1932

Abstract

Enveloped viruses infect host cells by a membrane fusion reaction that takes place at the cell surface or in intracellular compartments following virus uptake. Fusion is mediated by the membrane interactions and conformational changes of specialized virus envelope proteins termed membrane fusion proteins. This article discusses the structures and refolding reactions of specific fusion proteins and the methods for their study and highlights outstanding questions in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085521
2014-09-29
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085521.html?itemId=/content/journals/10.1146/annurev-virology-031413-085521&mimeType=html&fmt=ahah

Literature Cited

  1. Harrison SC. 1.  2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15:690–98 [Google Scholar]
  2. White JM, Delos SE, Brecher M, Schornberg K. 2.  2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189–219 [Google Scholar]
  3. Plemper RK. 3.  2011. Cell entry of enveloped viruses. Curr. Opin. Virol. 1:92–100 [Google Scholar]
  4. Baquero E, Albertini AA, Vachette P, Lepault J, Bressanelli S, Gaudin Y. 4.  2013. Intermediate conformations during viral fusion glycoprotein structural transition. Curr. Opin. Virol. 3:143–50 [Google Scholar]
  5. Weissenhorn W, Hinz A, Gaudin Y. 5.  2007. Virus membrane fusion. FEBS Lett. 581:2150–55 [Google Scholar]
  6. Kielian M, Rey FA. 6.  2006. Virus membrane fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:67–76 [Google Scholar]
  7. Mercer J, Schelhaas M, Helenius A. 7.  2010. Virus entry by endocytosis. Annu. Rev. Biochem. 79:803–33 [Google Scholar]
  8. Marsh M, Bron R. 8.  1997. SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 110:95–103 [Google Scholar]
  9. Liao M, Kielian M. 9.  2005. Domain III from class II fusion proteins functions as a dominant-negative inhibitor of virus-membrane fusion. J. Cell Biol. 171:111–20 [Google Scholar]
  10. Marsh M, Helenius A. 10.  1989. Virus entry into animal cells. Adv. Virus Res. 36:107–51 [Google Scholar]
  11. Silverstein SC, Steinman RM, Cohn ZA. 11.  1977. Endocytosis. Annu. Rev. Biochem. 46:669–722 [Google Scholar]
  12. Sun E, He J, Zhuang X. 12.  2013. Live cell imaging of viral entry. Curr. Opin. Virol. 3:34–43 [Google Scholar]
  13. Rust MJ, Lakadamyali M, Zhang F, Zhuang X. 13.  2004. Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat. Struct. Mol. Biol. 11:567–73 [Google Scholar]
  14. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SPJ. 14.  2009. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 5:e1000394 [Google Scholar]
  15. van der Schaar HM, Rust MJ, Chen C, van der Ende-Metselaar H, Wilschut J. 15.  et al. 2008. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 4:e1000244 [Google Scholar]
  16. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. 16.  2009. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137:433–44 [Google Scholar]
  17. Mercer J, Helenius A. 17.  2008. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320:531–35 [Google Scholar]
  18. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W. 18.  2007. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 9:310–15 [Google Scholar]
  19. Zhong P, Agosto LM, Munro JB, Mothes W. 19.  2013. Cell-to-cell transmission of viruses. Curr. Opin. Virol. 3:44–50 [Google Scholar]
  20. Dale BM, Alvarez RA, Chen BK. 20.  2013. Mechanisms of enhanced HIV spread through T-cell virological synapses. Immunol. Rev. 251:113–24 [Google Scholar]
  21. Chernomordik LV, Kozlov MM. 21.  2008. Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15:675–83 [Google Scholar]
  22. Chernomordik LV, Kozlov MM. 22.  2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72:175–207 [Google Scholar]
  23. Rand RP, Parsegian VA. 23.  1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta 988:351–76 [Google Scholar]
  24. Wiley DC, Skehel JJ. 24.  1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365–94 [Google Scholar]
  25. McCune JM, Rabin LB, Feinberg MB, Lieberman M, Kosek JC. 25.  et al. 1988. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53:55–67 [Google Scholar]
  26. Heinz FX, Stiasny K, Puschner-Auer G, Holzmann H, Allison SL. 26.  et al. 1994. Structural changes and functional control of the tick-borne encephalitis virus glycoprotein E by the heterodimeric association with protein prM. Virology 198:109–17 [Google Scholar]
  27. Lorenz IC, Allison SL, Heinz FX, Helenius A. 27.  2002. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J. Virol. 76:5480–91 [Google Scholar]
  28. Melancon P, Garoff H. 28.  1986. Reinitiation of translocation in the Semliki Forest virus structural polyprotein: identification of the signal for the E1 glycoprotein. EMBO J. 5:1551–60 [Google Scholar]
  29. Andersson H, Barth BU, Ekström M, Garoff H. 29.  1997. Oligomerization-dependent folding of the membrane fusion protein of Semliki Forest virus. J. Virol. 71:9654–63 [Google Scholar]
  30. Carleton M, Lee H, Mulvey M, Brown DT. 30.  1997. Role of glycoprotein PE2 in formation and maturation of the Sindbis virus spike. J. Virol. 71:1558–66 [Google Scholar]
  31. Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM. 31.  2005. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643–45 [Google Scholar]
  32. Schornberg K, Matsuyama S, Kabsch K, Delos S, Bouton A, White J. 32.  2006. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J. Virol. 80:4174–78 [Google Scholar]
  33. Ruigrok RWH, Martin SR, Wharton SA, Skehel JJ, Bayley PM, Wiley DC. 33.  1986. Conformational changes in the hemagglutinin of influenza virus which accompany heat-induced fusion of virus with liposomes. Virology 155:484–97 [Google Scholar]
  34. Wharton SA, Skehel JJ, Wiley DC. 34.  1986. Studies of influenza haemagglutinin-mediated membrane fusion. Virology 149:27–35 [Google Scholar]
  35. Allison SL, Schalish J, Stiasny K, Mandl CW, Kunz C, Heinz FX. 35.  1995. Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J. Virol. 69:695–700 [Google Scholar]
  36. Stiasny K, Allison SL, Schalich J, Heinz FX. 36.  2002. Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J. Virol. 76:3784–90 [Google Scholar]
  37. Skehel JJ, Wiley DC. 37.  2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531–69 [Google Scholar]
  38. Kielian M, Klimjack MR, Ghosh S, Duffus WA. 38.  1996. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 134:863–72 [Google Scholar]
  39. Corver J, Bron R, Snippe H, Kraaijeveld C, Wilschut J. 39.  1997. Membrane fusion activity of Semliki Forest virus in a liposomal model system: specific inhibition by Zn2+ ions. Virology 238:14–21 [Google Scholar]
  40. Stiasny K, Kossl C, Lepault J, Rey FA, Heinz FX. 40.  2007. Characterization of a structural intermediate of flavivirus membrane fusion. PLoS Pathog. 3:e20 [Google Scholar]
  41. Kozlov MM, McMahon HT, Chernomordik LV. 41.  2010. Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35:699–706 [Google Scholar]
  42. Sánchez-San Martín C, Sosa H, Kielian M. 42.  2008. A stable prefusion intermediate of the alphavirus fusion protein reveals critical features of class II membrane fusion. Cell Host Microbe 4:600–8 [Google Scholar]
  43. Han X, Bushweller JH, Cafiso DS, Tamm LK. 43.  2001. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8:715–20 [Google Scholar]
  44. Buzon V, Natrajan G, Schibli D, Campelo F, Kozlov MM, Weissenhorn W. 44.  2010. Crystal structure of HIV-1 gp41 including both fusion peptide and membrane proximal external regions. PLoS Pathog. 6:e1000880 [Google Scholar]
  45. Chernomordik LV, Zimmerberg J, Kozlov MM. 45.  2006. Membranes of the world unite. ! J. Cell Biol. 175:201–7 [Google Scholar]
  46. Cohen FS, Melikyan GB. 46.  2004. The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199:1–14 [Google Scholar]
  47. Skehel JJ, Bayley PM, Brown EB, Martin SR, Waterfield MD. 47.  et al. 1982. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. USA 79:968–72 [Google Scholar]
  48. White JM, Wilson IA. 48.  1987. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza hemagglutinin. J. Cell Biol. 105:2887–96 [Google Scholar]
  49. Doms RW, Helenius A, White J. 49.  1985. Membrane fusion activity of the influenza virus hemagglutinin. J. Biol. Chem. 260:2973–81 [Google Scholar]
  50. Chernomordik LV, Leikina E, Frolov V, Bronk P, Zimmerberg J. 50.  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]
  51. Harter C, James P, Bachi T, Semenza G, Brunner J. 51.  1989. Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the “fusion peptide.”. J. Biol. Chem. 264:6459–64 [Google Scholar]
  52. Tsurudome M, Gluck R, Graf R, Falchetto R, Schaller U, Brunner J. 52.  1992. Lipid interactions of the hemagglutinin HA2 NH2-terminal segment during influenza virus-induced membrane fusion. J. Biol. Chem. 267:20225–32 [Google Scholar]
  53. Ahn A, Gibbons DL, Kielian M. 53.  2002. The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J. Virol. 76:3267–75 [Google Scholar]
  54. Kim YH, Donald JE, Grigoryan G, Leser GP, Fadeev AY. 54.  et al. 2011. Capture and imaging of a prehairpin fusion intermediate of the paramyxovirus PIV5. Proc. Natl. Acad. Sci. USA 108:20992–97 [Google Scholar]
  55. Cao S, Zhang W. 55.  2013. Characterization of an early-stage fusion intermediate of Sindbis virus using cryoelectron microscopy. Proc. Natl. Acad. Sci. USA 110:13362–67 [Google Scholar]
  56. Wild CT, Shugars DC, Greenwell TK, McDanal CB, Matthews TJ. 56.  1994. Peptides corresponding to a predictive α-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. USA 91:9770–74 [Google Scholar]
  57. Lambert DM, Barney S, Lambert AL, Guthrie K, Medinas R. 57.  et al. 1996. Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion. Proc. Natl. Acad. Sci. USA 93:2186–91 [Google Scholar]
  58. Melikyan GB, Markosyan RM, Hemmati H, Delmedico MK, Lambert DM, Cohen FS. 58.  2000. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J. Cell Biol. 151:413–23 [Google Scholar]
  59. Cohen FS, Melikyan GB. 59.  1998. Methodologies in the study of cell-cell fusion. Methods 16:215–26 [Google Scholar]
  60. Kemble GW, Danieli T, White JM. 60.  1994. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76:383–91 [Google Scholar]
  61. Floyd DL, Harrison SC, van Oijen AM. 61.  2009. Method for measurement of viral fusion kinetics at the single particle level. J. Vis. Exp. 7:e1484 [Google Scholar]
  62. Ivanovic T, Choi JL, Whelan SP, van Oijen AM, Harrison SC. 62.  2013. Influenza-virus membrane fusion by cooperative fold-back of stochastically induced hemagglutinin intermediates. eLife 2:e00333 [Google Scholar]
  63. Floyd DL, Ragains JR, Skehel JJ, Harrison SC, van Oijen AM. 63.  2008. Single-particle kinetics of influenza virus membrane fusion. Proc. Natl. Acad. Sci. USA 105:15382–87 [Google Scholar]
  64. Lescar J, Roussel A, Wien MW, Navaza J, Fuller SD. 64.  et al. 2001. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137–48 [Google Scholar]
  65. Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, Wiley DC. 65.  1998. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95:409–17 [Google Scholar]
  66. Wilson IA, Skehel JJ, Wiley DC. 66.  1981. Structure of the hemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289:366–78 [Google Scholar]
  67. Bullough PA, Hughson FM, Skehel JJ, Wiley DC. 67.  1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43 [Google Scholar]
  68. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS. 68.  2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38–44 [Google Scholar]
  69. Welch BD, Liu Y, Kors CA, Leser GP, Jardetzky TS, Lamb RA. 69.  2012. Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc. Natl. Acad. Sci. USA 109:16672–77 [Google Scholar]
  70. Baker KA, Dutch RE, Lamb RA, Jardetzky TS. 70.  1999. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3:309–19 [Google Scholar]
  71. Godley L, Pfeifer J, Steinhauer D, Ely B, Shaw G. 71.  et al. 1992. Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity. Cell 68:635–45 [Google Scholar]
  72. Thoennes S, Li ZN, Lee BJ, Langley WA, Skehel JJ. 72.  et al. 2008. Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology 370:403–14 [Google Scholar]
  73. Danieli T, Pelletier SL, Henis YI, White JM. 73.  1996. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell Biol. 133:559–69 [Google Scholar]
  74. Leikina E, Mittal A, Cho MS, Melikov K, Kozlov MM, Chernomordik LV. 74.  2004. Influenza hemagglutinins outside of the contact zone are necessary for fusion pore expansion. J. Biol. Chem. 279:26526–32 [Google Scholar]
  75. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC. 75.  1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375:291–98 [Google Scholar]
  76. Modis Y, Ogata S, Clements D, Harrison SC. 76.  2003. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 100:6986–91 [Google Scholar]
  77. Modis Y, Ogata S, Clements D, Harrison SC. 77.  2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313–19 [Google Scholar]
  78. Bressanelli S, Stiasny K, Allison SL, Stura EA, Duquerroy S. 78.  et al. 2004. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 23:728–38 [Google Scholar]
  79. DuBois RM, Vaney MC, Tortorici MA, Kurdi RA, Barba-Spaeth G. 79.  et al. 2013. Functional and evolutionary insight from the crystal structure of rubella virus protein E1. Nature 493:552–56 [Google Scholar]
  80. Dessau M, Modis Y. 80.  2013. Crystal structure of glycoprotein C from Rift Valley fever virus. Proc. Natl. Acad. Sci. USA 110:1696–701 [Google Scholar]
  81. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 81.  2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705–8 [Google Scholar]
  82. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C. 82.  et al. 2010. Glycoprotein organization of chikungunya virus particles revealed by X-ray crystallography. Nature 468:709–12 [Google Scholar]
  83. Roussel A, Lescar J, Vaney MC, Wengler G, Wengler G, Rey FA. 83.  2006. Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure 14:75–86 [Google Scholar]
  84. Gibbons DL, Vaney MC, Roussel A, Vigouroux A, Reilly B. 84.  et al. 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427:320–25 [Google Scholar]
  85. Kuhn RJ. 85.  2007. Togaviridae: the viruses and their replication. Fields Virology DM Knipe, PM Howley 1001–22 Philadelphia: Lippincott, Williams & Wilkins [Google Scholar]
  86. Sjoberg M, Lindqvist B, Garoff H. 86.  2011. Activation of the alphavirus spike protein is suppressed by bound E3. J. Virol. 85:5644–50 [Google Scholar]
  87. Salminen A, Wahlberg JM, Lobigs M, Liljeström P, Garoff H. 87.  1992. Membrane fusion process of Semliki Forest virus. II. Cleavage-dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol. 116:349–57 [Google Scholar]
  88. Li L, Lok SM, Yu IM, Zhang Y, Kuhn RJ. 88.  et al. 2008. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319:1830–34 [Google Scholar]
  89. Yu IM, Holdaway HA, Chipman PR, Kuhn RJ, Rossmann MG, Chen J. 89.  2009. Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. J. Virol. 83:12101–7 [Google Scholar]
  90. Yu IM, Zhang W, Holdaway HA, Li L, Kostyuchenko VA. 90.  et al. 2008. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319:1834–37 [Google Scholar]
  91. Vaney MC, Rey FA. 91.  2011. Class II enveloped viruses. Cell. Microbiol. 13:1451–59 [Google Scholar]
  92. Backovic M, Jardetzky TS. 92.  2009. Class III viral membrane fusion proteins. Curr. Opin. Struct. Biol. 19:189–96 [Google Scholar]
  93. Roche S, Bressanelli S, Rey FA, Gaudin Y. 93.  2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187–91 [Google Scholar]
  94. Roche S, Rey FA, Gaudin Y, Bressanelli S. 94.  2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315:843–48 [Google Scholar]
  95. Yagnik AT, Lahm A, Meola A, Roccasecca RM, Ercole BB. 95.  et al. 2000. A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40:355–66 [Google Scholar]
  96. Garry RF, Dash S. 96.  2003. Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 307:255–65 [Google Scholar]
  97. Kielian M. 97.  2006. Class II virus membrane fusion proteins. Virology 344:38–47 [Google Scholar]
  98. Krey T, d'Alayer J, Kikuti CM, Saulnier A, Damier-Piolle L. 98.  et al. 2010. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog. 6:e1000762 [Google Scholar]
  99. Omari K, Iourin O, Harlos K, Grimes JM, Stuart DI. 99.  El 2013. Structure of a pestivirus envelope glycoprotein E2 clarifies its role in cell entry. Cell Rep. 3:30–35 [Google Scholar]
  100. Li Y, Wang J, Kanai R, Modis Y. 100.  2013. Crystal structure of glycoprotein E2 from bovine viral diarrhea virus. Proc. Natl. Acad. Sci. USA 110:6805–10 [Google Scholar]
  101. Kong L, Giang E, Nieusma T, Kadam RU, Cogburn KE. 101.  et al. 2013. Hepatitis C virus E2 envelope glycoprotein core structure. Science 342:1090–94 [Google Scholar]
  102. Khan AG, Whidby J, Miller MT, Scarborough H, Zatorski AV. 102.  et al. 2014. Structure of the core ectodomains of the hepatitis C virus envelope glycoprotein 2. Nature 509381–84
  103. Boutilier J, Duncan R. 103.  2011. The reovirus fusion-associated small transmembrane (FAST) proteins: virus-encoded cellular fusogens. Curr. Top. Membr. 68:107–40 [Google Scholar]
  104. Moss B. 104.  2012. Poxvirus cell entry: How many proteins does it take?. Viruses 4:688–707 [Google Scholar]
  105. Kielian M, Chanel-Vos C, Liao M. 105.  2010. Alphavirus entry and membrane fusion. Viruses 2:796–825 [Google Scholar]
  106. Zaitseva E, Mittal A, Griffin DE, Chernomordik LV. 106.  2005. Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J. Cell Biol. 169:167–77 [Google Scholar]
  107. Mukhopadhyay S, Zhang W, Gabler S, Chipman PR, Strauss EG. 107.  et al. 2006. Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14:63–73 [Google Scholar]
  108. deCurtis I, Simons. 108.  1988. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl. Acad. Sci. USA 85:8052–56 [Google Scholar]
  109. Zhang X, Fugere M, Day R, Kielian M. 109.  2003. Furin processing and proteolytic activation of Semliki Forest virus. J. Virol. 77:2981–89 [Google Scholar]
  110. Uchime O, Fields W, Kielian M. 110.  2013. The role of E3 in pH protection during alphavirus assembly and exit. J. Virol. 87:10255–62 [Google Scholar]
  111. Fields W, Kielian M. 111.  2013. A key interaction between the alphavirus envelope proteins responsible for initial dimer dissociation during fusion. J. Virol. 87:3774–81 [Google Scholar]
  112. Meyer WJ, Johnston RE. 112.  1993. Structural rearrangement of infecting Sindbis virions at the cell surface: mapping of newly accessible epitopes. J. Virol. 67:5117–25 [Google Scholar]
  113. Vaney MC, Duquerroy S, Rey FA. 113.  2013. Alphavirus structure: activation for entry at the target cell surface. Curr. Opin. Virol. 3:151–58 [Google Scholar]
  114. Liu CY, Kielian M. 114.  2009. E1 mutants identify a critical region in the trimer interface of the Semliki Forest virus fusion protein. J. Virol. 83:11298–306 [Google Scholar]
  115. Umashankar M, Sánchez-San Martín C, Liao M, Reilly B, Guo A. 115.  et al. 2008. Differential cholesterol binding by class II fusion proteins determines membrane fusion properties. J. Virol. 82:9245–53 [Google Scholar]
  116. Liu CY, Besanceney C, Song Y, Kielian M. 116.  2010. Pseudorevertants of a Semliki Forest virus fusion-blocking mutation reveal a critical interchain interaction in the core trimer. J. Virol. 84:11624–33 [Google Scholar]
  117. Roman-Sosa G, Kielian M. 117.  2011. The interaction of alphavirus E1 protein with exogenous domain III defines stages in virus-membrane fusion. J. Virol. 85:12271–79 [Google Scholar]
  118. Zheng Y, Sánchez-San Martín C, Qin ZL, Kielian M. 118.  2011. The domain I–domain III linker plays an important role in the fusogenic conformational change of the alphavirus membrane fusion protein. J. Virol. 85:6334–42 [Google Scholar]
  119. Sánchez-San Martín C, Nanda S, Zheng Y, Fields W, Kielian M. 119.  2013. Cross-inhibition of chikungunya virus fusion and infection by alphavirus E1 domain III proteins. J. Virol. 87:7680–87 [Google Scholar]
  120. Gibbons DL, Erk I, Reilly B, Navaza J, Kielian M. 120.  et al. 2003. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell 114:573–83 [Google Scholar]
  121. Fuller SD, Berriman JA, Butcher SJ, Gowen BE. 121.  1995. Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell 81:715–25 [Google Scholar]
  122. Haag L, Garoff H, Xing L, Hammar L, Kan ST, Cheng RH. 122.  2002. Acid-induced movements in the glycoprotein shell of an alphavirus turn the spikes into membrane fusion mode. EMBO J. 21:4402–10 [Google Scholar]
  123. Paredes AM, Ferreira D, Horton M, Saad A, Tsuruta H. 123.  et al. 2004. Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 324:373–86 [Google Scholar]
  124. Wu SR, Haag L, Hammar L, Wu B, Garoff H. 124.  et al. 2007. The dynamic envelope of a fusion class II virus: prefusion stages of Semliki Forest virus revealed by electron cryomicroscopy. J. Biol. Chem. 282:6752–62 [Google Scholar]
  125. Bubeck D, Filman DJ, Kuzmin M, Fuller SD, Hogle JM. 125.  2008. Post-imaging fiducial markers aid in the orientation determination of complexes with mixed or unknown symmetry. J. Struct. Biol. 162:480–90 [Google Scholar]
  126. Moore JP, Doms RW. 126.  2003. The entry of entry inhibitors: a fusion of science and medicine. Proc. Natl. Acad. Sci. USA 100:10598–602 [Google Scholar]
  127. Pierson TC, Kielian M. 127.  2013. Flaviviruses: braking the entering. Curr. Opin. Virol. 3:3–12 [Google Scholar]
  128. Schoggins JW, Randall G. 128.  2013. Lipids in innate antiviral defense. Cell Host Microbe 14:379–85 [Google Scholar]
  129. Cianci C, Langley DR, Dischino DD, Sun Y, Yu KL. 129.  et al. 2004. Targeting a binding pocket within the trimer-of-hairpins: small-molecule inhibition of viral fusion. Proc. Natl. Acad. Sci. USA 101:15046–51 [Google Scholar]
  130. Frey G, Rits-Volloch S, Zhang XQ, Schooley RT, Chen B, Harrison SC. 130.  2006. Small molecules that bind the inner core of gp41 and inhibit HIV envelope-mediated fusion. Proc. Natl. Acad. Sci. USA 103:13938–43 [Google Scholar]
  131. Zhou Z, Khaliq M, Suk JE, Patkar C, Li L. 131.  et al. 2008. Antiviral compounds discovered by virtual screening of small-molecule libraries against dengue virus E protein. ACS Chem. Biol. 3:765–75 [Google Scholar]
  132. Russell RJ, Kerry PS, Stevens DJ, Steinhauer DA, Martin SR. 132.  et al. 2008. Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc. Natl. Acad. Sci. USA 105:17736–41 [Google Scholar]
  133. Hrobowski YM, Garry RF, Michael SF. 133.  2005. Peptide inhibitors of dengue virus and West Nile virus infectivity. Virol. J. 2:49 [Google Scholar]
  134. Schmidt AG, Yang PL, Harrison SC. 134.  2010. Peptide inhibitors of dengue-virus entry target a late-stage fusion intermediate. PLoS Pathog. 6:e1000851 [Google Scholar]
  135. Kaufmann B, Chipman PR, Holdaway HA, Johnson S, Fremont DH. 135.  et al. 2009. Capturing a flavivirus pre-fusion intermediate. PLoS Pathog. 5:e1000672 [Google Scholar]
  136. Melikyan GB. 136.  2010. Driving a wedge between viral lipids blocks infection. Proc. Natl. Acad. Sci. USA 107:17069–70 [Google Scholar]
  137. Vigant F, Hollmann A, Lee J, Santos NC, Jung ME, Lee B. 137.  2014. The rigid amphipathic fusion inhibitor dUY11 acts through photosensitization of viruses. J. Virol. 88:1849–53 [Google Scholar]
  138. Vigant F, Lee J, Hollmann A, Tanner LB, Akyol-Ataman Z. 138.  et al. 2013. A mechanistic paradigm for broad-spectrum antivirals that target virus-cell fusion. PLoS Pathog. 9:e1003297 [Google Scholar]
  139. Wolf MC, Freiberg AN, Zhang T, Akyol-Ataman Z, Grock A. 139.  et al. 2010. A broad-spectrum antiviral targeting entry of enveloped viruses. Proc. Natl. Acad. Sci. USA 107:3157–62 [Google Scholar]
  140. St Vincent MR, Colpitts CC, Ustinov AV, Muqadas M, Joyce MA. 140.  et al. 2010. Rigid amphipathic fusion inhibitors, small molecule antiviral compounds against enveloped viruses. Proc. Natl. Acad. Sci. USA 107:17339–44 [Google Scholar]
  141. Skehel JJ, Wiley DC. 141.  1998. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 95:871–74 [Google Scholar]
  142. Sutton RB, Fasshauer D, Jahn R, Brunger AT. 142.  1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:347–53 [Google Scholar]
  143. Sudhof TC, Rothman JE. 143.  2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–77 [Google Scholar]
  144. Perez-Vargas J, Krey T, Valansi C, Avinoam O, Haouz A. 144.  et al. 2014. Structural basis of eukaryotic cell-cell fusion. Cell 157:407–19 [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085521
Loading
/content/journals/10.1146/annurev-virology-031413-085521
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error