skehel J.J., Wiley D.C. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell. 95:1998;409-417.
32. 2 subunit to form an N cap that terminates the triple-stranded coiled coil. Proc. Natl. Acad. Sci. U.S.A. 96:1999;8967-8972.
33. Bizebard T., Gigant B., Rigolet P., Rasmussen B., Diat O., Bosecke P., Wharton S.A., Skehel J.J., Knossow M. Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature. 376:1995;92-94.
34. Gray C., Tamm L.K. pH-induced conformational changes of membrane-bound influenza hemagglutinin and its effect on target lipid bilayers. Protein Sci. 7:1998;2359-2373.
35. Tatulian S.A., Tamm L.K. Reversible pH-dependent conformational change of reconstituted influenza hemagglutinin. J. Mol. Biol. 260:1996;312-316.
36. Leikina E., Ramos C., Markovic I., Zimmerberg J., Chernomordik L.V. Reversible stages of the low-pH-triggered conformational change in influenza virus hemagglutinin. EMBO J. 21:2002;5701-5710.
37. Carr C.M., Kim P.S. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell. 73:1993;823-832.
38. 2) folds in Escherichia coli into the low-pH-induced conformation. Proc. Natl. Acad. Sci. U.S.A. 92:1995;12205-12209.
39. Carr C.M., Chaudhry C., Kim P.S. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl. Acad. Sci. U.S.A. 94:1997;14306-14313.
40. Weissenhorn W., Dessen A., Harrison S.C., Skehel J.J., Wiley D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature. 387:1997;426-430.
41. Chan D.C., Fass D., Berger J.M., Kim P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell. 89:1997;263-273.
42. Tan K., Liu J., Wang J., Shen S., Lu M. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. U.S.A. 94:1997;12303-12308.
43. Caffrey M., Cai M., Kaufman J., Stahl S.J., Wingfield P.T., Covell D.G., Gronenborn A.M., Clore G.M. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17:1998;4572-4584.
44. Malashkevich V.N., Chan D.C., Chutkowski C.T., Kim P.S. Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: conserved helical interactions underlie the broad inhibitory activity of gp41 peptides. Proc. Natl. Acad. Sci. U.S.A. 95:1998;9134-9139.
45. Fass D., Harrison S.C., Kim P.S. Retrovirus envelope domain at 1.7 Ångstrom resolution. Nat. Struct. Biol. 3:1996;465-469.
46. Kobe B., Center R.J., Kemp B.E., Poumbourios P. Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retroviral transmembrane proteins. Proc. Natl. Acad. Sci. U.S.A. 96:1999;4319-4324.
47. Baker K.A., Dutch R.E., Lamb R.A., Jardetzky T.S. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell. 3:1999;309-319.
48. Zhao X., Singh M., Malashkevich V.N., Kim P.S. Structural characterization of the human respiratory syncytial virus fusion protein core. Proc. Natl. Acad. Sci. U.S.A. 97:2000;14172-14177.
49. Weissenhorn W., Carfi A., Lee K.H., Skehel J.J., Wiley D.C. Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol. Cell. 2:1998;605-616.
50. Malashkevich V.N., Schneider B.J., McNally M.L., Milhollen M.A., Pang J.X., Kim P.S. Core structure of the envelope glycoprotein GP2 from Ebola virus at 1.9 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 96:1999;2662-2667.
51. Markosyan R.M., Cohen F.S., Melikyan G.B. HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol. Biol. Cell. 14:2003;926-938.
52. Rey F.A., Heinz F.X., Mandl C., Kunz C., Harrison S.C. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature. 375:1995;291-298.
53. Lescar J., Roussel A., Wien M.W., Navaza J., Fuller S.D., Wengler G., Rey F.A. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell. 105: 2001;137-148 The structure of fusion protein E1 from Semliki Forest virus determined by X-ray crystallography was placed into the virus structure determined by cryo-EM. The structure of this alphavirus fusion protein is similar to that of the flavivirus fusion protein described in [52]. Both proteins, classified as class II fusion proteins, consist of three β-sheet domains, in marked contrast to the helical bundle (class I) fusion proteins.
54. ••], the fusion peptide of this class II fusion protein forms a loop at one end of the fusion protein, which lies flat on the viral membrane surface. A lattice rearrangement occurs at low (fusion) pH and exposes the fusion peptides of several E proteins to the target membrane, where they are proposed to insert in the form of a β barrel.
55. Jahn R., Lang T., Sudhof T.C. Membrane fusion. Cell. 112:2003;519-533 An excellent review of current thoughts on proteins involved in viral and intracellular membrane fusion.
56. Rothman J.E. The machinery and principles of vesicle transport in the cell. Nat. Med. 8:2002;1059-1062 A concise personal commentary on the history of discoveries on intracellular vesicle transport and fusion.
57. Wickner W., Haas A. Yeast homotypic vacuole fusion: a window on organelle trafficking mechanisms. Annu. Rev. Biochem. 69:2000;247-275.
58. Weber T., Zemelman B.V., McNew J.A., Westermann B., Gmachl M., Parlati F., Sollner T.H., Rothman J.E. SNAREpins: minimal machinery for membrane fusion. Cell. 92:1998;759-772.
59. Sutton R.B., Fasshauer D., Jahn R., Brunger A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature. 395:1998;347-353.
60. •].
61. Ernst J.A., Brunger A.T. High resolution structure, stability, and synaptotagmin binding of a truncated neuronal SNARE complex. J. Biol. Chem. 278:2003;8630-8636 Higher resolution (1.4 Å) structure of the neuronal SNARE complex described in [59]. Although truncated by several residues at both ends, the complex still retains binding to synaptotagmin I.
62. Fernandez I., Ubach J., Dulubova I., Zhang X., Sudhof T.C., Rizo J. Three-dimensional structure of an evolutionarily conserved N-terminal domain of syntaxin 1A. Cell. 94:1998;841-849.
63. Xiao W., Poirier M.A., Bennett M.K., Shin Y.K. The neuronal t-SNARE complex is a parallel four-helix bundle. Nat. Struct. Biol. 8:2001;308-311 Site-directed spin label EPR spectroscopy was used to demonstrate that t-SNAREs can form a four-helix bundle consisting of two syntaxin 1A, and the N- and C-terminal SNARE motifs of SNAP-25. This structure is similar to that of the final SNARE complex, but is more flexible near the central Q-layer region.
64. Fasshauer D., Sutton R.B., Brunger A.T., Jahn R. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. U.S.A. 95:1998;15781-15786.
65. Bock J.B., Matern H.T., Peden A.A., Scheller R.H. A genomic perspective on membrane compartment organization. Nature. 409:2001;839-841.
66. Munson M., Chen X., Cocina A.E., Schultz S.M., Hughson F.M. Interactions within the yeast t-SNARE Sso1p that control SNARE complex assembly. Nat. Struct. Biol. 7:2000;894-902.
67. Dulubova I., Sugita S., Hill S., Hosaka M., Fernandez I., Sudhof T.C., Rizo J. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18:1999;4372-4382.
68. Parlati F., Weber T., McNew J.A., Westermann B., Sollner T.H., Rothman J.E. 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. U.S.A. 96:1999;12565-12570.
69. Melia T.J., Weber T., McNew J.A., Fisher L.E., Johnston R.J., Parlati F., Mahal L.K., Sollner T.H., Rothman J.E. Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158:2002;929-940 A synaptobrevin-derived peptide that binds to the C-terminal part of the groove in the t-SNARE complex enhances the rate of SNARE-mediated fusion, providing evidence for SNARE complex zippering in the N→C direction and a C-terminal assembly switch in the t-SNARE complex.
70. Misura K.M.S., Scheller R.H., Weis W.I. Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature. 404:2000;355-362.
71. Bracher A., Weissenhorn W. Structural basis for the Golgi membrane recruitment of Sly1p by Sed5p. EMBO J. 21:2002;6114-6124 The authors present the crystal structure of a Golgi SM protein-SNARE complex. Although the general arch architecture of the SM protein is similar to that of the distantly related neuronal SM protein Munc-18, the t-SNARE associates via its N terminus on the outside of the N-terminal base of the arch (i.e. on the opposite side of the neuronal t-SNARE-binding site described in [70]). Comparison of the two complex structures shows that SM proteins exhibit different modes of interaction in different cellular compartments and/or at different stages of SNARE assembly.
72. ••].
73. Carr C.M., Grote E., Munson M., Hughson F.M., Novick P.J. Sec1p binds to SNARE complexes and concentrates at sites of secretion. J. Cell Biol. 146:1999;333-344.
74. Novick P., Guo W. Ras family therapy: Rab, Rho and Ral talk to the exocyst. Trends Cell Biol. 12:2002;247-249.
75. 2+-evoked neurotransmitter release, is shown in this structure to bind antiparallel to the groove between the synaptobrevin and syntaxin helices of the SNARE complex, and thereby stabilize these helices.
76. 2+-independent SNARE complex interaction. J. Cell Biol. 147:1999;589-598.
77. 2+/phospholipid-binding fold. Cell. 80:1995;929-938.
78. 2+ induce a conformational change? Biochemistry. 37:1998;16106-16115.
79. Ubach J., Garcia J., Nittler M.P., Sudhof T.C., Rizo J. Structure of the janus-faced C2B domain of rabphilin. Nat. Cell Biol. 1:1999;106-112.
80. 2+-binding loops penetrate about 5 Å deep into the membrane.
81. Wu Y., He Y., Bai J., Ji S.R., Tucker W.C., Chapman E.R., Sui S.F. Visualization of synaptotagmin I oligomers assembled onto lipid monolayers. Proc. Natl. Acad. Sci. U.S.A. 100:2003;2082-2087 Synaptotagmin I C2A-C2B domains bound to lipid monolayers are shown by EM to form ring-like heptameric structures. Self-assembly into these rings is mediated by the C2B domains.
82. 2+ in a reconstituted system. This stimulatory effect is topologically restricted to v-SNARE vesicles and only occurs in trans to t-SNARE vesicles.
83. 2B domain triggers fast exocytosis without stimulating SNARE interactions. Neuron. 37:2003;99-108.
84. Wagner M.L., Tamm L.K. Reconstituted syntaxin1A/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers. Biophys. J. 81:2001;266-275.
85. Durell S.R., Martin I., Ruysschaert J.M., Shai Y., Blumenthal R. What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion. Mol. Membr. Biol. 14:1997;97-112.
86. Tamm L.K., Han X. Viral fusion peptides: a tool set to disrupt and connect biological membranes. Biosci. Rep. 20:2000;501-518.
87. Han X., Tamm L.K. pH-dependent self-association of influenza hemagglutinin fusion peptides in lipid bilayers. J. Mol. Biol. 304:2000;953-965.
88. Han X., Tamm L.K. A host-guest to study structure-function relationships of membrane fusion peptides. Proc. Natl. Acad. Sci. U.S.A. 97:2000;13097-13102.
89. Saez-Cirion A., Nieva J.L. Conformational transitions of membrane-bound HIV-1 fusion peptide. Biochim. Biophys. Acta. 1564:2002;57-65.
90. Yang J., Gabrys C.M., Weliky D.P. Solid-state nuclear magnetic resonance evidence for an extended beta strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistry. 40:2001;8126-8137.
91. Li Y., Han X., Tamm L.K. Thermodynamics of fusion peptide-membrane interactions. Biochemistry. 42:2003;7245-7251.
92. Han X., Bushweller J.H., Cafiso D.S., Tamm L.K. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8:2001;715-720 The NMR structures of the influenza HA fusion peptide at pH 7 and pH 5 were docked to lipid bilayers using distance constraints from site-directed spin labeling. The fusogenic pH 5 structure is characterized by a V-shaped 'boomerang' with two highly amphipathic helical arms. The N-terminal arm penetrates at an oblique angle about 20 Å deep (i.e. to about the middle of the lipid bilayer).
93. Dubovskii P.V., Li H., Takahashi S., Arseniev A.S., Akasaka K. Structure of an analog of fusion peptide from hemagglutinin. Protein Sci. 9:2000;786-798.
94. Tamm L.K., Han X., Li Y., Lai A.L. Structure and function of membrane fusion peptides. Biopolymers. 66:2002;249-260 A recent review of the structures and lipid interactions of viral fusion peptides.
95. Qiao H., Armstrong R.T., Melikyan G.B., Cohen F.S., White J.M. A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol. Biol. Cell. 10:1999;2759-2769.
96. Tamm L.K. Hypothesis: spring-loaded boomerang mechanism of influenza hemagglutinin-mediated membrane fusion. Biochim. Biophys. Acta. 1614:2003;14-23 Recent advances in our understanding of the structures and thermodynamics of viral class I fusion proteins are combined to propose a 'spring-loaded boomerang mechanism' of viral membrane fusion.
97. Tatulian S.A., Tamm L.K. Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin. Biochemistry. 39:2000;496-507.
98. Dennison S.M., Greenfield N., Lenard J., Lentz B.R. VSV transmembrane domain (TMD) peptide promotes PEG-mediated fusion of liposomes in a conformationally sensitive fashion. Biochemistry. 41:2002;14925-14934.
99. Melikyan G.B., Lin S., Roth M.G., Cohen F.S. Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell. 10:1999;1821-1836.
100. Armstrong R.T., Kushnir A.S., White J.M. The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J. Cell Biol. 151:2000;425-437.
101. Melikyan G.B., Markosyan R.M., Roth M.G., Cohen F.S. A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol. Biol. Cell. 11:2000;3765-3775.
102. Cleverley D.Z., Lenard J. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. U.S.A. 95:1998;3425-3430.
103. Senes A., Gerstein M., Engelman D.M. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J. Mol. Biol. 296:2000;921-936.
104. Margittai M., Otto H., Jahn R. A stable interaction between syntaxin 1a and synaptobrevin 2 mediated by their transmembrane domains. FEBS Lett. 446:1999;40-44.
105. Laage R., Rohde J., Brosig B., Langosch D. A conserved membrane-spanning amino acid motif drives homomeric and supports heteromeric assembly of presynaptic SNARE proteins. J. Biol. Chem. 275:2000;17481-17487.
106. Fleming K.G., Engelman D.M. Computation and mutagenesis suggest a right-handed structure for the synaptobrevin transmembrane dimer. Proteins. 45:2001;313-317.
107. Bowen M.E., Engelman D.M., Brunger A.T. Mutational analysis of synaptobrevin transmembrane domain oligomerization. Biochemistry. 41:2002;15861-15866.
108. Kweon D.H., Kim C.S., Shin Y.K. The membrane-dipped neuronal SNARE complex: a site-directed spin labeling electron paramagnetic resonance study. Biochemistry. 41:2002;9264-9268.
109. Langosch D., Crane J.M., Brosig B., Hellwig A., Tamm L.K., Reed J. Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. J. Mol. Biol. 311:2001;709-721.
110. Zhao J., Tamm L.K. FTIR and fluorescence studies of interactions of synaptic fusion proteins in polymer-supported bilayers. Langmuir. 19:2003;1838-1846.
111. Cohen FS, Markosyan RM, Melikyan GB: The process of membrane fusion: nipples, hemifusion, pores, and pore growth. In Peptid-Lipid Interactions, Current Topics in Membranes, vol 52. Edited by Simon SA, McIntosh TJ: Academic Press; 2002:501-529.
112. Chernomordik L.V., Kozlov M.M. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72:2003;175-207 A review describing intermediates and curvature effects in biological and pure lipid bilayer membrane fusion and fission.
113. Epand R.M., Epand R.F. Relationship between the infectivity of influenza virus and the ability of its fusion peptide to perturb bilayers. Biochem. Biophys. Res. Commun. 202:1994;1420-1425.
114. Colotto A., Epand R.M. Structural study of the relationship between the rate of membrane fusion and the ability of the fusion peptide of influenza virus to perturb bilayers. Biochemistry. 36:1997;7644-7651.
115. Gray C., Tatulian S.A., Wharton S.A., Tamm L.K. Effect of the N-terminal glycine on the secondary structure, orientation, and interaction of the influenza hemagglutinin fusion peptide with lipid bilayers. Biophys. J. 70:1996;2275-2286.
116. Haque M.E., McCoy A.J., Glenn J., Lee J., Lentz B.R. Effects of hemagglutinin fusion peptide on poly(ethylene glycol)-mediated fusion of phosphatidylcholine vesicles. Biochemistry. 40:2001;14243-14251.
117. Haque M.E., Lentz B.R. Influence of gp41 fusion peptide on the kinetics of poly(ethylene glycol)-mediated model membrane fusion. Biochemistry. 41:2002;10866-10876.
118. Nagle J.F., Tristram-Nagle S. Structure of lipid bilayers. Biochim. Biophys. Acta. 1469:2000;159-195.
119. Noguchi H., Takasu M. Fusion pathways of vesicles: a Brownian dynamics simulation. J. Chem. Phys. 115:2001;9547-9551.
120. Marrink S.J., Tieleman D.P. Molecule dynamics simulation of spontaneous membrane fusion during a cubic-hexagonal phase transition. Biophys. J. 83:2002;2386-2392.
121. Müller M, Katsov K, Schick M: A new mechanism of model membrane fusion determined from Monte Carlo simulation. Biophys J 2003, 85:in press.
122. Lee S., Kuhn R.J., Rossmann M.G. Probing the potential glycoprotein binding site of Sindbis virus capsid protein with dioxane and model building. Proteins. 33:1998;311-317.
123. Zhang W., Mukhopadhyay S., Pletnev S.V., Baker T.S., Kuhn R.H., Rossmann M.G. Placement of the structural proteins in Sindbis virus. J. Virol. 76:2002;11645-11658.
124. Kweon D.-H., Kim C.S., Shin Y.-K. Regulation of neuronal SNARE assembly by the membrane. Nat. Struct. Biol. 10:2003;440-447 A spin-label EPR study of a membrane-reconstituted v-SNARE, demonstrating the insertion of the juxtamembrane domain of this protein into the membrane interface and a concomitant inability of the v-SNARE to form a SNARE complex with the cognate t-SNARE.
125. Hu C.H., Ahmed M., Melia T.J., Söllner T.H., Mayer T., Rothman J.E. Fusion of cells by flipped SNAREs. Science. 300:2003;1745-1749 A new cell-cell fusion assay demonstrating efficient fusion between cell pairs expressing t- and v-SNAREs on their respective surfaces. As no other cytosolic proteins are present, this experiment demonstrates that cognate SNAREs alone can fuse biological membranes.