Reversibility in Fusion Protein Conformational Changes The Intriguing Case of Rhabdovirus-Induced Membrane Fusion

  • Yves Gaudin
Part of the Subcellular Biochemistry book series (SCBI, volume 34)


Influenza Virus Membrane Fusion Rabies Virus Vesicular Stomatitis Virus Fusion Peptide 
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  1. Allison, S. L., Schalich, J., Stiasny, K., Mandl, C. W., Kunz, C., and Heinz, F. X., 1995, Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J. Virol. 69:695–700.Google Scholar
  2. Anderson, R. W. G., and Orci, L., 1988, A view of acidic intracellular compartment. J. Cell Biol. 106:539–543.Google Scholar
  3. Bagai Joshi, S., Dutch, R. E., and Lamb, R. A. (1998) A core trimer of the paramyxovirus fusion protein: parallels to influenza virus hemagglutinin and HIV-1 gp41. Virology 248:20–34.Google Scholar
  4. Balch, W. E., Elliott, M. M., and Keller, D. S., 1986, ATP-coupled transport of vesicular stomatitis virus G protein between the endoplasmic reticulum and the Golgi. J. Biol. Chem., 261:14681–14689.Google Scholar
  5. Benmansour, A., Leblois, H., Coulon, P., Tuffereau, C., Gaudin, Y., Flamand, A., and Lafay, F., 1991, Antigenicity of rabies virus glycoprotein. J. Virol., 65:4198–4203.Google Scholar
  6. Bizebard, T., Gigant, B., Rigolet, B., Rasmussen, B., Diat, O., Bosecke, P., Wharton, S.A., Skehel, J. J., and Knossow, M., 1995, Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 376:92–94.Google Scholar
  7. Blumenthal, R., Sarkar, D. P., Durell, S., Howard, D. E., and Morris, S. J., 1996, Dilation of the influenza hemagglutinin pore revealed by the kinetics of individual cell-cell fusion events. J. Cell Biol. l35:63–71.Google Scholar
  8. Brunner, J., 1989, Photochemical labeling of the apolar phase of membranes. Meth. in Enzymol. 172:628–687.Google Scholar
  9. Brunner, J., 1993, New photolabeling and crosslinking methods. Annual Review of Biochmistry 62:483–514.Google Scholar
  10. Buckland, R., Malvoisin, E., Beauverger, P., and Wild, F., 1992, A leucine zipper structure present in the measles virus fusion protein is not required for its tetramerization but is essential for fusion. J. Gen. Virol., 73:1703–1707.Google Scholar
  11. Bullough, P. A., Hughson, F. M., Skehel, J. J., add Wiley, D. C., 1994, Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43.Google Scholar
  12. Bundo-Morita, K., Gibson, S., and Lenard, J., 1988, Radiation inactivation analysis of fusion and hemolysis by vesicular stomatitis virus Virology 163:622–424.Google Scholar
  13. Carr, C. M., Chaudhry, C., and Kim, P. S., 1997, Influenza hemagglutinin is spring-loaded by a metastable native conformation. P N R SUSA 94:14306–14313.Google Scholar
  14. Carr, C. M., and Kim, P. S., 1993, A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823–832.Google Scholar
  15. Chan, D. C., Fass, D., Berger, J. M., and Kim, P. S., 1997, Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263–273.Google Scholar
  16. Chambers, P., Pringle, C. R., and Easton, A. J., 1990, Heptad repeat sequences are located adjacent to hydrophobic regions in several types of virus fusion glycoproteins J. Gen. Virol. 71:3075–3080.Google Scholar
  17. Chen, J., Ho Lee, K., Steinhauer, D. A., Stevens, D. J., Skehel, J. J., and Wiley, D. C., 1998, Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95:409–417.Google Scholar
  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.Google Scholar
  19. Chernomordik, L., Kozlov, M. M., and Zimmerberg, J., 1995, Lipids in biological membrane fusion. J. Memb. Biol. 146:1–14.Google Scholar
  20. Chernomordik, L.V., Leikina, E., Frolov, V., Bronk, P., and Zimmerberg, J., 1997, An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136:81–93.Google Scholar
  21. Clague, M. J., Schoch, C., Zech, L., and Blumenthal, R., 1990, Gating kinetics of pH-activated membrane fusion of vesicular stomatitis virus with cells: stopped-flow measurements by dequenching of octadecylrhodamine fluorescence. Biochemistry 29:1303–1308.Google Scholar
  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. PN.A.S. USA 95:3425–3430.Google Scholar
  23. Coulon, P, Ternaux, J. P., Flamand, A., and Tuffereau, C., 1998, An avirulent mutant of rabies virus is unable to infect motoneurons in vivo and in vitro. J. Virol. 72:273–278.Google Scholar
  24. Crimmins, D. L., Mehard, W. B., and Schlesinger, S., 1983, Physical properties of a soluble form of the glycoprotein of vesicular stomatitis virus at neutral and acidic pH. Biochemistry 22:5790–5796.Google Scholar
  25. Danieli, T., Pelletier, S. L., Henis, Y. I., and White, J. M., 1996, Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell Biol. 133:559–569.Google Scholar
  26. Daniels, R. S., Downie, J. C., Hay, A. J., Knossow, M., Skehel, J. J., Wang, M. L., and Wiley, D. C., 1985, Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40:431–439.Google Scholar
  27. Dietzschold, B., Gore, M., Marchadier, D., Niu, H. S., Bunschoten, H. S., Otvos, L. Jr., Wunner, W. H., Ertl, H. C. J., Osterhaus, A. D. M. E., and Koprowski, H., 1990, Structural and immunological characterization of a linear neutralizing epitope of the rabies virus glycoprotein and its possible use in a synthetic vaccine. J. Virol. 64:3804–3809.Google Scholar
  28. Dietzschold, B., Wiktor, T. J., Macfarlan, R., and Vanichio, A., 1982, Antigenic structure of rabies virus glycoprotein: ordering and immunological characterization of the large CNBr cleavage fragments. J. Virol. 44:595–602.Google Scholar
  29. Doms, R. W., Helenius, A. H., and White, J. M., 1985, Membrane fusion activity of the influenza virus hemagglutinin: the lowpH-induced conformational change. J.Biol.Chem. 260: 2973–2981.Google Scholar
  30. Doms, R. W., Keller, D. S., Helenius, A., and Balch, W., 1987, Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J. Cell Biol. 105:1957–1969.Google Scholar
  31. Durell, S. R., Martin, I., Ruysschaert, J. M., Shai, Y., and Blumenthal, R., 1997, What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion (review). Mol. Membr. Biol. 14:97–112.Google Scholar
  32. Durrer, P., Gaudin, Y., Ruigrok, R. W. H., Graf, R., and Brunner, J., 1995, Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. J. Biol. Chem. 270:17575–17581.Google Scholar
  33. Fass, D., Harrison, S. C., and Kim, P. S., 1996, Retrovirus envelope domain at 1.7Å resolution. Nat. struct. Biol. 3:465–469.Google Scholar
  34. Florkiewicz, R. Z., and Rose, J. K., 1984, A cell line expressing vesicular stomatitis virus glycoprotein fuses at low pH. Science 225:721–723.Google Scholar
  35. Fredericksen, B. L., and Whitt, M. A., 1995, Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity. J. Virol. 69:1435–1443.Google Scholar
  36. Fredericksen, B. L., and Whitt, M. A., 1996, Mutations at two conserved amino acids in the glycoprotein of vesicular stomatitis virus affect pH-dependent conformational changes and reduce the pH threshold for membrane fusion. Virology 217:49–57.Google Scholar
  37. Fredericksen, B. L., and Whitt, M. A., 1998, Attenuation of recombinant vesicular stomatitis viruses encoding mutant glycoproteins demonstrate a critical role for maintaining a high pH threshold for membrane fusion in viral fitness. Virology 240:349–358.Google Scholar
  38. 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. Stuct. Biol. 5:276–279.Google Scholar
  39. Gastka, M. J., Horvath, J., and Lentz, T. L., 1996, Rabies virus binding to the nicotinic acetylcholine receptor a subunit demonstrated by the virus overlay protein binding assay. J. Gen. Virol. 77:2437–2440.Google Scholar
  40. Gaudin, Y., 1997, Folding of rabies virus glycoprotein: epitope acquisition and interaction with endoplasmic reticulum chaperones. J. Virol. 71:3742–3750.Google Scholar
  41. Gaudin, Y., De Kinkelin, P., and Benmansour, A., 1999a, Mutations in the glycoprotein of viral hemorrhagic septicemia virus that affect virulence for fish and the pH threshold for membrane fusion. J. Gen. Virol. in press.Google Scholar
  42. Gaudin, Y., Moreira, S., Bénèjean, J., Blondel, D., Flamand, A., and Tuffereau, C., 1999b, Soluble ectodomain of rabies virus glycoprotein expressed in eucaryotic cells folds in a monomeric conformation which is antigenically distinct from the native state of the complete membrane-anchored glycoprotein. J. Gen. Virol. in press.Google Scholar
  43. Gaudin, Y., Raux, H., Flamand, A., and Ruigrok, R. W. H., 1996, Identification of amino acids controlling the low-pH-induced conformational change of rabies virus glycoprotein. J. Virol. 70:7371–7378.Google Scholar
  44. Gaudin, Y., Ruigrok, R. W. H., and Brunner, J., 1995a, Low-pH induced conformational changes in viral fusion proteins: implications for the fusion mechanism. J.Gen. Virol. 76:1541–1556.Google Scholar
  45. Gaudin, Y., Ruigrok, R. W. H., Knossow, M., and Flamand, A., 1993, Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion. J. Virol. 67:1365–1372.Google Scholar
  46. Gaudin, Y., Ruigrok, R. W. H., Tuffereau, C., Knossow, M., and Flamand, A., 1992, Rabies virus glycoprotein is a trimer. Virology 187:627–632.Google Scholar
  47. Gaudin, Y., Tuffereau, C., Durrer, P., Flamand, A., and Ruigrok, R. W. H., 1995b, Biological function of the low-pH, fusion-inactive conformation of rabies virus glycoprotein (G): G is transported in a fusion-inactive state-like conformation. J. Virol. 69:5528–5534.Google Scholar
  48. Gaudin, Y., Tuffereau, C., Segretain, D., Knossow, M., and Flamand, A., 1991, Reversible conformational changes and fusion activity of rabies virus glycoprotein. J. Virol. 65:4852–4859.Google Scholar
  49. Halonen, P. E., Toivanen, P., and Nikkari, T., 1974, Non-specific serum inhibitors of activity of haemagglutinins of rabies and vesicular stomatitis viruses. J. Gen. Virol. 22:309–318.Google Scholar
  50. Hanson, P. I., Roth, R., Morisaki, H., Jahn, R., and Heuser, J. E., 1997, Structure and conformational changes in NSF and its membranereceptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90:523–535.Google Scholar
  51. Heinz, F. X., Stiasny, K., Püschner-Auer, G., Holzmann, H., Allison, S. L., Mandl, C. W., and Kunz, C., 1994, Structural changes and functional control of the Tick-Borne encephalitis virus glycoprotein E by the heterodimeric association with protein prM. Virology 198: 109–117.Google Scholar
  52. Herrmann, A., Clague, M. J., Puri, A., Morris, S. J., Blumenthal, R., and Grimaldi, S., 1990, Effect of erythrocyte transbilayer phospholipid distribution on fusion with vesicular stomatitis virus. Biochemistry 29:4054–4058.Google Scholar
  53. Justman, J., Klimjack, M.R., and Kielian, M.,1993, Role of spikeprotein conformational changes in fusion of Semliki forest virus. J. Virol. 67:7597–7607.Google Scholar
  54. Kemble, G. W., Danieli, T., and White, J. M., 1994, Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76:383–391.Google Scholar
  55. Kenney, J. M., Sjöberg, M., Garoff, H., and Fuller, S. D., 1994, Visualization of fusion activation in the Semliki Forest virus spike. Structure 2:823–832.Google Scholar
  56. Korte, T., and Herrmann, A., 1994, pH-dependent binding of the fluorophore bis-ANS to influenza virus reflects the conformational changeof hemagglutinin. Eur. Biophysics J. 23:105–113.Google Scholar
  57. Korte, T., Ludwig, K., Krumbiegel, M., Zirwer, D., Damaschun, G., and Herrmann, A., 1997, Transient changes of the conformation of hemagglutinin of influenza virus at low pH detected by time-resolved circular dichroism spectroscopy. J. Biol. Chem. 272:9764–9770.Google Scholar
  58. Kraulis, P. E., 1991, MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:924–950.Google Scholar
  59. Kreis, T. E., and Lodish, H. F., 1986, Oligomerization is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell 46:929–937.Google Scholar
  60. Krumbiegel, M., Herrmann, A., and Blumenthal, R., 1994, Kinetics of the low pH-induced conformational changes and fusogenic activity of influenza hemagglutinin. Biophys. J. 67: 2355–2360.Google Scholar
  61. Kuwert, E., Wiktor, T. J., Sokol, F., and Koprowski, H., 1968, Hemagglutination by rabies virus. J. Virol. 2:1381–1392.Google Scholar
  62. Lafay, F., Benmansour, A., Chebli, K., and Flamand, A., 1996, Immunodominant epitopes defined by a yeast-expressed library of random fragments of the rabies virus glycoprotein map outside major antigenic sites. J. Gen. Virol. 77:339–346.Google Scholar
  63. Lafon, M., Wiktor, T. J., and Macfarlan, R. I., 1983, Antigenic sites of the CVS rabies virus glycoprotein: analysis with monoclonal antibodies. J. Gen. Virol. 64:843–851.Google Scholar
  64. Lee, J. K., and Lentz, B. R., 1998, Secretory and viral fusion may share mechanistics events with fusion between curved lipid bilayers. P.NA.S. USA 95:9274–9279.Google Scholar
  65. Lentz, T. L., Burrage, T. G., Smith, A. L., Crick, J., and Tignor, G. H., 1982, Is the acetylcholine receptor a rabies receptor? Science 215:182–184.Google Scholar
  66. Lentz, T. L., Wilson, P. T., Hawrot, E., and Speicher, D. W., 1984, Amino acid sequence similarity between rabies virus glycoprotein and snake venom curaremimetic neurotoxins. Science 226:2347–848.Google Scholar
  67. Li, Y., Drone, C., Sat, E., and Ghosh, H. P., 1993, Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains. J. Virol. 67:4070–4077.Google Scholar
  68. Lobigs, M., and Garoff, H., 1990, Fusion function of the Semliki Forest virus spike is activated by proteolytic cleavage of the envelope glycoprotein precursor p62. J. Virol. 64:1233–1240.Google Scholar
  69. Lu, M., Blacklow, S. C., and Kim, P. S., 1995, A trimeric structural domain of the HIV-1 trans-membrane glycoprotein. Nat. Struct. Biol. 2:1075–1082.Google Scholar
  70. 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.Google Scholar
  71. Lyles, D. S., Varela, V. A., and Parce, J. W., 1990, Dynamic Nature of the quaternary structure of the vesicular stomatitis virus envelope glycoprotein. Biochemistry 29:2442–2449.Google Scholar
  72. 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.Google Scholar
  73. 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.Google Scholar
  74. Mebatsion, T., König, M., and Conzelmann, K. K., 1996, Budding of rabies virus particles in the absence of the spike glycoprotein. Cell 84:941–951.Google Scholar
  75. Metsikkö, K., Van Meer, G., and Simons, K., 1986, Reconstitution of the fusogenic activity of vesicular stomatitis virus. EMBO J. 5:3429–3435.Google Scholar
  76. Mifune, K., Ohuchi, M., and Mannen, K., 1982, Hemolysis and cell fusion by rhabdoviruses. FEBS Lett. 137:293–297.Google Scholar
  77. Nicholson, K. L., Munson, M., Miller, R. B., Filip, T. J., Fairman, R., and Hughson, F. M., 1998, Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p. Nat. Struct. Biol. 5:793–802.Google Scholar
  78. Odell, D., Wanas, E., Yan, J., and Ghosh, H. P., 1997, Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein G. J. Virol. 71:7996–8000.Google Scholar
  79. Ohnishi, S., 1988, Fusion of viral envelopes with cellular membranes. Curr. Top. Memb. Tramp. 32:257–296.Google Scholar
  80. Pak, C. C., Puri, A., and Blumenthal, R., 1997, Conformational changes and fusion activity of vesicular stomatitis virus glycoprotein: [1251]iodonaphtyl azide photolabeling studies in biological membranes. Biochemistry 36:8890–8896.Google Scholar
  81. Plonsky, I., and Zimmerberg, J., 1996, The initial fusion pore induced by baculovirus GP64 is large and forms quickly. J. Cell Biol. 135:1831–1839.Google Scholar
  82. Préhaud, C., Coulon, P., Lafay, F., Thiers, C., and Flamand, A., 1988, Antigenic site II of the rabies virus glycoprotein: structure and role in viral virulence. J. Virol. 62:l-7.Google Scholar
  83. Puri, A., Booy, F. P., Doms, R. W., White, J. M., and Blumenthal, R., 1990, Conformational changes and fusion activity of influenza virus hemagglutinin of the H2 and H3 subtypes: effects of acid pretreatment. J. Virol 64:3824–3832.Google Scholar
  84. Puri, A., Grimaldi, S., and Blumenthal, R., 1992, Role of viral envelope sialic acid in membrane fusion mediated by the vesicular stomatitis virus envelope glycoproteins. Biochemistry 31:10108–10113.Google Scholar
  85. Puri, A., Winick, J., Lowry, R. J., Covell, D., Eidelman, O., Walter, A., and Blumenthal, R., 1988, Activation of vesicular stomatitis virus fusion with cells by pretreatment at low pH. J. Biol. Chem 263:4749–4753.Google Scholar
  86. Qiao, H., Pelletier, S. L., Hoffman, L., Hacker, J., Armstrong, R. T., and White, J. M., 1998, Specific single or double proline substitutions in the “spring-loaded” coiled-coil region of the influenza hemagglutinin impair or abolish membrane fusion activity. J. Cell Biol. 141:1335–1347.Google Scholar
  87. Ramalho-Santos, J., Nir, S., Duzgunes, N., Pato de Carvalho, A,, and Pedroso de Lima, M. C., 1993, A common mechanism for influenza virus fusion activity and inactivation. Biochemistry 32:2771–2779.Google Scholar
  88. Ramsdale, E. E., Kingsman, S. M., and Kingsman, A. J., 1996, The “putative” leucine zipper region of murine leukemia virus transmembrane protein (P15e) is essential for viral infectivity. Virology 220:100–108.Google Scholar
  89. Rand, R. P., 1981, Interacting phospholipid bilayers: measured forces and induced structural changes. Ann. Rev. of Biophys. Bioeng. 10:277–314.Google Scholar
  90. Raux, H., Coulon, P., Lafay, F., and Flamand, A,, 1995, Monoclonal antibodies which recognize the acidic configuration of the rabies glycoprotein at the surface of the virion can be neutralizing. Virology 210:400–408.Google Scholar
  91. Reitter, J. N., Sergel, T., and Morrison, T. G., 1995, Mutational analysis of the leucine zipper motif in the Newcastle disease virus fusion protein. J. Virol. 69:5995–6004.Google Scholar
  92. Rey, F. A., Heinz, F. X., Mandl, C., Kunz, C., and Harrison, S. C., 1995, The envelope glycoprotein from tick-borne encephalitis virus at 2Å resolution. Nature 375:291–298.Google Scholar
  93. Riedel, H. C., Kondor-Koch, C., and Garoff, H., 1984, Cell surface expression of fusogenic vesicular stomatitis virus G protein from cloned cDNA. EMBO J. 3:1477–1483.Google Scholar
  94. Ruigrok, R. W. H., Martin, S. R., Wharton, S. A., Skehel, J. J., Bayley, P. M., and Wiley, D. C., 1986, Conformational changes in the hemagglutinin of influenza virus which accompany heat-induced fusion of virus with liposomes. Virology 155:484–497.Google Scholar
  95. Salminen, A., Wahlberg, J. M., Lobigs, M., Liljeström, P., and Garoff, H., 1992, Membrane fusion process of Semliki forest virus II: cleavage-dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol. 116:349–457.Google Scholar
  96. Sauter, N. K., Bednarski, M. D., Wurzburg, B. A., Hanson, J. E., Whitesides, G. M., Skehel, J. J., and Wiley, D. C., 1989, Hemagglutinin from two influenza virus variants bind to sialic acid derivatives with millimolar dissociations constants: a 500-Mhz proton nuclear magnetic resonance study. Biochemistry 28:8388–8396.Google Scholar
  97. Schlegel, R., Tralka, M., Willingham, M. C., and Pastan, I., 1983, Inhibition of VSV binding and infectivity by phosphatidylserine: is phosphatidylserine a VSV-binding site? Cell 32:639–646.Google Scholar
  98. Seif, I., Coulon, P., Rollin, P. E., and Flamand, A., 1985, Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J. Virol, 53:926–934.Google Scholar
  99. Shokralla, S., He, Y., Wanas, E., and Ghosh, H. P., 1998, Mutations in a carboxy-terminal region of vesicular stomatitis virus glycoprotein G that affect membrane fusion activity. Virology 242:39–50.Google Scholar
  100. Siegel, D. P., 1993, Energetic of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophys. J. 65:2124–2140.Google Scholar
  101. Skehel, J. J., and Wiley, D. C., 1998, Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 95:871–874.Google Scholar
  102. Skehel, J. J., Bayley, P. M., Brown, E. B., Martin, S. R., Waterfield, M. D., White, J. M., Wilson, I. A., and Wiley, D. C., 1982, Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. P.N.A.S. USA 79:968–972.Google Scholar
  103. Stegmann, T., Booy, F. P., and Wilschut, J., 1987, Effects of low pH on influenza virus. J. Biol. Chem. 262:17744–17749.Google Scholar
  104. Stegmann, T., Delfino, J. M., Richards, F. M., and Helenius, A., 1991, The HA2 subunit of influenza hemagglutinin inserts into the target membrane prior to fusion. J. Biol. Chem. 266: 18404–18410.Google Scholar
  105. Stegmann, T., White, J. M., and Helenius, A., 1990, Intermediates in influenza induced membrane fusion. EMBO J. 9:4231–4241.Google Scholar
  106. Stiasny, K., Allison, S. L., Marchler-Bauer, A., Kunz, C., and Heinz, F. X., 1996, Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tickborne encephalitis virus. J. Virol. 70:8142–8147.Google Scholar
  107. Sugrue, R. J., Bahadur, G., Zambon, M. C., Hall-Smith, M., Douglas, A. R., and Hay, A., 1990, Specific structural alteration of the influenza hemagglutinin by amantadine. EMBO J. 9:3469–3476.Google Scholar
  108. Superti, F., Derer, M., and Tsiang, H., 1984a, Mechanism of rabies virus entry into CER cells. J. Gen. Virol. 65:781–789.Google Scholar
  109. Superti, E, Seganti, H., Tsiang, H., and Orci, N., 1984b, Role of phospholipids in rhabdovirus attachment to CER cells. Arch. Virol. 81:321–328.Google Scholar
  110. Superti, F., Hauttecoeur, B., Morelec, M. J., Goldoni, P., Bizzini, B., and Tsiang, H., 1986, Involvement of gangliosides in rabies virus infection. J. Gen. Virol. 67:47–56.Google Scholar
  111. Sutton, R. B., Fasshauer, D., Jahn, R., and Brünger, A. T., 1998, Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4Å resolution. Nature 395:347–353.Google Scholar
  112. Thoulouze, M. I., Lafage, M., Schachner, M., Hartmann, U., Cremer, H., and Lafon, M., 1998, The neural cell adhesion molecule is a receptor for rabies virus. J. Virol, 72:7181–7190.Google Scholar
  113. Tsurudome, M., Glück, R., Graf, R., Falchetto, R., Schaller, U., and Brunner, J., 1992, Lipid interactions of the hemagglutinin HA2 NH2-terminal segment during influenza virus-induced membrane fusion. J. Biol. Chem. 267:20225–20232Google Scholar
  114. Tuffereau, C., Bénèjean, J., Blondel, D., Kieffer, B., and Flamand, A,, 1998, Low-affinity nerve-growth factor receptor (P7SNTR) can serve as a receptor for rabies virus. EMBO J. 17:7250–7259.Google Scholar
  115. Tuffereau, C., Leblois, H., Bénèjean, J., Coulon, P., Lafay, F., and Flamand, A., 1989, Arginine or Lysine in position 333 of ERA and CVS glycoprotein is necessary for rabies virulence in adult mice. Virology 172:206–212.Google Scholar
  116. Wahlberg, J. M., Boere, W. A. M., and Garoff, R., 1989, The heterodimeric association between the membrane proteins of Semliki forest virus changes its sensitivity to low pH during virus maturation. J. Virol. 63:4991–4997.Google Scholar
  117. Wahlberg, J. M., Bron, R., Wilschut, J., and Garoff, H., 1992, Membrane fusion of Semliki forest virus involves homotrimers of the fusion protein. J. Virol. 66:7309–7318.Google Scholar
  118. Wahlberg, J. M., and Garoff, H., 1992, Membrane fusion process of Semliki forest virus: low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J. Cell Biol. 116:339–348.Google Scholar
  119. Weber, T., Paesold, G., Mischler, R., Semenza, G., and Brunner, J., 1994, Evidence for H+-induced insertion of the influenza hemagglutinin HA2 N-terminal segment into the viral membrane. J. Biol. Chem. 269:18353–18358.Google Scholar
  120. Webster, R. G., Brown, L. E., and Jackson, D. C., 1983, Changes in the antigenicity of the hemagglutinin molecule of H3 influenza virus at acidic pH. Virology 126:587–599.Google Scholar
  121. Weiss, W., Brown, J. H., Cusack, S., Paulson, J. C., Skehel, J. J., and Wiley, D. C., 1988, Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333:426–431.Google Scholar
  122. 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.Google Scholar
  123. Weissenhorn, W., Dessen, A., Harrison, S. C., Skehel, J. J., and Wiley, D. C., 1997, Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426–430.Google Scholar
  124. Wharton, S. A., Skehel, J. J., and Wiley, D. C., 1986, Studies of influenza haemagglutinin-mediated membrane fusion. Virology 149:27–35.Google Scholar
  125. Wharton, S. A., Calder, L. J., Ruigrok, R. W. H., Skehel, J. J., Steinhauer, D. A., and Wiley, D. C., 1995, Electron microscopy of antibody complexes of influenza virus haemagglutinin in the fusion pH conformation. EMBO J. 14:240–246.Google Scholar
  126. White, J., Math, K., and Helenius, A., 1981, Cell fusion by Semliki forest, Influenza and vesicular stomatitis virus. J. Cell Biol. 89:674–679.Google Scholar
  127. White, J. M., Kartenbeck, J., and Helenius, A., 1982, Membrane fusion activity of influenza virus. EMBO J. 1:217–222.Google Scholar
  128. White, J. M., and Wilson, I. A., 1987, Anti-peptide antibodies detect steps in a protein conformational change: low pH-activation of the influenza virus hemagglutinin. J. Cell Biol. 105:2887–2896.Google Scholar
  129. Whitt, M. A., Buonocore, L., Prehaud, C., and Rose, J. K., 1991, Membrane fusion activity, oligomerization, and assembly of the rabies virus glycoprotein. Virology 185:681–688.Google Scholar
  130. Wiktor, T.J., and Koprowski, H.,1980, Antigenic variants of rabies virus. J. Exp. Med. 152:99–112.Google Scholar
  131. Wilcox, M. D., McKenzie, M. O., Parce, J. W., and Lyles, D. S., 1992, Subunit interactions of vesicular stomatitis virus envelope glycoprotein influenced by detergent micelles and lipid bilayers. Biochemistry 31:10458–10464.Google Scholar
  132. Wiley, D. C., and Skehel, J. J., 1987, The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Ann. Rev. Bioch. 56:365–374.Google Scholar
  133. Wilson, I. A., Skehel, J. J., and Wiley, D. C., 1981, Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolution. Nature 289:366–373.Google Scholar
  134. Yamada, S., and Ohnishi, S., 1986, Vesicular stomatitis virus binds and fuses with phospholipid domain in target cell membranes. Biochemistry 25:3703–3708.Google Scholar
  135. Yao, Y., and Compans, R. W., 1996, Peptides corresponding to the heptad repeat sequence of human parainfluenza virus fusion protein are potent inhibitors of virus infection. Virology 223: 103–112.Google Scholar
  136. Yewdell, J. W., Gerhard, W., and Bächi, T., 1983, Monoclonal antihemagglutinin antibodies detect irreversible antigenic alterations that coincide with the acid activation of influenza virus A/PR/8/34-mediated hemolysis. J. Virol. 48:239–248.Google Scholar
  137. Zagouras, P., Ruusala, A., and Rose, J. K., 1991, Dissociation and reassociation of oligomeric viral glycoprotein subunits in the endoplasmic reticulum. J. Virol. 65:1976–1984.Google Scholar
  138. Zhang, L., and Ghosh, H. P., 1994, Characterization of the putative fusogenic domain in vesicular stomatitis virus glycoprotein G. J. Virol. 68:2186–2193.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Yves Gaudin
    • 1
  1. 1.Laboratoire de Génétique des virusCNRSGif sur Yvette CedexFrance

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