Physical aspects of viral membrane fusion

TheScientificWorldJournal

Volumn 9, Issue , 2009, Pages 764-780

  Wessels, Laura ^a   Weninger, Keith ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Class I, II, and III fusion proteins; E1; gp64; Hemagluttin (HA); Viral membrane fusion

Indexed keywords

ENFUVIRTIDE; HYDROQUINONE; MEMBRANE FUSION PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PRO 140; SNARE PROTEIN; VIRUS FUSION PROTEIN; VIRUS PROTEIN;

AVIAN SARCOMA VIRUS; EBOLA VIRUS; ENDOCYTOSIS; GENOME; HEPATITIS C VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MEMBRANE FUSION; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN STRUCTURE; REVIEW; SEMLIKI FOREST ALPHAVIRUS; SENDAI VIRUS; X RAY CRYSTALLOGRAPHY; CHEMISTRY; PROTEIN CONFORMATION; VIRAL PHENOMENA AND FUNCTIONS;

MEMBRANE FUSION; PROTEIN CONFORMATION; VIRAL PROTEINS; VIRUS PHYSIOLOGICAL PHENOMENA;

EID: 70350746423     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/tsw.2009.76     Document Type: Review

References (144)

1. Brunger, A.T. (2005) Structure and function of SNARE and SNARE-interacting proteins. Q. Rev. Biophys. 38, 1-47.
2. Chen, E.H. and Olson, E.N. (2005) Unveiling the mechanisms of cell-cell fusion. Science 308, 369-373.
3. Chan, D.C. (2006) Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 22, 79-99.
4. Primakoff, P. and Myles, D.G. (2007) Cell-cell membrane fusion during mammalian fertilization. FEBS Lett. 581, 2174-2180.
5. Damm, E.M. and Pelkmans, L. (2006) Systems biology of virus entry in mammalian cells. Cell. Microbiol. 8, 1219-1227.
6. Sollner, T.H. (2004) Intracellular and viral membrane fusion: a uniting mechanism. Curr. Opin. Cell Biol. 16, 429-435.
7. Harrison, S.C. (2008) Viral membrane fusion. Nat. Struct. Mol. Biol. 15, 690-698.
8. Basanez, G. (2002) Membrane fusion: the process and its energy suppliers. Cell. Mol. Life Sci. 59, 1478-1490.
9. Chernomordik, L.V. and Kozlov, M.M. (2005) Membrane hemifusion: crossing a chasm in two leaps. Cell 123, 375-382.
10. Porcar, L., Hamilton, W.A., Butler, P.D., and Warr, G.G. (2004) Topological relaxation of a shear-induced lamellar phase to sponge equilibrium and the energetics of membrane fusion. Phys. Rev. Lett. 93, 198301.
11. Chernomordik, L.V. and Kozlov, M.M. (2008) Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15, 675-683.
12. Martens, S. and McMahon, H.T. (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9, 543-556.
13. White, J.M., Delos, S.E., Brecher, M., and Schornberg, K. (2008) Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43, 189-219.
14. 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.
15. Freed, E.O., Myers, D.J., and Risser, R. (1990) Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc. Natl. Acad. Sci. U. S. A. 87, 4650-4654.
16. Yang, Z.N., Mueser, T.C., Kaufman, J., Stahl, S.J., Wingfield, P.T., and Hyde, C.C. (1999) The crystal structure of the SIV gp41 ectodomain at 1.47 A resolution. J. Struct. Biol. 126, 131-144.
17. Center, R.J., Kobe, B., Wilson, K.A., Teh, T., Howlett, G.J., Kemp, B.E., and Poumbourios, P. (1998) Crystallization of a trimeric human T cell leukemia virus type 1 gp21 ectodomain fragment as a chimera with maltose-binding protein. Protein Sci. 7, 1612-1619.
18. Weissenhorn, W., Carfi, A., Lee, K.H., Skehel, J.J., and Wiley, D.C. (1998) Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol. Cell 2, 605-616.
19. Kashiwada, A., Matsuda, K., Mizuno, T., and Tanaka, T. (2008) Construction of a pH-responsive artificial membrane fusion system by using designed coiled-coil polypeptides. Chemistry 14, 7343-7350.
20. Harris, A., Cardone, G., Winkler, D.C., Heymann, J.B., Brecher, M., White, J.M., and Steven, A.C. (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. U. S. A. 103, 19123-19127.
21. Stegmann, T., Nir, S., and Wilschut, J. (1989) Membrane-fusion activity of influenza-virus. Effects of gangliosides and negatively charged phospholipids in target liposomes. Biochemistry 28, 1698-1704.
22. Tsao, Y.S. and Huang, L. (1985) Sendai virus induced leakage of liposomes containing gangliosides. Biochemistry 24, 1092-1098.
23. Hinterdorfer, P., Baber, G., and Tamm, L.K. (1994) Reconstitution of membrane fusion sites. A total internal reflection fluorescence microscopy study of influenza hemagglutinin-mediated membrane fusion. J. Biol. Chem. 269, 20360-20368.
24. Matlin, K.S., Reggio, H., Helenius, A., and Simons, K. (1981) Infectious entry pathway of influenza virus in a canine kidney cell line. J. Cell Biol. 91, 601-613.
25. Bullough, P.A., Hughson, F.M., Skehel, J.J., and Wiley, D.C. (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371, 37-43.
26. Kielian, M. and Rey, F.A. (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4, 67-76.
27. Floyd, D.L., Ragains, J.R., Skehel, J.J., Harrison, S.C., and van Oijen, A.M. (2008) Single-particle kinetics of influenza virus membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 105, 15382-15387.
28. Blumenthal, R., Sarkar, D.P., Durell, S., Howard, D.E., and Morris, S.J. (1996) Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J. Cell Biol. 135, 63-71.
29. Gunther-Ausborn, S., Schoen, P., Bartoldus, I., Wilschut, J., and Stegmann, T. (2000) Role of hemagglutinin surface density in the initial stages of influenza virus fusion: lack of evidence for cooperativity. J. Virol. 74, 2714-2720.
30. Earp, L.J., Hernandez, L.D., Delos, S.E., and White, J.M. (2003) Receptor-activated binding of viral fusion proteins to target membranes. Methods Enzymol. 372, 428-440.
31. Rawat, S.S., Viard, M., Gallo, S.A., Rein, A., Blumenthal, R., and Puri, A. (2003) Modulation of entry of enveloped viruses by cholesterol and sphingolipids (Review). Mol. Membr. Biol. 20, 243-254.
32. Reeves, J.D., Gallo, S.A., Ahmad, N., Miamidian, J.L., Harvey, P.E., Sharron, M., Pohlmann, S., Sfakianos, J.N., Derdeyn, C.A., Blumenthal, R., Hunter, E., and Doms, R.W. (2002) Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc. Natl. Acad. Sci. U. S. A. 99, 16249-16254.
33. Haque, M.E., Koppaka, V., Axelsen, P.H., and Lentz, B.R. (2005) Properties and structures of the influenza and HIV fusion peptides on lipid membranes: implications for a role in fusion. Biophys. J. 89, 3183-3194.
34. Doms, R.W. and Trono, D. (2000) The plasma membrane as a combat zone in the HIV battlefield. Genes Dev. 14, 2677-2688.
35. Suzuki, T. and Suzuki, Y. (2006) Virus infection and lipid rafts. Biol. Pharm. Bull. 29, 1538-1541.
36. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J., and Hendrickson, W.A. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659.
37. Reeves, J.D., Lee, F.H., Miamidian, J.L., Jabara, C.B., Juntilla, M.M., and Doms, R.W. (2005) Enfuvirtide resistance mutations: impact on human immunodeficiency virus envelope function, entry inhibitor sensitivity, and virus neutralization. J. Virol. 79, 4991-4999.
38. Rimsky, L.T., Shugars, D.C., and Matthews, T.J. (1998) Determinants of human immunodeficiency virus type 1 resistance to gp41-derived inhibitory peptides. J. Virol. 72, 986-993.
39. Wild, C.T., Shugars, D.C., Greenwell, T.K., McDanal, C.B., and Matthews, T.J. (1994) Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. U. S. A. 91, 9770-9774.
40. Furuta, R.A., Wild, C.T., Weng, Y., and Weiss, C.D. (1998) Capture of an early fusion-active conformation of HIV-1 gp41. Nat. Struct. Biol. 5, 276-279.
41. Frey, G., Peng, H., Rits-Volloch, S., Morelli, M., Cheng, Y., and Chen, B. (2008) A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 105, 3739-3744.
42. Munoz-Barroso, I., Durell, S., Sakaguchi, K., Appella, E., and Blumenthal, R. (1998) Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J. Cell Biol. 140, 315-323.
43. Miyauchi, K., Kim, Y., Latinovic, O., Morozov, V., and Melikyan, G.B. (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137, 433-444.
44. Lescar, J., Roussel, A., Wien, M.W., Navaza, J., Fuller, S.D., Wengler, G., and Rey, F.A. (2001) The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105, 137-148.
45. Zhang, W., Mukhopadhyay, S., Pletnev, S.V., Baker, T.S., Kuhn, R.J., and Rossmann, M.G. (2002) Placement of the structural proteins in Sindbis virus. J. Virol. 76, 11645-11658.
46. Voisset, C. and Dubuisson, J. (2004) Functional hepatitis C virus envelope glycoproteins. Biol. Cell 96, 413-420.
47. Penin, F., Dubuisson, J., Rey, F.A., Moradpour, D., and Pawlotsky, J.M. (2004) Structural biology of hepatitis C virus. Hepatology 39, 5-19.
48. Op De Beeck, A. and Dubuisson, J. (2003) Topology of hepatitis C virus envelope glycoproteins. Rev. Med. Virol. 13, 233-241.
49. Rey, F.A., Heinz, F.X., Mandl, C., Kunz, C., and Harrison, S.C. (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375, 291-298.
50. Modis, Y., Ogata, S., Clements, D., and Harrison, S.C. (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427, 313-319.
51. Nybakken, G.E., Nelson, C.A., Chen, B.R., Diamond, M.S., and Fremont, D.H. (2006) Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 80, 11467-11474.
52. Schibli, D.J. and Weissenhorn, W. (2004) Class I and class II viral fusion protein structures reveal similar principles in membrane fusion (Review). Mol. Membr. Biol. 21, 361-371.
53. Helenius, A., Kartenbeck, J., Simons, K., and Fries, E. (1980) On the entry of Semliki forest virus into BHK-21 cells. J. Cell Biol. 84, 404-420.
54. Smit, J.M., Li, G., Schoen, P., Corver, J., Bittman, R., Lin, K.C., and Wilschut, J. (2002) Fusion of alphaviruses with liposomes is a non-leaky process. FEBS Lett. 521, 62-66.
55. Paredes, A.M., Ferreira, D., Horton, M., Saad, A., Tsuruta, H., Johnston, R., Klimstra, W., Ryman, K., Hernandez, R., Chiu, W., and Brown, D.T. (2004) Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 324, 373-386.
56. Wang, G., Hernandez, R., Weninger, K., and Brown, D.T. (2007) Infection of cells by Sindbis virus at low temperature. Virology 362, 461-467.
57. Mukhopadhyay, S., Zhang, W., Gabler, S., Chipman, P.R., Strauss, E.G., Strauss, J.H., Baker, T.S., Kuhn, R.J., and Rossmann, M.G. (2006) Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14, 63-73.
58. Wessels, L., Elting, M.W., Scimeca, D., and Weninger, K. (2007) Rapid membrane fusion of individual virus particles with supported lipid bilayers. Biophys. J. 93, 526-538.
59. Zaitseva, E., Mittal, A., Griffin, D.E., and Chernomordik, L.V. (2005) Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J. Cell Biol. 169, 167-177.
60. 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.
61. Jardetzky, T.S. and Lamb, R.A. (2004) Virology: a class act. Nature 427, 307-308.
62. Cohen, F.S. and Melikyan, G.B. (2004) The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199, 1-14.
63. Weissenhorn, W., Hinz, A., and Gaudin, Y. (2007) Virus membrane fusion. FEBS Lett. 581, 2150-2155.
64. Kadlec, J., Loureiro, S., Abrescia, N.G., Stuart, D.I., and Jones, I.M. (2008) The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 15, 1024-1030.
65. Roche, S., Bressanelli, S., Rey, F.A., and Gaudin, Y. (2006) Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313, 187-191.
66. Heldwein, E.E., Lou, H., Bender, F.C., Cohen, G.H., Eisenberg, R.J., and Harrison, S.C. (2006) Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313, 217-220.
67. Gaudin, Y. (2000) Rabies virus-induced membrane fusion pathway. J. Cell Biol. 150, 601-612.
68. Markovic, I., Pulyaeva, H., Sokoloff, A., and Chernomordik, L.V. (1998) Membrane fusion mediated by baculovirus gp64 involves assembly of stable gp64 trimers into multiprotein aggregates. J. Cell Biol. 143, 1155-1166.
69. Wickner, W. and Schekman, R. (2008) Membrane fusion. Nat. Struct. Mol. Biol. 15, 658-664.
70. 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.
71. Bowen, M.E., Weninger, K., Brunger, A.T., and Chu, S. (2004) Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs). Biophys. J. 87, 3569-3584.
72. Parpura, V. and Mohideen, U. (2008) Molecular form follows function: (un)snaring the SNAREs. Trends Neurosci. 31, 435-443.
73. Rizo, J. and Rosenmund, C. (2008) Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665-674.
74. Sutton, R.B., Fasshauer, D., Jahn, R., and Brunger, A.T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353.
75. Antonin, W., Fasshauer, D., Becker, S., Jahn, R., and Schneider, T.R. (2002) Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 9, 107-111.
76. Malinin, V.S. and Lentz, B.R. (2004) Energetics of vesicle fusion intermediates: comparison of calculations with observed effects of osmotic and curvature stresses. Biophys. J. 86, 2951-2964.
77. Farsad, K. and De Camilli, P. (2003) Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372-381.
78. Lang, T., Halemani, N.D., and Rammner, B. (2008) Interplay between lipids and the proteinaceous membrane fusion machinery. Prog. Lipid Res. 47, 461-469.
79. Waarts, B.L., Bittman, R., and Wilschut, J. (2002) Sphingolipid and cholesterol dependence of alphavirus membrane fusion. Lack of correlation with lipid raft formation in target liposomes. J. Biol. Chem. 277, 38141-38147.
80. Rawicz, W., Smith, B.A., McIntosh, T.J., Simon, S.A., and Evans, E. (2008) Elasticity, strength, and water permeability of bilayers that contain raft microdomain-forming lipids. Biophys. J. 94, 4725-4736.
81. Hung, W.C., Lee, M.T., Chen, F.Y., and Huang, H.W. (2007) The condensing effect of cholesterol in lipid bilayers. Biophys. J. 92, 3960-3967.
82. Vashishtha, M., Phalen, T., Marquardt, M.T., Ryu, J.S., Ng, A.C., and Kielian, M. (1998) A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J. Cell Biol. 140, 91-99.
83. Smit, J.M., Waarts, B.L., Bittman, R., and Wilschut, J. (2003) Liposomes as target membranes in the study of virus receptor interaction and membrane fusion. Methods Enzymol. 372, 374-392.
84. 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.
85. 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.
86. Agrawal, P., Kiihne, S., Hollander, J., Hulsbergen, F., Hofmann, M., Langosch, D., and 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.
87. 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.
88. Yang, L. and Huang, H.W. (2002) Observation of a membrane fusion intermediate structure. Science 297, 1877-1879.
89. Gruner, S.M. (2002) Caught in the act. Science 297, 1817-1818.
90. Nunes-Correia, I., Eulalio, A., Nir, S., Duzgunes, N., Ramalho-Santos, J., and Pedroso de Lima, M.C. (2002) Fluorescent probes for monitoring virus fusion kinetics: comparative evaluation of reliability. Biochim. Biophys. Acta 1561, 65-75.
91. Razinkov, V.I., HernandezJimenez, E.I., Mikhalyov, I.I., Cohen, F.S., and Molotkovsky, J.G. (1997) New fluorescent lysolipids: preparation and selective labeling of inner liposome leaflet. Biochim. Biophys. Acta 1329, 149-158.
92. Bonnafous, P. and Stegmann, T. (2003) Pore formation in target liposomes by viral fusion proteins. Methods Enzymol. 372, 408-418.
93. Chizmadzhev, Y.A. (2004) The mechanisms of lipid-protein rearrangements during viral infection. Bioelectrochemistry 63, 129-136.
94. Yoon, T.Y., Lu, X., Diao, J., Lee, S.M., Ha, T., and Shin, Y.K. (2008) Complexin and Ca2+ stimulate SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 15, 707-713.
95. Estes, D.J., Lopez, S.R., Fuller, A.O., and Mayer, M. (2006) Triggering and visualizing the aggregation and fusion of lipid membranes in microfluidic chambers. Biophys. J. 91, 233-243.
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. Kemble, G.W., Henis, Y.I., and White, J.M. (1993) GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity. J. Cell Biol. 122, 1253-1265.
98. Kemble, G.W., Danieli, T., and White, J.M. (1994) Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76, 383-391.
99. Schroth-Diez, B., Ludwig, K., Baljinnyam, B., Kozerski, C., Huang, Q., and Herrmann, A. (2000) The role of the transmembrane and of the intraviral domain of glycoproteins in membrane fusion of enveloped viruses. Biosci. Rep. 20, 571-595.
100. Chatterjee, P.K., Vashishtha, M., and Kielian, M. (2000) Biochemical consequences of a mutation that controls the cholesterol dependence of Semliki Forest virus fusion. J. Virol. 74, 1623-1631.
101. Duffus, W.A., Levy-Mintz, P., Klimjack, M.R., and Kielian, M. (1995) Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly. J. Virol. 69, 2471-2479.
102. West, J., Hernandez, R., Ferreira, D., and Brown, D.T. (2006) Mutations in the endodomain of Sindbis virus glycoprotein E2 define sequences critical for virus assembly. J. Virol. 80, 4458-4468.
103. Whitehurst, C.B., Willis, J.H., Sinodis, C.N., Hernandez, R., and Brown, D.T. (2006) Single and multiple deletions in the transmembrane domain of the Sindbis virus E2 glycoprotein identify a region critical for normal virus growth. Virology 347, 199-207.
104. Navaratnarajah, C.K. and Kuhn, R.J. (2007) Functional characterization of the Sindbis virus E2 glycoprotein by transposon linker-insertion mutagenesis. Virology 363, 134-147.
105. Epand, R.M. (2003) Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta 1614, 116-121.
106. Hua, Y. and Scheller, R.H. (2001) Three SNARE complexes cooperate to mediate membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 98, 8065-8070.
107. Wilson, I.A., Skehel, J.J., and Wiley, D.C. (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289, 366-373.
108. Kanaseki, T., Kawasaki, K., Murata, M., Ikeuchi, Y., and Ohnishi, S. (1997) Structural features of membrane fusion between influenza virus and liposome as revealed by quick-freezing electron microscopy. J. Cell Biol. 137, 1041-1056.
109. Russell, R.J., Kerry, P.S., Stevens, D.J., Steinhauer, D.A., Martin, S.R., Gamblin, S.J., and Skehel, J.J. (2008) Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 105, 17736-17741.
110. von Bonsdorff, C.H. and Harrison, S.C. (1975) Sindbis virus glycoproteins form a regular icosahedral surface lattice. J. Virol. 16, 141-145.
111. Curtis, H. (1989) Biology. Worth, New York.
112. 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. U. S. A. 103, 19731-19736.
113. Peisajovich, S.G. and Shai, Y. (2003) Liposomes in identification and characterization of viral fusogenic peptides. Methods Enzymol. 372, 361-373.
114. Ohki, S., Flanagan, T.D., and Hoekstra, D. (1998) Probe transfer with and without membrane fusion in a fluorescence fusion assay. Biochemistry 37, 7496-7503.
115. Thongthai, W. and Weninger, K. (2008) Photoinactivation of Sindbis virus infectivity without inhibition of membrane fusion. Photochem. Photobiol. 85, 801-806.
116. Yoshina-Ishii, C. and Boxer, S.G. (2003) Arrays of mobile tethered vesicles on supported lipid bilayers. J. Am. Chem. Soc. 125, 3696-3697.
117. Boukobza, E., Sonnenfeld, A., and Haran, G. (2001) Immobilization in surface-tethered lipid vesicles as a new tool for single biomolecule spectroscopy. J. Phys. Chem. B 105, 12165-12170.
118. Manley, S., Horton, M.R., Lecszynski, S., and Gast, A.P. (2008) Sorting of streptavidin protein coats on phase-separating model membranes. Biophys. J. 95, 2301-2307.
119. Ewers, H., Jacobsen, V., Klotzsch, E., Smith, A.E., Helenius, A., and Sandoghdar, V. (2007) Label-free optical detection and tracking of single virions bound to their receptors in supported membrane bilayers. Nano Lett. 7, 2263-2266.
120. Greber, U.F. and Way, M. (2006) A superhighway to virus infection. Cell 124, 741-754.
121. Marsh, M. and Helenius, A. (2006) Virus entry: open sesame. Cell 124, 729-740.
122. Pelkmans, L. and Helenius, A. (2003) Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15, 414-422.
123. Brandenburg, B. and Zhuang, X. (2007) Virus trafficking - learning from single-virus tracking. Nat. Rev. Microbiol. 5, 197-208.
124. Seisenberger, G., Ried, M.U., Endress, T., Buning, H., Hallek, M., and Brauchle, C. (2001) Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294, 1929-1932.
125. Finke, S., Brzozka, K., and Conzelmann, K.K. (2004) Tracking fluorescence-labeled rabies virus: enhanced green fluorescent protein-tagged phosphoprotein P supports virus gene expression and formation of infectious particles. J. Virol. 78, 12333-12343.
126. van der Schaar, H.M., Rust, M.J., Waarts, B.L., van der Ende-Metselaar, H., Kuhn, R.J., Wilschut, J., Zhuang, X., and Smit, J.M. (2007) Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J. Virol. 81, 12019-12028.
127. Melikyan, G.B., Barnard, R.J., Abrahamyan, L.G., Mothes, W., and Young, J.A. (2005) Imaging individual retroviral fusion events: from hemifusion to pore formation and growth. Proc. Natl. Acad. Sci. U. S. A. 102, 8728-8733.
128. Markosyan, R.M., Cohen, F.S., and Melikyan, G.B. (2005) Time-resolved imaging of HIV-1 Env-mediated lipid and content mixing between a single virion and cell membrane. Mol. Biol. Cell 16, 5502-5513.
129. Lakadamyali, M., Rust, M.J., Babcock, H.P., and Zhuang, X. (2003) Visualizing infection of individual influenza viruses. Proc. Natl. Acad. Sci. U. S. A. 100, 9280-9285.
130. Lakadamyali, M., Rust, M.J., and Zhuang, X. (2004) Endocytosis of influenza viruses. Microbes Infect. 6, 929-936.
131. Jaiswal, J.K. and Simon, S.M. (2007) Imaging single events at the cell membrane. Nat. Chem. Biol. 3, 92-98.
132. Marrink, S.J. and Tieleman, D.P. (2002) Molecular dynamics simulation of spontaneous membrane fusion during a cubic-hexagonal phase transition. Biophys. J. 83, 2386-2392.
133. Tieleman, D.P. and Bentz, J. (2002) Molecular dynamics simulation of the evolution of hydrophobic defects in one monolayer of a phosphatidylcholine bilayer: relevance for membrane fusion mechanisms. Biophys. J. 83, 1501-1510.
134. 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. U. S. A. 103, 11916-11921.
135. Gibbons, M.M. and Klug, W.S. (2008) Influence of nonuniform geometry on nanoindentation of viral capsids. Biophys. J. 95, 3640-3649.
136. Tumpey, T.M., Garcia-Sastre, A., Mikulasova, A., Taubenberger, J.K., Swayne, D.E., Palese, P., and Basler, C.F. (2002) Existing antivirals are effective against influenza viruses with genes from the 1918 pandemic virus. Proc. Natl. Acad. Sci. U. S. A. 99, 13849-13854.
137. Sui, J., Hwang, W.C., Perez, S., Wei, G., Aird, D., Chen, L.M., Santelli, E., Stec, B., Cadwell, G., Ali, M., Wan, H., Murakami, A., Yammanuru, A., Han, T., Cox, N.J., Bankston, L.A., Donis, R.O., Liddington, R.C., and Marasco, W.A. (2009) Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16, 265-273.
138. Kilby, J.M., Hopkins, S., Venetta, T.M., DiMassimo, B., Cloud, G.A., Lee, J.Y., Alldredge, L., Hunter, E., Lambert, D., Bolognesi, D., Matthews, T., Johnson, M.R., Nowak, M.A., Shaw, G.M., and Saag, M.S. (1998) Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. Nat. Med. 4, 1302-1307.
139. Poveda, E., Briz, V., and Soriano, V. (2005) Enfuvirtide, the first fusion inhibitor to treat HIV infection. AIDS Rev. 7, 139-147.
140. Strockbine, B. and Rizzo, R.C. (2007) Binding of antifusion peptides with HIVgp41 from molecular dynamics simulations: quantitative correlation with experiment. Proteins 67, 630-642.
141. Eckert, D.M. and Kim, P.S. (2001) Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70, 777-810.
142. Markosyan, R.M., Cohen, F.S., and Melikyan, G.B. (2005) Time-resolved imaging of HIV-1 Env-mediated lipid and content mixing between a single virion and cell membrane. Mol. Biol. Cell 16, 5502-5513.
143. Kopetzki, E., Jekle, A., Ji, C., Rao, E., Zhang, J., Fischer, S., Cammack, N., Sankuratri, S., and Heilek, G. (2008) Closing two doors of viral entry: intramolecular combination of a coreceptor- and fusion inhibitor of HIV-1. Virol. J. 5, 56.
144. Ji, C., Kopetzki, E., Jekle, A., Stubenrauch, K.-G., Liu, X., Zhang, J., Rao, E., Schlothauer, T., Fischer, S., Cammack, N., Heilek, G., Ries, S., and Sankuratri, S. (2009) CD4-anchoring HIV-1 fusion inhibitor with enhanced potency and in vivo stability. J. Biol. Chem. 284, 5175-5185.