Advertisement

The Journal of Membrane Biology

, Volume 199, Issue 1, pp 1–14 | Cite as

The Energetics of Membrane Fusion from Binding, through Hemifusion, Pore Formation, and Pore Enlargement

  • F.S. CohenEmail author
  • G.B. Melikyan
Topical Review

Abstract

The main steps of viral membrane fusion are local membrane approach, hemifusion, pore formation, and pore enlargement. Experiments and theoretical analyses have helped determine the relative energies required for each step. Key protein structures and conformational changes of the fusion process have been identified. The physical deformations of monolayer bending and lipid tilt have been applied to the steps of membrane fusion. Experiment and theory converge to strongly indicate that, contrary to former conceptions, the fusion process is progressively more energetically difficult: hemifusion has a relatively low energy barrier, pore formation is more energy-consuming, and pore enlargement is the most difficult to achieve.

Keywords

Viral fusion proteins Six-helix bundle Trimeric hairpin Lipid splay Lipid tilt 

Notes

Acknowledgments

We thank Drs. Leonid Chernomordik, Yuri Chizmadzhev, Michael Kozlov, Peter Kuzmin, and Joshua Zimmerberg for discussions over many years on the theory of membrane mechanics and its application to membrane fusion. This work was supported by National Institutes of Health grants GM-27367 and GM-54787.

References

  1. 1.
    Abrahamyan, L.G., Markosyan, R.M., Moore, F.S., Cohen, J.P., Melikyan, G.B. 2003Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusionJ. Virol7758295836CrossRefPubMedGoogle Scholar
  2. 2.
    Armstrong, R.T., Kushnir, A.S., White, J.M. 2000The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transitionJ. Cell Biol151425438CrossRefPubMedGoogle Scholar
  3. 3.
    Barnett, A.L., Davey, R.A., Cunningham, J.M. 2001Modular organization of the Friend murine leukemia virus envelope protein underlies the mechanism of infectionProc. Natl. Acad. Sci. USA9841134118CrossRefPubMedGoogle Scholar
  4. 4.
    Bentz, J., Mittal, A. 2003Architecture of the influenza hemagglutinin membrane fusion siteBiochim. Biophys. Acta16142435PubMedGoogle Scholar
  5. 5.
    Borrego-Diaz, E., Peeples, M.E., Markosyan, R.M., Melikyan, G.B., Cohen, F.S. 2003Completion of trimeric hairpin formation of influenza virus hemagglutinin promotes fusion pore opening and enlargementVirology316234244CrossRefPubMedGoogle Scholar
  6. 6.
    Bressanelli, S., Stiasny, K., Allison, S.L., Stura, E.A., Duquerroy, S., Lescar, J., Heinz, F.X., Rey, F.A. 2004Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformationEMBO J.23728738CrossRefPubMedGoogle Scholar
  7. 7.
    Bullough, P.A., Hughson, F.M., Skehel, J.J., Wiley, D.C. 1994Structure of influenza haemagglutinin at the pH of membrane fusionNature3713743CrossRefPubMedGoogle Scholar
  8. 8.
    Cao, J., Bergeron, L., Helseth, E., Thali, M., Repke, H., Sodoroski, J. 1993Effects of amino acid changes in the extracellular domain of the human immunodeficiency virus type 1 gp41 envelope glycoproteinJ. Virol6727472755PubMedGoogle Scholar
  9. 9.
    Carr, C.M., Kim, P.S. 1993A spring-loaded mechanism for the conformational change of influenza hemagglutininCell73823832CrossRefPubMedGoogle Scholar
  10. 10.
    Chanturiya, A., Chernomordik, L.V., Zimmerberg, J. 1997Flickering fusion pores comparable with initial exocytotic pores occur in protein-free phospholipid bilayersProc. Natl. Acad. Sci USA941442314428CrossRefPubMedGoogle Scholar
  11. 11.
    Chen, C.H., Matthews, T.J., McDanal, C.B., Bolognesi, M.L., Greenberg, D.P. 1995A molecular clasp in the human immunodeficiency virus (HIV) type 1 TM protein determines the anti-HIV activity of gp41 derivatives: implication for viral fusionJ. Virol6937713777PubMedGoogle Scholar
  12. 12.
    Chen, J., Lee, K.H., Steinhauer, D.A., Stevens, D.J., Skehel, J.J., Wiley, D.C. 1998Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformationCell95409417CrossRefPubMedGoogle Scholar
  13. 13.
    Chen, J., Skehel, J.J., Wiley, D.C. 1999N- and C-terminal residues combine in the fusion-pH influenza hemagglutinin HA(2) subunit to form an N cap that terminates the triple- stranded coiled coilProc. Natl. Acad. Sci. USA9689678972CrossRefPubMedGoogle Scholar
  14. 14.
    Chen, J., Wharton, S.A., Weisshborn, W., Calder, L.J., Hughson, F.M., Skehel, J.J., Wiley, D.C. 1995A soluble domain of the membrane-anchoring chain of influenza virus hemagglutinin (HA2) folds in Escherichia coli into the low-pH-induced conformationProc. Natl. Acad. Sci. USA921220512209PubMedGoogle Scholar
  15. 15.
    Chernomordik, L., KozIov, M.M., Zimmerberg, J. 1995Lipids in biological membrane fusionJ. Membrane Biol146l14CrossRefGoogle Scholar
  16. 16.
    Chernomordik, L.V., Frolov, V.A., Leikina, E., Bronk, P., Zimmerberg, J. 1998The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formationJ.Cell Biol14013691382CrossRefPubMedGoogle Scholar
  17. 17.
    Chernomordik, L.V., KozIov, M.M. 2003Protein-lipid interplay in fusion and fission of biological membranesAnnu Rev Biochem72175207CrossRefPubMedGoogle Scholar
  18. 18.
    Chernomordik, L.V., Melikyan, G.B., Abidor, I.G., Markin, V.S., Chizmadzhev, Y.A. 1985The shape of lipid molecules and monolayer membrane fusionBiochim. Biophys Acta.812643655Google Scholar
  19. 19.
    Chernomordik, L.V., Sukharev, S.I., Popov, S.V., Pastushenko, V.F., Sokirko, A.V., Abidor, I.G., Chizmadzhev, Y.A. 1987The electrical breakdown of cell and lipid membranes: the similarity of phenomenologiesBiochim. Biophys. Acta902360373PubMedGoogle Scholar
  20. 20.
    Chizmadzhev, Y.A., Cohen, F.S., Shcherbakov, A., Zimmerberg, J. 1995Membrane mechanics can account for fusion pore dilation in stagesBiophys. J.6924892500PubMedGoogle Scholar
  21. 21.
    Chizmadzhev, Y.A., Kuzmin, P.I., Kumenko, D.A., Zimmerberg, J., Cohen, F.S. 2000Dynamics of fusion pores connecting membranes of different tensionsBiophys. J.7822412256PubMedGoogle Scholar
  22. 22.
    Cleverley, D.Z., Lenard, J. 1998The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G proteinProc. Natl. Acad. Sci. USA9534253430CrossRefPubMedGoogle Scholar
  23. 23.
    Cohen, F.S., Markosyan, R.M., Melikyan, G.B. 2002The process of membrane fusion: nipples, hemifusion, pores, and pore growthCurr. Top. Membranes52501529Google Scholar
  24. 24.
    Cohen, F.S., Melikyan, G.B. 1998Methodologies in the study of cell-cell fusionMethods16215226CrossRefPubMedGoogle Scholar
  25. 25.
    Colman, P.M., Lawrence, M.C. 2003The structural biology of type I viral membrane fusionNat. Rev. Mol. Cell Biol4309319CrossRefPubMedGoogle Scholar
  26. 26.
    Cross, K.J., Wharton, S.A., Skehel, J.J., Wiley, D.C., Steinhauer, D.A. 2001Studies on influenza haemagglutinin fusion peptide mutants generated by reverse geneticsEMBO J.2044324442CrossRefPubMedGoogle Scholar
  27. 27.
    Dubay, J.W., Roberts, S.J., Brody, B., Hunter, E. 1992Mutations in the leucine zipper of the human immunodeficiency virus type 1 transmembrane glycoprotein affect fusion and infectivityJ. Virol6647484756PubMedGoogle Scholar
  28. 28.
    Durell, S.R., Martin, I., Ruysschaert, M., Shai, Y., Blumenthal, R. 1997What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion (review)Mol. Membr. Biol.1497112PubMedGoogle Scholar
  29. 29.
    Epand, R.F., Macosko, J.C., Russel, C.J., Shin, Y.K., Epand, R.M. 1999The ectodomain of HA2 of influenza virus promotes rapid pH dependent membrane fusionJ. Mol. Biol.286489503CrossRefPubMedGoogle Scholar
  30. 30.
    Epand, R.M., Epand, R.F. 2002Thermal denaturation of influenza virus and its relationship to membrane fusionBiochem. J.365841848PubMedGoogle Scholar
  31. 31.
    Frolov, V., Cho, M., Reese, T.S., Zimmerberg, J. 2000Both hemifusion and fusion pores are induced by GPI-linked influenza hemagglutininTraffic1622630CrossRefPubMedGoogle Scholar
  32. 32.
    Fuller, N., Rand, R.P. 2001The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranesBiophys. J.81243254PubMedGoogle Scholar
  33. 33.
    Gibbons, D.L., Erk, I., Reilly, B., Navaza, J., Kielian, M., Rey, F., Lepault, J. 2003Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallographyCell114573583CrossRefPubMedGoogle Scholar
  34. 34.
    Gibbons, D.L., Vaney, M.C., Roussel, A., Vigouroux, A., Reilly, B., Lepault, J., Kielian, M., Rey, F.A. 2004Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virusNature427320325CrossRefPubMedGoogle Scholar
  35. 35.
    Hamm, H., Kozlov, M. 2000Elastic energy of tilt and bending of fluid membranesEur. Phys. J.3323335Google Scholar
  36. 36.
    Hamm, M., Kozlov, M. 1998Tilt model of inverted amphipathic mesophasesEur. Phys. J.B6519528Google Scholar
  37. 37.
    Han, X., Bushweller, J.H., Cafiso, D.S., Tamm, L.K. 2001Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutininNature Strurt. Biol.8715720CrossRefGoogle Scholar
  38. 38.
    Harter, C., James, P., Bachi, T., Semenza, G., Brunner, J. 1989Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the “fusion peptide”J. Biol. Chem.26464596464PubMedGoogle Scholar
  39. 39.
    Helm, C.A., Israelachvilli, J.N., McGuiggan, P.M. 1992Role of hydrophobic forces in bilayer adhesion and fusionBiochemistry3117941805CrossRefPubMedGoogle Scholar
  40. 40.
    Hernandez, L.D., Hoffman, L.R., Wolfsberg, T.G., White, J.M. 1996Virus-cell and cell-cell fusionAnnu. Rev. Cell. Dev. Biol.12627661PubMedGoogle Scholar
  41. 41.
    Hu, C., Ahmed, M., Melia, T.J., Sollner, T.H., Mayer, T., Rothman, J.E. 2003Fusion of cells by flipped SNAREsScience30017451749CrossRefPubMedGoogle Scholar
  42. 42.
    Israelachvili, J., Pashley, R. 1982The hydrophobic interaction is long range, decaying exponentially with distanceNature300341342CrossRefPubMedGoogle Scholar
  43. 43.
    Jahn, R., Lang, T., Sudhof, T.C. 2003Membrane fusionCell112519533CrossRefPubMedGoogle Scholar
  44. 44.
    Jelesarov, I., Lu, M. 2001Thermodynamics of trimer-of-hairpins formation by the SIV gp41 envelope proteinJ. Mol. Biol.307637656CrossRefPubMedGoogle Scholar
  45. 45.
    Jin, H., Leser, G.P., Lamb, R.A. 1994The influenza virus hemagglutinin cytoplasmic tail is not essential for virus assembly or infectivityEMBO J.1355045515PubMedGoogle Scholar
  46. 46.
    Kemble, G., Danieli, T., White, J.M. 1994Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusionCell76383391CrossRefPubMedGoogle Scholar
  47. 47.
    Kemble, G.W., Henis, Y.I., White, J.M. 1993GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activityJ. Cell. Biol.12212531265CrossRefPubMedGoogle Scholar
  48. 48.
    Kobe, B., Center, R.J., Kemp, B.E., Poumbourios, P. 1999Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retroviral transmembrane proteinsProc. Natl. Acad. Sci. USA9643194324CrossRefPubMedGoogle Scholar
  49. 49.
    Kozlov, M.M., Markin, V.S. 1983Possible mechanism of membrane fusionBiofizika28255261Google Scholar
  50. 50.
    Kozlovsky, Y., Chernomordik, L.V., Kozlov, M.M. 2002Lipid intermediates in membrane fusion: formation, structure, and decay of hemifusion diaphragmBiophys. J.8326342651PubMedGoogle Scholar
  51. 51.
    Kozlovsky, Y., Kozlov, M.M. 2002Stalk model of membrane fusion: solution of energy crisisBiophys. J.82882895PubMedGoogle Scholar
  52. 52.
    Kuzmin, P.I., Zimmerberg, J., Chizmadzhev, Y.A., Cohen, F.S. 2001A quantitative model for membrane fusion based on low-energy intermediatesProc. Natl. Acad. Sci. USA9872357240CrossRefPubMedGoogle Scholar
  53. 53.
    Leckband, D., Israelachvili, J. 2001Intermolecular forces in biologyQ. Rev. Biophys.34105267PubMedGoogle Scholar
  54. 54.
    Lee, J., Lentz, B.R. 1997Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusionBiochemistry3662516259CrossRefPubMedGoogle Scholar
  55. 55.
    Leikin, S., Kozlov, M.M., Fuller, N.L., Rand, R.P. 1996Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranesBiophys. J.7126232632PubMedGoogle Scholar
  56. 56.
    Leikin, S., Parsegian, V.A., Rau, D.C, Rand, R.P 1993Hydration forcesAnnu. Rev. Phys. Chem.44369395CrossRefPubMedGoogle Scholar
  57. 57.
    Leikin, S.L., Kozlov, M.M., Chernomordik, L.V., Markin, V.S., Chizmadzhev, Y.A. 1987Membrane fusion: overcoming of the hydration barrier and local restructuringJ. Theor. Biol129411425PubMedGoogle Scholar
  58. 58.
    Leikina, E., LeDuc, D.L., Macosko, J.C., Epand, R., Shin, Y.K., Chernomordik, L.V. 2001The 1-127 HA2 construct of influenza virus hemagglutinin induces cell-cell hemifusionBiochemistry4083788386CrossRefPubMedGoogle Scholar
  59. 59.
    Li, Y., Han, X., Tamm, L.K. 2003Thermodynamics of fusion peptide-membrane interactionsBiochemistry4272457251CrossRefPubMedGoogle Scholar
  60. 60.
    Lin, X., Derdeyn, C.A., Bluementhal, R., West, J., Hunter, E. 2003Progressive truncations C terminal to the membrane-spanning domain of simian immunodeficiency virus Env reduce fusogenicity and increase concentration dependence of Env for fusionJ. Virol7770677077CrossRefPubMedGoogle Scholar
  61. 61.
    Lindau, M., Almers, W. 1995Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusionCurr. Opin. Cell. Biol.7509517CrossRefPubMedGoogle Scholar
  62. 62.
    Lu, M., Blacklow, S.C., Kim, P.S. 1995A trimeric structural domain of the HIV-1 transmembrane glycoproteinNat. Struct. Biol.210751082CrossRefPubMedGoogle Scholar
  63. 63.
    Lu, M., Ji, H., Shen, S. 1999Subdomain folding and biological activity of the core structure from human immunodeficiency virus type 1 gp41: implications for viral membrane fusionJ. Virol7344334438PubMedGoogle Scholar
  64. 64.
    Lu, M., Stoller, M.O., Wang, S., Liu, J., Fagan, M.B., Numberg, J.H. 2001Structural and functional analysis of interhelical interactions in the Human Immunodeficiency Virus type 1 gp41 envelope glycoprotein by alanine-scanning mutagenesisJ. Virol751114611156CrossRefPubMedGoogle Scholar
  65. 65.
    Markin, V.S., Albanesi, J.P. 2002Membrane fusion: stalk model revisitedBiophys. J.82693712PubMedGoogle Scholar
  66. 66.
    Markin, V.S., Kozlov, M.M., Borovjagin, V.L. 1984On the theory of membrane fusionThe stalk mechanism. Gen. Physiol. Biophys.3361377Google Scholar
  67. 67.
    Markosyan, R.M., Cohen, F.S., Melikyan, G.B. 2000The lipid-anchored ectodomain of influenza virus hemagglutinin (GPI-HA) is capable of inducing nonenlarging fusion poresMol. Biol.Cell1111431152PubMedGoogle Scholar
  68. 68.
    Markosyan, R.M., Cohen, F.S., Melikyan, G.B. 2003HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formationMol. Biol. Cell14926938CrossRefPubMedGoogle Scholar
  69. 69.
    Markosyan, R.M., Ma, X., Lu, M., Cohen, F.S., Melikyan, G.B. 2002The mechanism of inhibition of HIV-1 env-mediated cell-cell fusion by recombinant cores of gp41 ectodomainVirology302174184CrossRefPubMedGoogle Scholar
  70. 70.
    Markovic, I., Leikina, E., Zhukovsky, M., Zimmerberg, J., Chernomordik, L.V. 2001Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machinesJ. Cell. Biol.155833844CrossRefPubMedGoogle Scholar
  71. 71.
    May, S. 2002Structure and energy of fusion stalks: the role of membrane edgesBiophys. J.8329692980PubMedGoogle Scholar
  72. 72.
    Melikyan, G.B., Brener, S.A., Ok, D.C., Cohen, F.S. 1997Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusionJ. Cell. Biol.1369951005CrossRefPubMedGoogle Scholar
  73. 73.
    Melikyan, G.B., Jin, H., Lamb, R.A., Cohen, F.S. 1997The role of the cytoplasmic tail region of influenza virus hemagglutinin in formation and growth of fusion poresVirology235118128CrossRefPubMedGoogle Scholar
  74. 74.
    Melikyan, G.B., Lin, S., Roth, M.G., Cohen, F.S. 1999Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusionMol. Biol. Cell1018211836PubMedGoogle Scholar
  75. 75.
    Melikyan, G.B., Markosyan, R.M., Hemmati, H., Delmedico, M.K., Lambert, D.M, Cohen, F.S. 2000Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusionJ. Cell. Biol.151413424CrossRefPubMedGoogle Scholar
  76. 76.
    Melikyan, G.B., Markosyan, R.M., Roth, M.G., Cohen, F.S. 2000A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusionMol. Biol Cell1137653775PubMedGoogle Scholar
  77. 77.
    Melikyan, G.B., White, J.M., Cohen, F.S. 1995GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranesJ. Cell131679691CrossRefGoogle Scholar
  78. 78.
    Mittal, A., Leikina, E., Chernomordik, L.V., Bentz, J. 2003Kinetically differentiating influenza hemagglutinin fusion and hemifusion machinesBiophys J.8517131724PubMedGoogle Scholar
  79. 79.
    Modis, Y., Ogata, S., Clements, D., Harrison, S.C. 2004Structure of the dengue virus envelope protein after membrane fusionNature427313319CrossRefPubMedGoogle Scholar
  80. 80.
    Muller, M., Katsov, K., S chick, M. 2003A new mechanism of model membrane fusion determined from Monte Carlo simulationBiophys. J.8516111623PubMedGoogle Scholar
  81. 81.
    Munoz-Barroso, I., Durell, S., Sakaguchi, K., Appella, E., Blumenthal, R. 1998Dilation of the human immunodeficiency virus- 1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41J. Cell. Biol.140315323CrossRefPubMedGoogle Scholar
  82. 82.
    Munoz-Barroso, I., Salzwedel, K., Hunter, E., Blumenthal, R. 1999Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusionJ. Virol.7360896092PubMedGoogle Scholar
  83. 83.
    Neher, E. 1974Asymmetric membranes resulting from the fusion of two black lipid bilayersBiochim. Biophys. Acta.373327336PubMedGoogle Scholar
  84. 84.
    Noguchi, H., Takasu, M. 2001Fusion pathways of vesicles: A Brownian dynamics simulationJ. Chem. Phys.11595479551CrossRefGoogle Scholar
  85. 85.
    Nüssler, F., Clague, M.J., Herrmann, A. 1997Meta-stability of the hemifusion intermediate induced by glycosylphosphatidylinositol-anchored influenza hemagglutininBiophys. J.17322802291Google Scholar
  86. 86.
    Odell, D., Wanas, E., Yan, J., Ghosh, H.P. 1997Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein GJ. Virol.7179968000PubMedGoogle Scholar
  87. 87.
    Pak, C.C., Puri, A., Blumenthal, R. 1997Conformational changes and fusion activity of vesicular stomatitis virus glycoprotein: [125I] iodonaphthyl azide photolabeling studies in biological membranesBiochemistry3688908896CrossRefPubMedGoogle Scholar
  88. 88.
    Pantazatos, D.P., Pantazatos, S.P., MacDonald, R.C. 2003Bilayer mixing, fusion, and lysis following the interaction of populations of cationic and anionic phospholipid bilayer vesiclesJ. Membrane Biol.194129139CrossRefGoogle Scholar
  89. 89.
    Park, H.E., Gruenke, J.A., White, J.M. 2003Leash in the groove mechanism of membrane fusionNat. Struct. Biol.1010481053CrossRefPubMedGoogle Scholar
  90. 90.
    Parsegian, V.A., Rand, R.P., Gingell, D. 1984Lessons for the study of membrane fusion from membrane interactions in phospholipid systemsCiba Found. Symp.103927PubMedGoogle Scholar
  91. 91.
    Pecheur, E.I., Hoekstra, D., Sainte-Marie, J., Maurin, L., Bienvenue, A., Philippot, J.R. 1997Membrane anchorage brings about fusogenic properties in a short synthetic peptideBiochemistry3637733781CrossRefPubMedGoogle Scholar
  92. 92.
    Qiao, H., Armstrong, R.T., Melikyan, G.B., Cohen, F.S., White, J.M. 1999A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotypeMol. Biol. Cell1027592769PubMedGoogle Scholar
  93. 93.
    Rapaport, D., Shai, Y. 1994Interaction of fluorescently labeled analogues of the amino-terminal fusion peptide of Sendai virus with phospholipid membranesJ. Biol. Chem.2691512415131PubMedGoogle Scholar
  94. 94.
    Rawicz, W., Olbrich, K.C., McIntosh, T., Needham, D., Evans, E. 2000Effect of chain length and unsaturation on elasticity of lipid bilayersBiophys. J.79328339PubMedGoogle Scholar
  95. 95.
    Razinkov, V., Melikyan, G.B., Cohen, F.S. 1999Hemifusion between cells expressing hemagglutinin (HA) of influenza virus and planar membranes can precede the formation of fusion pores that subsequently fully enlargeBiophys. J.7731443151PubMedGoogle Scholar
  96. 96.
    Remeta, D.P., Krumbiegel, M., Minetti, C.A., Puri, A., Ginsburg, A., Blumenthal, R. 2002Acid-induced changes in thermal stability and fusion activity of influenza hemagglutininBiochemistry4120442054CrossRefPubMedGoogle Scholar
  97. 97.
    Russell, C.J., Jardetzky, T.S., Lamb, R.A. 2001Membrane fusion machines of paramyxoviruses: capture of intermediates of fusionEMBO J.2040244034CrossRefPubMedGoogle Scholar
  98. 98.
    Sackett, K., Shai, Y. 2003How structure correlates to function for membrane associated HIV-1 gp41 constructs corresponding to the N-terminal half of the ectodomainJ. Mol. Biol.3334758CrossRefPubMedGoogle Scholar
  99. 99.
    Schoch, C., Blumenthal, R. 1993Role of the fusion peptide sequence in initial stages of influenza hemagglutinin-induced cell fusionJ. Biol. Chem.26892679274PubMedGoogle Scholar
  100. 100.
    Sheetz, M.P., Singer, S.J. 1974Biological membranes as bilayer couplesA molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA7144574461Google Scholar
  101. 101.
    Siegel, D.P. 1993Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanismsBiophys. J.6521242140PubMedGoogle Scholar
  102. 102.
    Siegel, D.P. 1999The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusionBiophys. J.76291313PubMedGoogle Scholar
  103. 103.
    Skehel, J.J., Wiley, D.C. 1998Coiled coils in both intracellular vesicle and viral membrane fusionCell95871874CrossRefPubMedGoogle Scholar
  104. 104.
    Stegmann, T., Delfino, J.M., Richards, F.M., Helenius, A. 1991The HA2 subunit of influenza hemagglutinin inserts into the target membrane prior to fusionJ. Biol.Chem.2661840418410PubMedGoogle Scholar
  105. 105.
    Stegmann, T., Doms, R.W. 1989Protein-mediated membrane fusionAnnu, Rev. Biophys. Biophys. Chem.18187211Google Scholar
  106. 106.
    Szule, J.A., Fuller, N.L., Rand, R.P. 2002The effects of acyl chain length and saturation of diacylglycerols and phosphatidylcholines on membrane monolayer curvatureBiophys. J.83977984PubMedGoogle Scholar
  107. 107.
    Tatulian, S.A., Hinterdorfer, P., Baber, G., Tamm, L.K. 1995Influenza hemagglutinin assumes a tilted conformation during membrane fusion as determined by attenuated total reflection FTIR spectroscopyEMBO J.1455145523PubMedGoogle Scholar
  108. 108.
    Taylor, G.M., Sanders, D.A. 1999The role of the membrane-spanning domain sequence in glycoprotein-mediated membrane fusionMol. Biol. Cell1028032815PubMedGoogle Scholar
  109. 109.
    Tse, F.W., Iwata, A., Almers, W. 1993Membrane flux through the pore formed by a fusogenic viral envelope protein during cell fusionJ. Cell Biol.121543552CrossRefPubMedGoogle Scholar
  110. 110.
    Weng, Y., Yang, Z., Weiss, C.D. 2000Structure- function studies of the self-assembly domain of the human immunodeficiency virus type 1 transmembrane protein gp41J. Virol.7453685372CrossRefPubMedGoogle Scholar
  111. 111.
    White, J.M., Wilson, I.A. 1987Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutininJ. Cell. Biol.10528872896CrossRefPubMedGoogle Scholar
  112. 112.
    Wild, C.T., Shugars, D.C., Greenwell, T.K., McDanal, C.B., Matthews, T.J. 1994Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infectionProc. Natl. Acad. Sci. USA9197709774PubMedGoogle Scholar
  113. 113.
    Wilk, T., Pfeiffer, T., Bukovsky, A., Moldenhauer, G., Bosch, V. 1996Glycoprotein incorporation and HIV-1 infectivity despite exchange of the gp160 membrane-spanning domainVirology218269274CrossRefPubMedGoogle Scholar
  114. 114.
    Wilson, I.A., Skehel, J.J., Wiley, D.C. 1981Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolutionNature289366373CrossRefPubMedGoogle Scholar
  115. 115.
    Yang, L., Ding, L., Huang, H.W. 2003New phases of phospholipids and implications to the membrane fusion problemBiochemistry4266316635CrossRefPubMedGoogle Scholar
  116. 116.
    Yang, L., Huang, H.W. 2002Observation of a membrane fusion intermediate structureScience29718771879CrossRefPubMedGoogle Scholar
  117. 117.
    Zavorotinskaya, T., Qian, Z., Franks, J., Albritton, L.M. 2004A point mutation in the binding subunit of a retroviral envelope protein arrests virus entry at hemifusionJ. Virol.78473481CrossRefPubMedGoogle Scholar
  118. 118.
    Zimmerberg, J., Blumenthal, R., Sarkar, D.P., Curran, M., Morris, S.J. 1994Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusionJ. Cell. Biol.12718851894CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Molecular Biophysics and PhysiologyRush University Medical CenterChicagoUSA

Personalised recommendations