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Class II Fusion Proteins

  • Yorgo Modis
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 790)

Abstract

Enveloped viruses rely on fusion proteins in their envelope to fuse the viral membrane to the host-cell membrane. This key step in viral entry delivers the viral genome into the cytoplasm for replication. Although class II fusion proteins are genetically and structurally unrelated to class I fusion proteins, they use the same physical principles and topology as other fusion proteins to drive membrane fusion. Exposure of a fusion loop first allows it to insert into the host-cell membrane. Conserved hydrophobic residues in the fusion loop act as an anchor, which penetrates only partway into the outer bilayer leaflet of the host-cell membrane. Subsequent folding back of the fusion protein on itself directs the C-terminal viral transmembrane anchor towards the fusion loop. This fold-back forces the host-cell membrane (held by the fusion loop) and the viral membrane (held by the C-terminal transmembrane anchor) against each other, resulting in membrane fusion. In class II fusion proteins, the fold-back is triggered by the reduced pH of an endosome, and is accompanied by the assembly of fusion protein monomers into trimers. The fold-back occurs by domain rearrangement rather than by an extensive refolding of secondary structure, but this domain rearrangement and the assembly of monomers into trimers together bury a large surface area. The energy that is thus released exerts a bending force on the apposed viral and cellular membranes, causing them to bend towards each other and, eventually, to fuse.

Keywords

Fusion Protein West Nile Virus Dengue Virus Membrane Fusion Fusion Peptide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Lindenbach BD, Rice CM. Flaviviridae: The viruses and their replication. In: Knipe DM, Howley PM, eds. Fields Virology. 4th ed. Philadelphia: Lippincott Williams and Wilkins, 2001:991–1041.Google Scholar
  2. 2.
    Schlesinger S, Schlesinger MJ. Togaviridae: The viruses and their replication. In: Knipe DM, Howley PM, eds. Fields Virology. 4th ed. Philadelphia: Lippincott Williams and Wilkins, 2001:895–916.Google Scholar
  3. 3.
    Kuzmin PI, Zimmerberg J, Chizmadzhev YA et al. A quantitative model for membrane fusion based on low-energy intermediates. Proc Natl Acad Sci USA 2001; 98(13):7235–7240.PubMedCrossRefGoogle Scholar
  4. 4.
    Kozlov MM, Chernomordik LV. A mechanism of protein-mediated fusion: Coupling between refolding of the influenza hemagglutinin and lipid rearrangements. Biophys J 1998; 75(3): 1384–1396.PubMedCrossRefGoogle Scholar
  5. 5.
    Baker KA, Dutch RE, Lamb RA et al. Structural basis for paramyxovirus-mediated membrane fusion. Mol Cell 1999;3(3):309–319.PubMedCrossRefGoogle Scholar
  6. 6.
    Melikyan GB, Markosyan RM, Hemmati H et al. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J Cell Biol 2000; 151(2):413–423.PubMedCrossRefGoogle Scholar
  7. 7.
    Russell CJ, Jardetzky TS, Lamb RA. Membrane fusion machines of paramyxoviruses: Capture of intermediates of fusion. EMBO J 2001; 20(15):4024–4034.PubMedCrossRefGoogle Scholar
  8. 8.
    Skehel JJ, Wiley DC. Receptor binding and membrane fusion in virus entry: The influenza hemagglutinin. Annu Rev Biochem 2000; 69:531–569.PubMedCrossRefGoogle Scholar
  9. 9.
    Wilson IA, Skehel JJ, Wiley DC. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 1981; 289(5796):366–373.PubMedCrossRefGoogle Scholar
  10. 10.
    Rey FA, Heinz FX, Mandl C et al. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 1995; 375(6529):291–298.PubMedCrossRefGoogle Scholar
  11. 11.
    Rosenthal PB, Zhang X, Formanowski F et al. Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 1998; 396(6706):92–96.PubMedCrossRefGoogle Scholar
  12. 12.
    Lescar J, Roussel A, Wien MW et al. The Fusion glycoprotein shell of Semliki Forest virus: An icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 2001; 105(1): 137–148.PubMedCrossRefGoogle Scholar
  13. 13.
    Modis Y, Harrison SC. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci USA 2003; 100:6986–6991.PubMedCrossRefGoogle Scholar
  14. 14.
    Modis Y, Ogata S, Clements D et al. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J Virol 2005; 79(2):1223–1231.PubMedCrossRefGoogle Scholar
  15. 15.
    Yin HS, Wen X, Paterson RG et al. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 2006; 439(7072):38–44.PubMedCrossRefGoogle Scholar
  16. 16.
    Bullough PA, Hughson FM, Skehel JJ et al. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 1994; 371(6492):37–43.PubMedCrossRefGoogle Scholar
  17. 17.
    Fass D, Harrison SC, Kim PS. Retrovirus envelope domain at 1.7 angstrom resolution. Nat Struct Biol 1996; 3(5):465–469.PubMedCrossRefGoogle Scholar
  18. 18.
    Chan DC, Fass D, Berger JM et al. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997; 89(2):263–273.PubMedCrossRefGoogle Scholar
  19. 19.
    Tan K, Liu J, Wang J et al. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc Natl Acad Sci USA 1997; 94(23):12303–12308.PubMedCrossRefGoogle Scholar
  20. 20.
    Weissenhorn W, Dessen A, Harrison SC et al. Atomic structure of the ectodomain from HIV-1 gp41. Nature 1997; 387(6631):426–430.PubMedCrossRefGoogle Scholar
  21. 21.
    Malashkevich VN, Chan DC, Chutkowski CT et al. Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: Conserved helical interactions underlie the broad inhibitory activity of gp41 peptides. Proc Natl Acad Sci USA 1998; 95(16):9134–9139.PubMedCrossRefGoogle Scholar
  22. 22.
    Caffrey M, Cai M, Kaufman J et al. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J 1998; 17(16):4572–4584.PubMedCrossRefGoogle Scholar
  23. 23.
    Weissenhorn W, Carfi A, Lee KH et al. Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol Cell 1998; 2(5):605–616.PubMedCrossRefGoogle Scholar
  24. 24.
    Kobe B, Center RJ, Kemp BE et al. Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retro viral transmembrane proteins. Proc Natl Acad Sci USA 1999; 96(8):4319–4324.PubMedCrossRefGoogle Scholar
  25. 25.
    Chen J, Skehel JJ, Wiley DC. N-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 coil. Proc Natl Acad Sci USA 1999; 96(16):8967–8972.PubMedCrossRefGoogle Scholar
  26. 26.
    Zhao X, Singh M, Malashkevich VN et al. Structural characterization of the human respiratory syncytial virus fusion protein core. Proc Natl Acad Sci USA 2000; 97(26): 14172–14177.PubMedCrossRefGoogle Scholar
  27. 27.
    Xu Y, Lou Z, Liu Y et al. Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J Biol Chem 2004; 279(47):49414–49419.PubMedCrossRefGoogle Scholar
  28. 28.
    Xu Y, Liu Y, Lou Z et al. Structural basis for coronavirus-mediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J Biol Chem 2004; 279(29):30514–30522.PubMedCrossRefGoogle Scholar
  29. 29.
    Modis Y, Ogata S, Clements D et al. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004; 427(6972):313–319.PubMedCrossRefGoogle Scholar
  30. 30.
    Gething MJ, White JM, Waterfield MD. Purification of the fusion protein of Sendai virus: Analysis of the NH2-terminal sequence generated during precursor activation. Proc Natl Acad Sci USA 1978; 75(6):2737–2740.PubMedCrossRefGoogle Scholar
  31. 31.
    Gallaher WR. Detection of afusionpeptide sequence in the transmembrane protein of human immunodeficiency virus. Cell 1987; 50(3):327–328.PubMedCrossRefGoogle Scholar
  32. 32.
    Supekar VM, Bruckmann C, Ingallinella P et al. Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc Natl Acad Sci USA 2004; 101(52): 17958–17963.PubMedCrossRefGoogle Scholar
  33. 33.
    Cheng SF, Wu CW, Kantchev EA et al. Structure and membrane interaction of the internal fusion peptide of avian sarcoma leukosis virus. Eur J Biochem 2004; 271(23–24):4725–4736.PubMedCrossRefGoogle Scholar
  34. 34.
    Allison SL, Schalich J, Stiasny K et al. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J Virol 2001; 75(9):4268–4275.PubMedCrossRefGoogle Scholar
  35. 35.
    Zhang Y, Zhang W, Ogata S et al. Conformational changes of the flavivirus E glycoprotein. Structure (Camb) 2004; 12(9):1607–1618.CrossRefGoogle Scholar
  36. 36.
    Chen Y, Maguire T, Hileman RE et al. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 1997; 3(8):866–871.PubMedCrossRefGoogle Scholar
  37. 37.
    Navarro-Sanchez E, Altmeyer R, Amara A et al. Dendritic-cell-specific ICAM3-grabbing nonintegrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 2003; 4(7 Suppl): 1–6.Google Scholar
  38. 38.
    Tassaneetrithep B, Burgess TH, Granelli-Piperno A et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 2003; 197(7): 823–829.PubMedCrossRefGoogle Scholar
  39. 39.
    Crill WD, Roehrig JT. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J Virol 2001; 75(16):7769–7773.PubMedCrossRefGoogle Scholar
  40. 40.
    Hung JJ, Hsieh MT, Young MJ et al. An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells. J Virol 2004; 78(l):378–388.PubMedCrossRefGoogle Scholar
  41. 41.
    Thepparit C, Smith DR. Serotype-specific entry of dengue virus into liver cells: Identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol 2004; 78(22):12647–12656.PubMedCrossRefGoogle Scholar
  42. 42.
    Chu JJ, Ng ML. Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J Biol Chem 2004; 279(52):54533–54541.PubMedCrossRefGoogle Scholar
  43. 43.
    Allison SL, Stiasny K, Stadler K et al. Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein E. J Virol 1999; 73(7):5605–5612.PubMedGoogle Scholar
  44. 44.
    Stadler K, Allison SL, Schalich J et al. Proteolytic activation of tick-borne encephalitis virus by furin. J Virol 1997; 71(11):8475–8481.PubMedGoogle Scholar
  45. 45.
    Zhang Y, Corver J, Chipman PR et al. Structures of immature flavivirus particles. EMBO J 2003; 22(11):2604–2613.PubMedCrossRefGoogle Scholar
  46. 46.
    Ferlenghi I, Gowen B, de Haas F et al. The first step: Activation of the Semliki Forest virus spike protein precursor causes a localized conformational change in the trimeric spike. J Mol Biol 1998; 283(1):71–81.PubMedCrossRefGoogle Scholar
  47. 47.
    Kuhn RJ, Zhang W, Rossmann MG et al. Structure of dengue virus: Implications for flavivirus organization, maturation, and fusion. Cell 2002; 108(5):717–725.PubMedCrossRefGoogle Scholar
  48. 48.
    Zhang W, Chipman PR, Corver J et al. Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat Struct Biol 2003; 10(11):907–912.PubMedCrossRefGoogle Scholar
  49. 49.
    Mukhopadhyay S, Kim BS, Chipman PR et al. Structure of West Nile virus. Science 2003; 302(5643):248.PubMedCrossRefGoogle Scholar
  50. 50.
    Mancini EJ, Clarke M, Gowen BE et al. Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus. Mol Cell 2000; 5(2):255–266.PubMedCrossRefGoogle Scholar
  51. 51.
    Zhang W, Mukhopadhyay S, Pletnev SV et al. Placement of the structural proteins in Sindbis virus. J Virol 2002;76(22):11645–11658.PubMedCrossRefGoogle Scholar
  52. 52.
    Elshuber S, Allison SL, Heinz FX et al. Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J Gen Virol 2003; 84(Pt 1):183–191.PubMedCrossRefGoogle Scholar
  53. 53.
    Guirakhoo F, Heinz FX, Mandl CW et al. Fusion activity of flaviviruses: Comparison of mature and immature (prM-containing) tick-borne encephalitis virions. J Gen Virol 1991; 72(Pt 6): 1323–1329.PubMedCrossRefGoogle Scholar
  54. 54.
    Guirakhoo F, Bolin RA, Roehrig JT. The Murray Valley encephalitis virus prM protein confers acid resistance to virus particles and alters the expression of epitopes within the R2 domain of E glycoprotein. Virology 1992; 191(2):921–931.PubMedCrossRefGoogle Scholar
  55. 55.
    Gibbons DL, Vaney MC, Roussel A et al. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 2004; 427(6972):320–325.PubMedCrossRefGoogle Scholar
  56. 56.
    Bressanelli S, Stiasny K, Allison SL et al. Structure of aflavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J 2004; 23(4):728–738.PubMedCrossRefGoogle Scholar
  57. 57.
    Cecilia D, Gould EA. Nucleotide changes responsible for loss of neuroinvasiveness in Japanese encephalitis virus neutralization-resistant mutants. Virology 1991; 181(l):70–77.PubMedCrossRefGoogle Scholar
  58. 58.
    Hasegawa H, Yoshida M, Shiosaka T et al. Mutations in the envelope protein of Japanese encephalitis virus affect entry into cultured cells and virulence in mice. Virology 1992; 191(1):158–165.PubMedCrossRefGoogle Scholar
  59. 59.
    Lee E, Weir RC, Dalgarno L. Changes in the dengue virus major envelope protein on passaging and their localization on the three-dimensional structure of the protein. Virology 1997; 232(2):281–290.PubMedCrossRefGoogle Scholar
  60. 60.
    Beasley DW, Aaskov JG. Epitopes on the dengue 1 virus envelope protein recognized by neutralizing IgM monoclonal antibodies. Virology 2001; 279(2):447–458.PubMedCrossRefGoogle Scholar
  61. 61.
    Hurrelbrink RJ, McMinn PC. Attenuation of Murray Valley encephalitis virus by site-directed mutagenesis of the hinge and putative receptor-bindingregions of the envelope protein. J Virol 2001; 75(16):7692–7702.PubMedCrossRefGoogle Scholar
  62. 62.
    Monath TP, Arroyo J, Levenbook I et al. Single mutation in the flavivirus envelope protein hinge region increases neurovirulence for mice and monkeys but decreases viscerotropism for monkeys: Relevance to development and safety testing of live, attenuated vaccines. J Virol 2002; 76(4): 1932–1943.PubMedCrossRefGoogle Scholar
  63. 63.
    Dubovskii PV, Li H, Takahashi S et al. Structure of an analog of fusion peptide from hemagglutinin. Protein Sci 2000; 9(4):786–798.PubMedCrossRefGoogle Scholar
  64. 64.
    Han X, Bushweller JH, Cafiso DS et al. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat Struct Biol 2001; 8(8):715–720.PubMedCrossRefGoogle Scholar
  65. 65.
    Tamm LK, Han X, Li Y et al. Structure and function of membrane fusion peptides. Biopolymers 2002; 66(4):249–260.PubMedCrossRefGoogle Scholar
  66. 66.
    Ruigrok RW, Aitken A, Calder LJ et al. Studies on the structure of the influenza virus haemagglutinin at the pH of membrane fusion. J Gen Virol 1988; 69(Pt 11):2785–2795.PubMedCrossRefGoogle Scholar
  67. 67.
    Stiasny K, Allison SL, Schalich J et al. Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J Virol 2002; 76(8):3784–3790.PubMedCrossRefGoogle Scholar
  68. 68.
    Chan DC, Kim PS. HIV entry and its inhibition. Cell 1998; 93(5):681–684.PubMedCrossRefGoogle Scholar
  69. 69.
    Danieli T, Pelletier SL, Henis YI et al. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J Cell Biol 1996; 133(3):559–569.PubMedCrossRefGoogle Scholar
  70. 70.
    Blumenthal R, Sarkar DP, Durell S et al. Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J Cell Biol 1996; 135(1):63–71.PubMedCrossRefGoogle Scholar
  71. 71.
    Razinkov VI, Melikyan GB, Cohen FS. Hemifusion between cells expressing hemagglutinin of influenza virus and planar membranes can precede the formation of fusion pores that subsequently fully enlarge. Biophys J 1999; 77(6):3144–3151.PubMedCrossRefGoogle Scholar
  72. 72.
    Kemble GW, Danieli T, White JM. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 1994; 76(2):383–391.PubMedCrossRefGoogle Scholar
  73. 73.
    Melikyan GB, White JM, Cohen FS. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J Cell Biol 1995; 131(3):679–691.PubMedCrossRefGoogle Scholar
  74. 74.
    Nussler F, Clague MJ, Herrmann A. Meta-stability of the hemifusion intermediate induced by glycosylphosphatidylinositol-anchored influenza hemagglutinin. Biophys J 1997; 73(5):2280–2291.PubMedCrossRefGoogle Scholar
  75. 75.
    Armstrong RT, Kushnir AS, White JM. The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J Cell Biol 2000; 151(2):425–437.PubMedCrossRefGoogle Scholar
  76. 76.
    Saifee O, Wei L, Nonet ML. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol Biol Cell 1998; 9(6):1235–1252.PubMedCrossRefGoogle Scholar
  77. 77.
    McNew JA, Weber T, Parlati F et al. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J Cell Biol 2000; 150(1): 105–117.PubMedCrossRefGoogle Scholar
  78. 78.
    West JT, Johnston PB, Dubay SR et al. Mutations within the putative membrane-spanning domain of the simian immunodeficiency virus transmembrane glycoprotein define the minimal requirements for fusion, incorporation, and infectivity. J Virol 2001; 75(20):9601–9612.PubMedCrossRefGoogle Scholar
  79. 79.
    Dutch RE, Lamb RA. Deletion of the cytoplasmic tail of the fusion protein of the paramyxovirus simian virus 5 affects fusion pore enlargement. J Virol 2001; 75(11):5363–5369.PubMedCrossRefGoogle Scholar
  80. 80.
    Melikyan GB, Markosyan RM, Brener SA et al. Role of the cytoplasmic tail of ecotropic moloney murine leukemia virus Env protein in fusion pore formation. J Virol 2000; 74(l):447–455.PubMedCrossRefGoogle Scholar
  81. 81.
    Melikyan GB, Jin H, Lamb RA et al. The role of the cytoplasmic tail region of influenza virus hemagglutinin information and growth of fusion pores. Virology 1997; 235(1):118–128.PubMedCrossRefGoogle Scholar
  82. 82.
    Bagai S, Lamb RA. Truncation of the COOH-terminal region of the paramyxovirus SV5 fusion protein leads to hemifusion but not complete fusion. J Cell Biol 1996; 135(1):73–84.PubMedCrossRefGoogle Scholar
  83. 83.
    Januszeski MM, Cannon PM, Chen D et al. Functional analysis of the cytoplasmic tail of Moloney murine leukemia virus envelope protein. J Virol 1997; 71(5):3613–3619.PubMedGoogle Scholar
  84. 84.
    Nieva JL, Bron R, Corver J et al. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J 1994; 13(12):2797–2804.PubMedGoogle Scholar
  85. 85.
    Vashishtha M, Phalen T, Marquardt MT et al. A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J Cell Biol 1998; 140(1):91–99.PubMedCrossRefGoogle Scholar
  86. 86.
    Chanel-Vos C, Kielian M. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J Virol 2004; 78(24): 13543–13552.PubMedCrossRefGoogle Scholar
  87. 87.
    Chatterjee PK, Eng CH, Kielian M. Novel mutations that control the sphingolipid and cholesterol dependence of the Semliki Forest virus fusion protein. J Virol 2002; 76(24):12712–12722.PubMedCrossRefGoogle Scholar
  88. 88.
    Stiasny K, Koessl C, Heinz FX. Involvement of lipids in different steps of the flavivirus fusion mechanism. J Virol 2003; 77(14):7856–7862.PubMedCrossRefGoogle Scholar
  89. 89.
    Burke DS, Monath TP. Flaviviruses. In: Knipe DM, Howley PM, eds. Fields Virology. 4th ed. Philadelphia: Lippincott Williams and Wilkins, 2001:1043–1125.Google Scholar
  90. 90.
    Smith TJ, Kremer MJ, Luo M et al. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science 1986; 233(4770): 1286–1293.PubMedCrossRefGoogle Scholar
  91. 91.
    Baldwin CE, Sanders RW, Berkhout B. Inhibiting HIV-1 entry with fusion inhibitors. Curr Med Chem 2003; 10(17):1633–1642.PubMedCrossRefGoogle Scholar
  92. 92.
    Kilby JM, Hopkins S, Venetta TM et al. Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. Nat Med 1998; 4(11):1302–1307.PubMedCrossRefGoogle Scholar
  93. 93.
    Kanai R, Kar K, Anthony K et al. Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. J Virol 2006; 80(22): 11000–11008.PubMedCrossRefGoogle Scholar
  94. 94.
    Nayak V, Dessau M, Kucera K et al. Crystal structure of dengue virus type 1 envelope protein in the postfusion conformation and its implications for membrane fusion. J Virol 2009; 83(9):4338–4344.PubMedCrossRefGoogle Scholar
  95. 95.
    Voss JE, Vaney MC, Duquerroy S et al. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 2010; 468(7324):709–712.PubMedCrossRefGoogle Scholar
  96. 96.
    Li L, Jose J, Xiang Y et al. Structural changes of envelope proteins during alphavirus fusion. Nature 2010; 468(7324):705–708.PubMedCrossRefGoogle Scholar
  97. 97.
    Cockburn JJ, Navarro Sanchez ME et al. Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus. EMBO J 2011; 31(3):767–779.PubMedCrossRefGoogle Scholar
  98. 98.
    Luca VC, AbiMansour J, Nelson CA, Fremont DH. Crystal structure of the Japanese encephalitis virus envelope protein. J Virol 2012; 86(4):2337–2346.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2013

Authors and Affiliations

  • Yorgo Modis
    • 1
  1. 1.Department of Molecular Biophysics and BiochemistryYale UniversityNew HavenUSA

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