What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion (Review)

References

• Almers W., Tse F. W. Transmitter release from synapses: Does a preassembled fusion pore initiate exocytosis. Neuron 1990; 4: 813–818
   PubMed Web of Science ®Google Scholar
• Bairoch A., Boeckmann B. The SWISS-PROT protein sequence data bank. Nucleic Acids Research 1992; 20: 2019–2022
   PubMed Web of Science ®Google Scholar
• Bentz J., Ellens H., Alford D. Architecture of the influenza hemagglutinin membrane fusion site. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 163–199
   Google Scholar
• Binley J., Moore J. P. The viral mousetrap. Nature 1997; 387: 346–348
   PubMed Web of Science ®Google Scholar
• Blumenthal R., Dimitrov D. S. Membrane fusion. Handbook of Physiology, J. F. Hoffman, J. C. Jamieson. Oxford University Press, New York 1997; 569–604
   Google Scholar
• Blumenthal R., Sarkar D. P., Durell S., Howard D. E., Morris S. J. Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. Journal of Cell Biology 1996; 135: 63–71
   PubMed Web of Science ®Google Scholar
• Booy F. P. Cryoelectron microscopy. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 21–54
   Google Scholar
• Bosch M. L., Earl P. L., Fargnoli K., Picciafuoco S., Giombini F., Wong-Staal F., Franchini G. Identification of the fusion peptide of primate immunodeficiency viruses. Science 1989; 244: 694–697
   PubMed Web of Science ®Google Scholar
• Brasseur R., Vandenbranden M., Cornet B., Burny A., Ruysschaert J.-M. Orientation into the lipid bilayer of an asymmetric amphipathic helical peptide located at the N-terminus of viral fusion proteins. Biochimica et Biophysica Acta 1990; 1029: 267–273
   PubMed Web of Science ®Google Scholar
• Broder C. C., Dimitrov D. S. HIV and the 7-transmembrane-domain receptors. Pathobiology 1996; 64: 171–179
   PubMed Web of Science ®Google Scholar
• Brunner J. Testing topological models for the membrane penetration of the fusion peptide of influenza virus hemagglutinin. FEBS Letters 1989; 257: 369–372
   PubMed Web of Science ®Google Scholar
• Brunner J. New photolabeling and crosslinking methods. Annual Review of Biochemistry 1993; 62: 483–514
   PubMed Web of Science ®Google Scholar
• Brunner J., Tsurudome M. Fusion-protein membrane interactions as studied by hydrophobic photolabeling. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 67–88
   Google Scholar
• Brunner J., Zugliani C., Mischler R. Fusion activity of influenza virus PR8/34 correlates with a temperature-induced conformational change within the hemagglutinin ectodomain detected by photochemical labeling. Biochemistry 1991; 30: 2432–2438
   PubMed Web of Science ®Google Scholar
• Buckland R., Malvoisin E., Beauverger P., Wild F. A leucine zipper structure present in the measles virus fusion protein is not required for its tetramerization but is essential for fusion. Journal of General Virology 1992; 73: 1703–1707
   PubMed Web of Science ®Google Scholar
• Bullough P. A., Hughson F. M., Skehel J. J., Wiley D. C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 1994; 371: 37–43
   PubMed Web of Science ®Google Scholar
• Burger K. N., Wharton S. A., Demel R. A., Verkleij A. J. The interaction of synthetic analogs of the N-terminal fusion sequence of influenza virus with a lipid monolayer. Comparison of fusion-active and fusion-defective analogs. Biochimica et Biophysica Acta 1991; 1065: 121–129
   PubMedGoogle Scholar
• Carr C. M., Kim P. S. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 1993; 73: 823–832
   PubMed Web of Science ®Google Scholar
• Chan D. C., Fass D., Berger J. M., Kim P. S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997; 89: 263–273
   PubMed Web of Science ®Google Scholar
• Chandler D. E., Heuser J. Membrane fusion during secretion: cortical granule exocytosis in sex urchin eggs as studied by quick-freezing and freeze-fracture. Journal of Cell Biology 1979; 83: 91–108
   PubMed Web of Science ®Google Scholar
• Chernomordik L., Kozlov M. M., Zimmerberg J. Lipids in biological membrane fusion. Journal of Membrane Biology 1995; 146: 1–14
   PubMed Web of Science ®Google Scholar
• Chothia C., Levitt M., Richardson D. Helix to helix packing in proteins. Journal of Molecular Biology 1981; 145: 215–250
   PubMed Web of Science ®Google Scholar
• Clague M. J., Schoch C., Blumenthal R. Delay time for influenza virus hemagglutinin-induced membrane fusion depends on hemagglutinin surface density. Journal of Virology 1991; 65: 2402–2407
   PubMed Web of Science ®Google Scholar
• Clague M. J., Schoch C., Blumenthal R. Toward a dissection of the influenza hemagglutinin-mediated membrane fusion pathway. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 113–132
   Google Scholar
• Colotto A., Martin I., Ruysschaert J.-M., Sen A., Hui S. W., Epand R. M. Structural study of the interaction between the SIV fusion peptide and model membranes. Biochemistry 1996; 35: 980–989
   PubMed Web of Science ®Google Scholar
• Cosson P., Bonifacino J. S. Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science 1992; 258: 659–662
   PubMed Web of Science ®Google Scholar
• Crick F. H. C. The packing of α-helices: simple coiled-coils. Acta Crystallography 1953; 6: 689–697
   Web of Science ®Google Scholar
• Danieli T., Pelletier S. L., Henis Y. I., White J. M. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. Journal of Cell Biology 1996; 133: 559–569
   PubMed Web of Science ®Google Scholar
• Daniels R. S., Downie J. C., Hay A. J., Knossow M., Skehel J. J., Wang M. L., Wiley D. C. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 1985; 40: 431–439
   PubMed Web of Science ®Google Scholar
• Delahunty M. D., Rhee I., Freed E. O., Bonifacino J. S. Mutational analysis of the fusion peptide of the human immunodeficiency virus type 1: identification of critical glycine residues. Virology 1996; 218: 94–102
   PubMed Web of Science ®Google Scholar
• Delwart E. L., Buchschacher G. L., Jr., Freed E. O., Panganiban A. T. Analysis of HIV-1 envelope mutants and pseudotyping of replication-defective HIV-1 vectors by genetic complementation. Aids Research and Human Retroviruses 1992; 8: 1669–1677
   PubMed Web of Science ®Google Scholar
• Delwart E. L., Mosialos G., Gilmore T. Retroviral envelope glycoproteins contain a ‘leucine zipper’-like repeat. AIDS Research and Human Retroviruses 1990; 6: 703–706
   PubMed Web of Science ®Google Scholar
• Doms R. W., Gething M. J., Henneberry J., White J., Helenius A. Variant influenza virus hemagglutinin that induces fusion at elevated pH. Journal of Virology 1986; 57: 603–613
   PubMed Web of Science ®Google Scholar
• Doms R. W., Lamb R. A., Rose J. K., Helenius A. Folding and assembly of viral membrane proteins. Virology 1993; 193: 545–562
   PubMed Web of Science ®Google Scholar
• Dubay J. W., Roberts S. J., Brody B., Hunter E. Mutations in the leucine zipper of the human immunodeficiency virus type 1 transmembrane glycoprotein affect fusion and infectivity. Journal of Virology 1992; 66: 4748–4756
   PubMed Web of Science ®Google Scholar
• Durrer P., Galli C., Hoenke S., Corti C., Gluck R., Vorherr T., Brunner J. H+-induced membrane insertion of influenza virus hemagglutinin involves the HA2 amino-terminal fusion peptide but not the coiled coil region. Journal of Biological Chemistry 1996; 271: 13417–13421
   PubMed Web of Science ®Google Scholar
• Durrer P., Gaudin Y., Ruigrok R. W., Graf R., Brunner J. Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. Journal of Biological Chemistry 1995; 270: 17575–17581
   PubMed Web of Science ®Google Scholar
• Duzgunes N., Gambale F. Membrane action of synthetic Nterminal peptides of influenza virus hemagglutinin and its mutants. FEBS Letters 1988; 227: 110–114
   PubMed Web of Science ®Google Scholar
• Ellens H., Bentz J., Mason D., Zhang F., White J. M. Fusion of influenza hemagglutinin-expressing fibroblasts with glycophorin-bearing liposomes: role of hemagglutinin surface density. Biochemistry 1990; 29: 9697–9707
   PubMed Web of Science ®Google Scholar
• Elson H. F., Dimitrov D. S., Blumenthal R. A trans-dominant mutation in human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein gp41 inhibits membrane fusion when expressed in target cells. Molecular Membrane Biology 1994; 11: 165–169
   PubMed Web of Science ®Google Scholar
• Epand R. M. Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry 1985; 24: 7092–7095
   PubMed Web of Science ®Google Scholar
• Epand R. M., Epand R. F. Relationship between the infectivity of influenza virus and the ability of its fusion peptide to perturb bilayers. Biochemical and Biophysical Research Communications 1994; 202: 1420–1425
   PubMed Web of Science ®Google Scholar
• Epand R. M., Epand R. F., Ahmed N., Chen R. Promotion of hexagonal phase formation and lipid mixing by fatty acids with varying degrees of unsaturation. Chemistry and Physics of Lipids 1991; 57: 75–80
   PubMed Web of Science ®Google Scholar
• Epand R. F., Martin I., Ruysschaert J.-M., Epand R. M. Membrane orientation of the SIV fusion peptide determines its effect on bilayer stability and ability to promote membrane fusion. Biochemical and Biophysical Research Communications 1994; 205: 1938–1943
   PubMed Web of Science ®Google Scholar
• Fass D., Harrison S. C., Kim P. S. Retrovirus envelope domain at 1.7 Å resolution. Nature Structural Biology 1996; 3: 465–469
   PubMedGoogle Scholar
• Formanowski F., Wharton S. A., Calder L. J., Hofbauer C., Meier-Ewert H. Fusion characteristics of influenza C viruses. Journal of General Virology 1990; 71: 1181–1188
   PubMed Web of Science ®Google Scholar
• Fredericksen B. L., Whitt M. A. Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity. Journal of Virology 1995; 69: 1435–1443
   PubMed Web of Science ®Google Scholar
• Freed E. O., Delwart E. L., Buchschacher G. L., Jr., Panganiban A. T. A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proceedings of the National Academy of Sciences, USA 1992; 89: 70–74
   PubMed Web of Science ®Google Scholar
• Freed E. O., Myers D. J., Risser R. Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proceedings of the National Academy of Sciences, USA 1990; 87: 4650–4654
   PubMed Web of Science ®Google Scholar
• Fringeli U. R., Günthard M. H. Infrared membrane spectroscopy. Membrane Spectroscopy, E. Grell. Springer-Verlag, Berlin, New York 1981; 270–332
   Google Scholar
• Gallaher W. R. Detection of a fusion peptide sequence in the transmembrane protein of human immunodeficiency virus. Cell 1987; 50: 327–328
   PubMed Web of Science ®Google Scholar
• Gallaher W. R., Ball J. M., Garry R. F., Griffin M. C., Montelaro R. C. A general model for the transmembrane proteins of HIV and other retroviruses. AIDS Research and Human Retroviruses 1989; 5: 431–440
   PubMed Web of Science ®Google Scholar
• Gallaher W. R., Segrest J. P., Hunter E. Are fusion peptides really ‘sided’ insertional helices. Cell 1992; 70: 531–532
   PubMed Web of Science ®Google Scholar
• Gaudin Y., Ruigrok R. W. H., Brunner J. Low-pH induced conformational changes in viral fusion proteins: implications for the fusion mechanism. Journal of General Virology 1995; 76: 1541–1556
   PubMed Web of Science ®Google Scholar
• Gazit E., Shai Y. Structural characterization, membrane interaction, and specific assembly within phospholipid membranes of hydrophobic segments from Bacillus thuringiensis var. israelensis cytolytic toxin. Biochemistry 1993; 32: 12363–12371
   PubMed Web of Science ®Google Scholar
• Gething M. J., Doms R. W., York D., White J. Studies on the mechanism of membrane fusion: site-specific mutagenesis of hemagglutinin of influenza virus. Journal of Cell Biology 1986; 102: 11–23
   PubMed Web of Science ®Google Scholar
• Gonzalez-Scarano F., Waxham M. N., Ross A. M., Hoxie J. A. Sequence similarities between human immunodeficiency virus gp41 and paramyxovirus fusion proteins. AIDS Research and Human Retroviruses 1987; 3: 245–252
   PubMed Web of Science ®Google Scholar
• Goormaghtigh E., Cabiaux V., Ruysschaert J.-M. Secondary structure and dosage of soluble and membrane proteins by attenuated total reflection Fourier-transform infrared spectroscopy on hydrated film. European Journal of Biochemistry 1990; 193: 409–420
   PubMedGoogle Scholar
• Goormaghtigh E., Cabiaux V., Ruysschaert J.-M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. Subcellular Biochemistry 1995; 23: 405–450
   Google Scholar
• Goormaghtigh E., Martin I., Vandenbranden M., Brasseur R., Ruysschaert J.-M. Secondary structure and orientation of a chemically synthesized mitochondrial signal sequence in phospholipid bilayers. Biochemical and Biophysical Research Communications 1989; 158: 610–616
   PubMed Web of Science ®Google Scholar
• Goormaghtigh E., Vigneron L., Knibiehler M., Lazdunski C., Ruysschaert J.-M. Secondary structure of the membrane-bound form of the pore-forming domain of colicin A: a FTIR-ATR study. European Journal of Biochemistry 1991; 202: 1299–1305
   PubMedGoogle Scholar
• Gordon L. M., Curtain C. C., Zhong Y. C., Kirkpatrick A., Mobley P. W., Waring A. J. The amino-terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: peptide conformation, orientation and aggregation. Biochimica et Biophysica Acta 1992; 1139: 257–274
   PubMed Web of Science ®Google Scholar
• 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. Biophysical Journal 1996; 70: 2275–2286
   PubMed Web of Science ®Google Scholar
• Guy H. R., Durell S. R. Using sequence homology to analyze the structure and function of voltage-gated ion channel proteins. Molecular Evolution of Physiological Processes, Society of General Physiologists, D. M. Fambrough. Rockefeller Univ. Press, New York 1994; 197–212, 47th Annual Symposium
   Google Scholar
• Guy H. R., Durell S. R. Developing three-dimensional models of ion channel proteins. Ion Channels, Vol. 4, T. Narahashi. Plenum Press, New York 1996; 1–40
   Google Scholar
• Harter C., Bachi T., Semenza G., Brunner J. Hydrophobic photolabeling identifies BHA2 as the subunit mediating the interaction of bromelain-solubilized influenza virus hemagglutinin with liposomes at low pH. Biochemistry 1988; 27: 1856–1864
   PubMed Web of Science ®Google Scholar
• Harter C., James P., Bachi T., Semenza G., Brunner J. Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the ‘fusion peptide’. Journal of Biological Chemistry 1989; 264: 6459–6464
   PubMed Web of Science ®Google Scholar
• Haywood A. M., Boyer B. P. Initiation of fusion and disassembly of Sendai virus membrane into liposomes. Biochimica et Biophysica Acta 1981; 646: 31–35
   PubMed Web of Science ®Google Scholar
• Horth M., Lambrecht B., Marinee C., Bex F., Thiriart C., Ruysschaert J.-M., Burny A., Brasseur R. Theoretical and functional analysis of the SIV fusion peptide. EMBO Journal 1991; 10: 2747–2755
   PubMed Web of Science ®Google Scholar
• Horvath C. M., Lamb R. A. Studies on the fusion peptide of a paramyxovirus fusion glycoprotein: roles of conserved residues in cell fusion. Journal of Virology 1992; 66: 2443–2455
   PubMed Web of Science ®Google Scholar
• Hughson F. M. Structural characterization of viral fusion proteins. Current Biology 1995; 5: 265–274
   PubMed Web of Science ®Google Scholar
• Ishiguro R., Kimura N., Takahashi S. Orientation of fusionactive synthetic peptides in phospholipid bilayers: determination by Fourier transform infrared spectroscopy. Biochemistry 1993; 32: 9792–9797
   PubMed Web of Science ®Google Scholar
• Ishiguro R., Matsumoto M., Takahashi S. Interaction of fusogenic synthetic peptide with phospholipid bilayers: orientation of the peptide alpha-helix and binding isotherm. Biochemistry 1996; 35: 4976–4983
   PubMed Web of Science ®Google Scholar
• Kemble G. W., Danieli T., White J. M. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 1994; 76: 383–391
   PubMed Web of Science ®Google Scholar
• Kliger Y., Aharoni A., Rapaport D., Jones P., Blumenthal R., Shai Y. Fusion peptides derived from the HIV type I glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion: structure-function study. Journal of Biological Chemistry 1997; 272: 13496–13505
   PubMed Web of Science ®Google Scholar
• Lear J. D., DeGrado W. F. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. Journal of Biological Chemistry 1987; 262: 6500–6505
   PubMed Web of Science ®Google Scholar
• Lemmon M. A., Flanagan J. M., Treutlein H. R., Zhang J., Engelman D. M. Sequence specificity in the dimerization of transmembrane α-helices. Biochemistry 1992; 31: 12719–12725
   PubMed Web of Science ®Google Scholar
• Lindau M., Almers W. Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Current Opinion in Cell Biology 1995; 7: 509–517
   PubMed Web of Science ®Google Scholar
• Lowy R. J., Sarkar D. P., Chen Y., Blumenthal R. Single Influenza virus-cell fusion events observed by Fluorescent Video Microscopy. Proceedings of the National Academy of Sciences, USA 1990; 87: 1850–1854
   PubMed Web of Science ®Google Scholar
• Lüneberg J., Martin I., Nussler F., Ruysschaert J.-M., Herrmann A. Structure and topology of the influenza virus fusion peptide in lipid bilayers. Journal of Biological Chemistry 1995; 270: 27606–27614
   PubMed Web of Science ®Google Scholar
• Marsh M., Helenius A. Virus entry into animal cells. Advances in Virus Research 1989; 36: 107–151
   PubMed Web of Science ®Google Scholar
• Martin I., Defrise-Quertain F., Decroly E., Vandenbranden M., Brasseur R., Ruysschaert J.-M. Orientation and structure of the NH2-terminal HIV-1 gp41 peptide in fused and aggregated liposomes. Biochimica et Biophysica Acta 1993; 1145: 124–133
   PubMed Web of Science ®Google Scholar
• Martin I., Defrise-Quertain F., Mandieau V., Nielsen N. M., Saermark T., Burny A., Brasseur R., Ruysschaert J.-M., Vandenbranden M. Fusogenic activity of SIV (simian immunodeficiency virus) peptides located in the GP32 NH2 terminal domain. Biochemical and Biophysical Research Communications 1991; 175: 872–879
   PubMed Web of Science ®Google Scholar
• Martin I., Dubois M. C., Defrise-Quertain F., Saermark T., Burny A., Brasseur R., Ruysschaert J.-M. Correlation between fusogenicity of synthetic modified peptides corresponding to the NH2-terminal extremity of simian immunodeficiency virus gp32 and their mode of insertion into the lipid bilayer: an infrared spectroscopy study. Journal of Virology 1994; 68: 1139–1148
   PubMed Web of Science ®Google Scholar
• Martin I., Schaal H., Scheid A., Ruysschaert J.-M. Lipid membrane fusion induced by the human immunodeficiency virus type 1 gp41 N-terminal extremity is determined by its orientation in the lipid bilayer. Journal of Virology 1996; 70: 298–304
   PubMed Web of Science ®Google Scholar
• Melikyan G. B., Niles W. D., Cohen F. S. Influenza virus hemagglutinin-induced cell-planar bilayer fusion: quantitative dissection of fusion pore kinetics into stages. Journal of General Physiology 1993a; 102: 1151–1170
   PubMed Web of Science ®Google Scholar
• Melikyan G. B., Niles W. D., Peeples M. E., Cohen F. S. Influenza hemagglutinin-mediated fusion pores connecting cells to planar membranes: flickering to final expansion. Journal of General Physiology 1993b; 102: 1131–1149
   PubMed Web of Science ®Google Scholar
• Melikyan G. B., White J. M., Cohen F. S. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. Journal of Cell Biology 1995; 131: 679–691
   PubMed Web of Science ®Google Scholar
• Monck J. R., Fernandez J. M. The exocytotic fusion pore. Journal of Cell Biology 1992; 119: 1395–1404
   PubMed Web of Science ®Google Scholar
• Monck J. R., Fernandez J. M. The fusion pore and mechanisms of biological membrane fusion. Current Opinion in Cell Biology 1996; 8: 524–533
   PubMed Web of Science ®Google Scholar
• Moore J. P., Jameson B. A., Weiss R. A., Sattentau Q. The HIV-cell fusion reaction. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 21–54
   Google Scholar
• Morris S. J., Howard D. E., Chang T. H., Sarkar D. P., Blumenthal R. Hemagglutinin-catalyzed cell-cell fusion: kinetics of initial pore formation from video rate, multi-wavelength fluorescence microscopy. Journal of the Microscopy Society of America 1995; 1: 47–54
   Google Scholar
• Murata M., Sugahara Y., Takahashi S., Ohnishi S.-I. pH-Dependent membrane fusion activity of a synthetic twenty amino acid peptide with the same sequence as that of the hydrophobic segment of influenza virus hemagglutinin. Journal of Biochemistry 1987; 102: 957–962
   PubMed Web of Science ®Google Scholar
• Murata M., Takahashi S., Kagiwada S., Suzuki A., Ohnishi S.-I. pH-Dependent membrane fusion and vesiculation of phospholipid large unilamellar vesicles induced by amphiphilic anionic and cationic peptides. Biochemistry 1992; 31: 1986–1992
   PubMed Web of Science ®Google Scholar
• Neher E., Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proceedings of the National Academy of Sciences, USA 1982; 79: 6712–6716
   PubMed Web of Science ®Google Scholar
• Nieva J. L., Nir S., Muga A., Goni F. M., Wilschut J. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: different structural requirements for fusion and leakage. Biochemistry 1994; 33: 3201–3209
   PubMed Web of Science ®Google Scholar
• Ohnishi S. I. Fusion of viral envelopes with cellular membranes. Current Topics in Membranes and Transport 1988; 32: 257–296
   PubMedGoogle Scholar
• Orlich M., Rott R. Thermolysin activation mutants with changes in the fusogenic region of an influenza virus hemagglutinin. Journal of Virology 1994; 68: 7537–7539
   PubMed Web of Science ®Google Scholar
• Pak C. C., Krumbiegel M., Blumenthal R., Raviv Y. Detection of influenza hemagglutinin interaction with biological membranes by photosensitized activation of [125I]iodonaphthylazide. Journal of Biological Chemistry 1994; 269: 14614–14619
   PubMed Web of Science ®Google Scholar
• Pereira F. B., Goni F. M., Nieva J. L. Liposome destabilization induced by the HIV-1 fusion peptide effect of a single amino acid substitution. FEBS Letters 1995; 362: 243–246
   PubMed Web of Science ®Google Scholar
• Puri A., Booy F. P., Doms R. W., White J. M., Blumenthal R. Conformational changes and fusion activity of influenza virus hemagglutinin of the H2 and H3 subtypes: effects of acid pretreatment. Journal of Virology 1990; 64: 3824–3832
   PubMed Web of Science ®Google Scholar
• Rafalski M., Lear J. D., DeGrado W. F. Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41. Biochemistry 1990; 29: 7917–7922
   PubMed Web of Science ®Google Scholar
• Rafalski M., Ortiz A., Rockwell A., van Ginkel L. C., Lear J. D., DeGrado W. F., Wilschult J. Membrane fusion activity of the influenza virus hemagglutinin: interaction of HA2 N-terminal peptides with phospholipid vesicles. Biochemistry 1991; 30: 10211–10220
   PubMed Web of Science ®Google Scholar
• Rapaport D., Shai Y. Interaction of fluorescently labeled analogues of the amino-terminal fusion peptide of Sendai virus with phospholipid membranes. Journal of Biological Chemistry 1994; 269: 15124–15131
   PubMed Web of Science ®Google Scholar
• Raussens V., Goormaghtigh E., Ryan R. O., Ruysschaert J.-M. Orientation of the lipid domains and of the apolipophor-in-III in the insect apolipophorin-III-dimyristoylphosphatidylcholine complexes. Journal of Biological Chemistry 1995; 270: 12542–12547
   PubMedGoogle Scholar
• 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 1995; 375: 291–298
   PubMed Web of Science ®Google Scholar
• Richardson C. D., Choppin P. W. Oligopeptides that specifically inhibit membrane fusion by paramyxoviruses: studies on the site of action. Virology 1983; 131: 518–532
   PubMed Web of Science ®Google Scholar
• Rott R., Orlich M., Klenk H.-D., Wang M. L., Skehel J. J., Wiley D. C. Studies on the adaptation of influenza viruses to MDCK cells. The EMBO Journal 1984; 3: 3329–3332
   PubMed Web of Science ®Google Scholar
• Sarkar D. P., Morris S. J., Eidelman O., Zimmerberg J., Blumenthal R. Initial stages of influenza hemagglutinin-induced cell fusion monitored simultaneously by two fluorescent events: cytoplasmic continuity and lipid mixing. Journal of Cell Biology 1989; 109: 113–122
   PubMed Web of Science ®Google Scholar
• Schaal H., Klein M., Gehrmann P., Adams O., Scheid A. Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion. Journal of Virology 1995; 69: 3308–3314
   PubMed Web of Science ®Google Scholar
• Schoch C., Blumenthal R. Role of the fusion peptide sequence in initial stages of influenza hemagglutinin-induced cell fusion. Journal of Biological Chemistry 1993; 268: 9267–9274
   PubMed Web of Science ®Google Scholar
• Shai Y. Molecular recognition between membrane-spanning polypeptides. Trends in Biochemical Sciences 1995; 20: 460–464
   PubMed Web of Science ®Google Scholar
• Siegel D. P. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophysical Journal 1993a; 65: 2124–2140
   PubMed Web of Science ®Google Scholar
• Siegel D. P. Modeling protein-induced fusion mechanisms: insights from the relative stability of lipidic structures. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993b; 475–512
   Google Scholar
• Spruce A. E., Iwata A., Aimers W. The first milliseconds of the pore formed by a fusogenic viral envelope protein during membrane fusion. Proceedings of the National Academy of Sciences, USA 1991; 88: 3623–3627
   PubMed Web of Science ®Google Scholar
• Spruce A. E., Iwata A., White J. M., Almers W. Patch clamp studies of single cell-fusion events mediated by a viral fusion protein. Nature 1989; 342: 555–558
   PubMed Web of Science ®Google Scholar
• Steffy K. R., Kraus G., Looney D. J., Wong-Staal F. Role of the fusogenic peptide sequence in syncytium induction and infectivity of human immunodeficiency virus type 2. Journal of Virology 1992; 66: 4532–4535
   PubMed Web of Science ®Google Scholar
• Stegmann T. Anchors aweigh. Current Biology 1994; 4: 551–554
   PubMed Web of Science ®Google Scholar
• Stegmann T., Delfino J. M., Richards F. M., Helenius A. The HA2 subunit of influenza hemagglutin inserts into the target membrane prior to fusion. Journal of Biological Chemistry 1991; 266: 18404–18410
   PubMed Web of Science ®Google Scholar
• Stegmann T., Doms R. W., Helenius A. Protein-mediated membrane fusion. Annual Review of Biophysics and Biophysical Chemistry 1989; 18: 187–211
   PubMedGoogle Scholar
• Stegmann T., Helenius A. Influenza virus fusion: from models toward a mechanism. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 89–111
   Google Scholar
• Steinhauer D. A., Wharton S. A., Skehel J. J., Wiley D. C. Studies of the membrane fusion activities of fusion peptide mutants of influenza virus hemagglutinin. Journal of Virology 1995; 69: 6643–6651
   PubMed Web of Science ®Google Scholar
• Takahashi S. Conformation of membrane fusion-active 20 residues peptides with or without lipid bilayers. Implication of α-helix formation for membrane fusion. Biochemistry 1990; 29: 6257–6264
   PubMed Web of Science ®Google Scholar
• Treutlein H. R., Lemmon M. A., Engelman D. M., Brünger A. T. The Glycophorin A transmembrane domain dimer: sequence-specific propensity for a right-handed supercoil of helices. Biochemistry 1992; 31: 12726–12733
   PubMed Web of Science ®Google Scholar
• Tse F. W., Iwata A., Aimers W. Membrane flux through the pore formed by a fusogenic viral envelope protein during cell fusion. Journal of Cell Biology 1993; 121: 543–552
   PubMed Web of Science ®Google Scholar
• Vandenbussche G., Clercx A., Clercx M., Curstedt T., Johansson J., Jornvall H., Ruysschaert J.-M. Secondary structure and orientation of the surfactant protein SP-B in a lipid environment. A Fourier transform infrared spectroscopy study. Biochemistry 1992; 31: 9169–9176
   PubMed Web of Science ®Google Scholar
• Voneche V., Portetelle D., Kettmann R., Willems L., Limbach K., Paoletti E., Ruysschaert J.-M., Burny A., Brasseur R. Fusogenic segments of Bovine Leukemia Virus and Simian Immunodeficiency Virus are interchangeable and mediate fusion via oblique insertion in the lipid bilayer of their target cells. Proceedings of the National Academy Sciences, USA 1992; 89: 3810–3814
   PubMed Web of Science ®Google Scholar
• Walker J. A., Kawaoka Y. Importance of conserved amino acids at the cleavage site of the haemagglutinin of a virulent avian influenza A virus. Journal of General Virology 1993; 74: 311–314
   PubMed Web of Science ®Google Scholar
• Weber T., Paesold G., Mischler R., Semenza G., Brunner J. Evidence for H+-induced insertion of the influenza hemagglutinin HA2 N-terminal segment into the viral membrane. Journal of Biological Chemistry 1994; 269: 18353–18358
   PubMed Web of Science ®Google Scholar
• Weis W. I., Cusack S. C., Brown J. H., Daniels R. S., Skehel J. J., Wiley D. C. The structure of a membrane fusion mutant of the influenza virus haemagglutinin. EMBO Journal 1990; 9: 17–24
   PubMed Web of Science ®Google Scholar
• Weissenhorn W., Dessen A., Harrison S. C., Skehel J. J., Wiley D. C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 1997; 387: 426–430
   PubMed Web of Science ®Google Scholar
• Wharton S. A., Calder L. J., Ruigrok R. W. H., Skehel J. J., Steinhauer D. A., Wiley D. C. Electron microscopy of antibody complexes of influenza virus haemagglutinin in the fusion pH conformation. EMBO Journal 1995; 14: 240–246
   PubMed Web of Science ®Google Scholar
• Wharton S. A., Martin S. R., Ruigrok R. W. H., Skehel J. J., Wiley D. C. Membrane fusion by peptide analogues of influenza virus haemagglutinin. Journal of General Virology 1988; 69: 1847–1857
   PubMed Web of Science ®Google Scholar
• Wharton S. A., Weis W., Skehel J. J., Wiley D. C. Structure, Function, and Antigenicity of the Hemagglutinin of Influenza Virus. The Influenza Viruses, R. M. Krug. Plenum Press. 1989; 153–173
   Google Scholar
• White J. M. Iral and cellular membrane fusion proteins. Annual Review of Physiology 1990; 52: 675–697
   PubMed Web of Science ®Google Scholar
• White J. M. Membrane Fusion. Science 1992; 258: 917–924
   PubMed Web of Science ®Google Scholar
• White J. M. Fusion of influenza virus in endosomes: role of the hemagglutinin. Cellular Receptors for Animal Viruses, E. Wimmer. Cold Spring Harbor Press, New York 1994; 281–301
   Google Scholar
• White J., Kielian M., Helenius A. Membrane fusion proteins of enveloped animal viruses. Quarterly Review of Biophysics 1983; 16: 151–195
   PubMed Web of Science ®Google Scholar
• White J. M., Wilson I. A. Antipeptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. Journal of Cell Biology 1987; 105: 2887–2896
   PubMed Web of Science ®Google Scholar
• Whitt M. A., Zagouras P., Crise B., Rose J. K. A fusion-defective mutant of the vesicular stomatitis virus glycoprotein. Journal of Virology 1990; 64: 4907–4913
   PubMed Web of Science ®Google Scholar
• Wild C., Dubay J. W., Greenwell T., Baird T., Jr., Oas T. G., McDanal C., Hunter E., Matthews T. Propensity for a leucine zipper-like domain of human immunodeficiency virus type 1 gp41 to form oligomers correlates with a role in virus-induced fusion rather than assembly of the glycoprotein complex. Proceedings of the National Academy of Sciences 1994; 91: 12676–12680
   PubMed Web of Science ®Google Scholar
• Wiley D. C., Skehel J. J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annual Review of Biochemistry 1987; 56: 365–394
   PubMed Web of Science ®Google Scholar
• Wilschut J., Bron R. The influenza virus hemagglutinin: membrane fusion activity in intact virions and reconstructed virosomes. Viral Fusion Mechanisms, J. Bentz. CRC Press, Boca Raton, Ann Arbor, London & Tokyo 1993; 133–161
   Google Scholar
• Wilson I. A., Skehel J. J., Wiley D. C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 angstroms resolution. Nature 1981; 289: 366–373
   PubMed Web of Science ®Google Scholar
• Yu Y. G., King D. S., Shin Y.-K. Insertion of a coiled-coil peptide from influenza virus hemagglutinin into membranes. Science 1994; 266: 274–276
   PubMed Web of Science ®Google Scholar
• Zhang L., Ghosh H. P. Characterization of the putative fusogenic domain in vesicular stomatitis virus glycoprotein G. Journal of Virology 1994; 68: 2186–2193
   PubMed Web of Science ®Google Scholar
• Zimmerberg J., Blumenthal R., Sarkar D. P., Curran M., Morris S. J. Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. Journal of Cell Biology 1994; 127: 1885–1894
   PubMed Web of Science ®Google Scholar
• Zimmerberg J., Curran M., Cohen F. S. A lipid/protein complex hypothesis for exocytotic fusion pore formation. Annals of the New York Academy of Sciences 1991; 635: 307–317
   PubMed Web of Science ®Google Scholar
• Zimmerberg J., Vogel S. S., Chernomordik L. V. Mechanisms of membrane fusion. Annual Review of Biophysics and Biomolecular Structure 1993; 22: 433–466
   PubMedGoogle Scholar