1932

Abstract

Flaviviruses are arthropod-borne RNA viruses that are a significant threat to global health due to their widespread distribution, ability to cause severe disease in humans, and capacity for explosive spread following introduction into new regions. Members of this genus include dengue, tick-borne encephalitis, yellow fever, and Zika viruses. Vaccination has been a highly successful means to control flaviviruses, and neutralizing antibodies are an important component of a protective immune response. High-resolution structures of flavivirus structural proteins and virions, alone and in complex with antibodies, provide a detailed understanding of viral fusion mechanisms and virus-antibody interactions. However, mounting evidence suggests these structures provide only a snapshot of an otherwise structurally dynamic virus particle. The contribution of the structural ensemble arising from viral breathing to the biology, antigenicity, and immunity of flaviviruses is discussed, including implications for the development and evaluation of flavivirus vaccines.

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2018-09-29
2024-12-06
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Literature Cited

  1. 1.  Monath TP, Vasconcelos PF 2015. Yellow fever. J. Clin. Virol. 64:160–73
    [Google Scholar]
  2. 2.  Tomori O 1999. Impact of yellow fever on the developing world. Adv. Virus Res. 53:5–34
    [Google Scholar]
  3. 3.  Barrett ADT 2017. Yellow fever live attenuated vaccine: a very successful live attenuated vaccine but still we have problems controlling the disease. Vaccine 35:5951–55
    [Google Scholar]
  4. 4.  Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW et al. 2013. The global distribution and burden of dengue. Nature 496:504–7
    [Google Scholar]
  5. 5.  Guzman MG, Alvarez M, Halstead SB 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch. Virol. 158:1445–59
    [Google Scholar]
  6. 6.  Mead PS, Hills SL, Brooks JT 2018. Zika virus as a sexually transmitted pathogen. Curr. Opin. Infect. Dis. 31:39–44
    [Google Scholar]
  7. 7.  Weaver SC, Costa F, Garcia-Blanco MA, Ko AI, Ribeiro GS et al. 2016. Zika virus: history, emergence, biology, and prospects for control. Antivir. Res. 130:69–80
    [Google Scholar]
  8. 8.  Weaver SC 2013. Urbanization and geographic expansion of zoonotic arboviral diseases: mechanisms and potential strategies for prevention. Trends Microbiol 21:360–63
    [Google Scholar]
  9. 9.  Noble CG, Shi PY 2012. Structural biology of dengue virus enzymes: towards rational design of therapeutics. Antivir. Res. 96:115–26
    [Google Scholar]
  10. 10.  Paul D, Bartenschlager R 2013. Architecture and biogenesis of plus-strand RNA virus replication factories. World J. Virol. 2:32–48
    [Google Scholar]
  11. 11.  Rey FA, Stiasny K, Heinz FX 2017. Flavivirus structural heterogeneity: implications for cell entry. Curr. Opin. Virol. 24:132–39
    [Google Scholar]
  12. 12.  Bressanelli S, Stiasny K, Allison SL, Stura EA, Duquerroy S et al. 2004. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J 23:728–38
    [Google Scholar]
  13. 13.  Modis Y, Ogata S, Clements D, Harrison SC 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313–19
    [Google Scholar]
  14. 14.  Yu IM, Zhang W, Holdaway HA, Li L, Kostyuchenko VA et al. 2008. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319:1834–37
    [Google Scholar]
  15. 15.  Perera R, Kuhn RJ 2008. Structural proteomics of dengue virus. Curr. Opin. Microbiol. 11:369–77
    [Google Scholar]
  16. 16.  Bothner B, Dong XF, Bibbs L, Johnson JE, Siuzdak G 1998. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J. Biol. Chem. 273:673–76
    [Google Scholar]
  17. 17.  Dowd KA, Jost CA, Durbin AP, Whitehead SS, Pierson TC 2011. A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLOS Pathog 7:e1002111
    [Google Scholar]
  18. 18.  Jimenez-Clavero MA, Douglas A, Lavery T, Garcia-Ranea JA, Ley V 2000. Immune recognition of swine vesicular disease virus structural proteins: novel antigenic regions that are not exposed in the capsid. Virology 270:76–83
    [Google Scholar]
  19. 19.  Lewis JK, Bothner B, Smith TJ, Siuzdak G 1998. Antiviral agent blocks breathing of the common cold virus. PNAS 95:6774–78
    [Google Scholar]
  20. 20.  Li Q, Yafal AG, Lee YM, Hogle J, Chow M 1994. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J. Virol. 68:3965–70
    [Google Scholar]
  21. 21.  Sauter P, Chehadeh W, Lobert PE, Lazrek M, Goffard A et al. 2008. A part of the VP4 capsid protein exhibited by coxsackievirus B4 E2 is the target of antibodies contained in plasma from patients with type 1 diabetes. J. Med. Virol. 80:866–78
    [Google Scholar]
  22. 22.  Kuhn RJ, Dowd KA, Beth Post C, Pierson TC 2015. Shake, rattle, and roll: impact of the dynamics of flavivirus particles on their interactions with the host. Virology 479–80:508–17
    [Google Scholar]
  23. 23.  Pierson TC, Kielian M 2013. Flaviviruses: braking the entering. Curr. Opin. Virol. 3:3–12
    [Google Scholar]
  24. 24.  Navarro-Sanchez E, Altmeyer R, Amara A, Schwartz O, Fieschi F et al. 2003. Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 4:723–28
    [Google Scholar]
  25. 25.  Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J et al. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823–29
    [Google Scholar]
  26. 26.  Davis CW, Nguyen HY, Hanna SL, Sanchez MD, Doms RW, Pierson TC 2006. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J. Virol. 80:1290–301
    [Google Scholar]
  27. 27.  Meertens L, Carnec X, Lecoin MP, Ramdasi R, Guivel-Benhassine F et al. 2012. The TIM and TAM families of phosphatidylserine receptors mediate dengue virus entry. Cell Host Microbe 12:544–57
    [Google Scholar]
  28. 28.  Carnec X, Meertens L, Dejarnac O, Perera-Lecoin M, Hafirassou ML et al. 2015. The phosphatidylserine and phosphatidylethanolamine receptor CD300a binds dengue virus and enhances infection. J. Virol. 90:92–102
    [Google Scholar]
  29. 29.  Hamel R, Dejarnac O, Wichit S, Ekchariyawat P, Neyret A et al. 2015. Biology of Zika virus infection in human skin cells. J. Virol. 89:8880–96
    [Google Scholar]
  30. 30.  Miller JL, de Wet BJ, Martinez-Pomares L, Radcliffe CM, Dwek RA et al. 2008. The mannose receptor mediates dengue virus infection of macrophages. PLOS Pathog 4:e17
    [Google Scholar]
  31. 31.  Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD et al. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3:866–71
    [Google Scholar]
  32. 32.  Kroschewski H, Allison SL, Heinz FX, Mandl CW 2003. Role of heparan sulfate for attachment and entry of tick-borne encephalitis virus. Virology 308:92–100
    [Google Scholar]
  33. 33.  Lee E, Lobigs M 2000. Substitutions at the putative receptor-binding site of an encephalitic flavivirus alter virulence and host cell tropism and reveal a role for glycosaminoglycans in entry. J. Virol. 74:8867–75
    [Google Scholar]
  34. 34.  Lozach PY, Burleigh L, Staropoli I, Navarro-Sanchez E, Harriague J et al. 2005. Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J. Biol. Chem. 280:23698–708
    [Google Scholar]
  35. 35.  Moesker B, Rodenhuis-Zybert IA, Meijerhof T, Wilschut J, Smit JM 2010. Characterization of the functional requirements of West Nile virus membrane fusion. J. Gen. Virol. 91:389–93
    [Google Scholar]
  36. 36.  Zaitseva E, Yang ST, Melikov K, Pourmal S, Chernomordik LV 2010. Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLOS Pathog 6:e1001131
    [Google Scholar]
  37. 37.  Hastings AK, Yockey LJ, Jagger BW, Hwang J, Uraki R et al. 2017. TAM receptors are not required for Zika virus infection in mice. Cell Rep 19:558–68
    [Google Scholar]
  38. 38.  Meertens L, Labeau A, Dejarnac O, Cipriani S, Sinigaglia L et al. 2017. Axl mediates ZIKA virus entry in human glial cells and modulates innate immune responses. Cell Rep 18:324–33
    [Google Scholar]
  39. 39.  van der Schaar HM, Rust MJ, Waarts BL, van der Ende-Metselaar H, Kuhn RJ et al. 2007. Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J. Virol. 81:12019–28
    [Google Scholar]
  40. 40.  Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CK et al. 2009. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5:365–75
    [Google Scholar]
  41. 41.  Apte-Sengupta S, Sirohi D, Kuhn RJ 2014. Coupling of replication and assembly in flaviviruses. Curr. Opin. Virol. 9:134–42
    [Google Scholar]
  42. 42.  Prasad VM, Miller AS, Klose T, Sirohi D, Buda G et al. 2017. Structure of the immature Zika virus at 9 Å resolution. Nat. Struct. Mol. Biol. 24:184–86
    [Google Scholar]
  43. 43.  Li L, Lok SM, Yu IM, Zhang Y, Kuhn RJ et al. 2008. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319:1830–34
    [Google Scholar]
  44. 44.  Elshuber S, Allison SL, Heinz FX, Mandl CW 2003. Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol. 84:183–91
    [Google Scholar]
  45. 45.  Stadler K, Allison SL, Schalich J, Heinz FX 1997. Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71:8475–81
    [Google Scholar]
  46. 46.  Hasan SS, Sevvana M, Kuhn RJ, Rossmann MG 2018. Structural biology of Zika virus and other flaviviruses. Nat. Struct. Mol. Biol. 25:13–20
    [Google Scholar]
  47. 47.  Zhang Y, Zhang W, Ogata S, Clements D, Strauss JH et al. 2004. Conformational changes of the flavivirus E glycoprotein. Structure 12:1607–18
    [Google Scholar]
  48. 48.  Zhang W, Chipman PR, Corver J, Johnson PR, Zhang Y et al. 2003. Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat. Struct. Biol. 10:907–12
    [Google Scholar]
  49. 49.  Allison SL, Schalich J, Stiasny K, Mandl CW, Heinz FX 2001. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J. Virol. 75:4268–75
    [Google Scholar]
  50. 50.  Vaney MC, Rey FA 2011. Class II enveloped viruses. Cell Microbiol 13:1451–59
    [Google Scholar]
  51. 51.  Kielian M, Rey FA 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:67–76
    [Google Scholar]
  52. 52.  Wang X, Li SH, Zhu L, Nian QG, Yuan S et al. 2017. Near-atomic structure of Japanese encephalitis virus reveals critical determinants of virulence and stability. Nat. Commun. 8:14
    [Google Scholar]
  53. 53.  Fibriansah G, Ng TS, Kostyuchenko VA, Lee J, Lee S et al. 2013. Structural changes in dengue virus when exposed to a temperature of 37°C. J. Virol. 87:7585–92
    [Google Scholar]
  54. 54.  Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, Rossmann MG 2013. Dengue structure differs at the temperatures of its human and mosquito hosts. PNAS 110:6795–99
    [Google Scholar]
  55. 55.  Kostyuchenko VA, Chew PL, Ng TS, Lok SM 2014. Near-atomic resolution cryo-electron microscopic structure of dengue serotype 4 virus. J. Virol. 88:477–82
    [Google Scholar]
  56. 56.  Pierson TC, Diamond MS 2012. Degrees of maturity: the complex structure and biology of flaviviruses. Curr. Opin. Virol. 2:168–75
    [Google Scholar]
  57. 57.  Junjhon J, Edwards TJ, Utaipat U, Bowman VD, Holdaway HA et al. 2010. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J. Virol. 84:8353–58
    [Google Scholar]
  58. 58.  Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL et al. 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLOS Pathog 6:e1000790
    [Google Scholar]
  59. 59.  Zellweger RM, Prestwood TR, Shresta S 2010. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 7:128–39
    [Google Scholar]
  60. 60.  Colpitts TM, Rodenhuis-Zybert I, Moesker B, Wang P, Fikrig E, Smit JM 2011. prM-antibody renders immature West Nile virus infectious in vivo. J. Gen. Virol. 92:2281–85
    [Google Scholar]
  61. 61.  Rodenhuis-Zybert IA, van der Schaar HM, da Silva Voorham JM, van der Ende-Metselaar H, Lei HY et al. 2010. Immature dengue virus: a veiled pathogen?. PLOS Pathog 6:e1000718
    [Google Scholar]
  62. 62.  Nelson S, Jost CA, Xu Q, Ess J, Martin JE et al. 2008. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLOS Pathog 4:e1000060
    [Google Scholar]
  63. 63.  Guirakhoo F, Bolin RA, Roehrig JT 1992. 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 191:921–31
    [Google Scholar]
  64. 64.  Plevka P, Battisti AJ, Sheng J, Rossmann MG 2014. Mechanism for maturation-related reorganization of flavivirus glycoproteins. J. Struct. Biol. 185:27–31
    [Google Scholar]
  65. 65.  Plevka P, Battisti AJ, Junjhon J, Winkler DC, Holdaway HA et al. 2011. Maturation of flaviviruses starts from one or more icosahedrally independent nucleation centres. EMBO Rep 12:602–6
    [Google Scholar]
  66. 66.  Mukherjee S, Dowd KA, Manhart CJ, Ledgerwood JE, Durbin AP et al. 2014. Mechanism and significance of cell type-dependent neutralization of flaviviruses. J. Virol. 88:7210–20
    [Google Scholar]
  67. 67.  Dejnirattisai W, Wongwiwat W, Supasa S, Zhang X, Dai X et al. 2015. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 16:170–77
    [Google Scholar]
  68. 68.  Cherrier MV, Kaufmann B, Nybakken GE, Lok SM, Warren JT et al. 2009. Structural basis for the preferential recognition of immature flaviviruses by a fusion-loop antibody. EMBO J 28:3269–76
    [Google Scholar]
  69. 69.  Nybakken GE, Oliphant T, Johnson S, Burke S, Diamond MS, Fremont DH 2005. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437:764–69
    [Google Scholar]
  70. 70.  Crill WD, Roehrig JT 2001. 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. 75:7769–73
    [Google Scholar]
  71. 71.  He RT, Innis BL, Nisalak A, Usawattanakul W, Wang S et al. 1995. Antibodies that block virus attachment to vero cells are a major component of the human neutralizing antibody response against dengue virus type 2. J. Med. Virol. 45:451–61
    [Google Scholar]
  72. 72.  Shi X, Deng Y, Wang H, Ji G, Tan W et al. 2016. A bispecific antibody effectively neutralizes all four serotypes of dengue virus by simultaneous blocking virus attachment and fusion. mAbs 8:574–84
    [Google Scholar]
  73. 73.  Della-Porta AJ, Westaway EG 1978. A multi-hit model for the neutralization of animal viruses. J. Gen. Virol. 38:1–19
    [Google Scholar]
  74. 74.  Dowd KA, Pierson TC 2011. Antibody-mediated neutralization of flaviviruses: a reductionist view. Virology 411:306–15
    [Google Scholar]
  75. 75.  Pierson TC, Xu Q, Nelson S, Oliphant T, Nybakken GE et al. 2007. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1:135–45
    [Google Scholar]
  76. 76.  Stiasny K, Kiermayr S, Holzmann H, Heinz FX 2006. Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J. Virol. 80:9557–68
    [Google Scholar]
  77. 77.  Oliphant T, Nybakken GE, Engle M, Xu Q, Nelson CA et al. 2006. Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J. Virol. 80:12149–59
    [Google Scholar]
  78. 78.  Mehlhop E, Nelson S, Jost CA, Gorlatov S, Johnson S et al. 2009. Complement protein C1q reduces the stoichiometric threshold for antibody-mediated neutralization of West Nile virus. Cell Host Microbe 6:381–91
    [Google Scholar]
  79. 79.  Rodrigo WW, Block OK, Lane C, Sukupolvi-Petty S, Goncalvez AP et al. 2009. Dengue virus neutralization is modulated by IgG antibody subclass and Fcγ receptor subtype. Virology 394:175–82
    [Google Scholar]
  80. 80.  Gollins SW, Porterfield JS 1986. A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature 321:244–46
    [Google Scholar]
  81. 81.  Thompson BS, Moesker B, Smit JM, Wilschut J, Diamond MS, Fremont DH 2009. A therapeutic antibody against West Nile virus neutralizes infection by blocking fusion within endosomes. PLOS Pathog 5:e1000453
    [Google Scholar]
  82. 82.  Lu LL, Suscovich TJ, Fortune SM, Alter G 2018. Beyond binding: antibody effector functions in infectious diseases. Nat. Rev. Immunol. 18:46–61
    [Google Scholar]
  83. 83.  Boehr DD, Wright PE 2008. How do proteins interact?. Science 320:1429–30
    [Google Scholar]
  84. 84.  Karplus M, Kuriyan J 2005. Molecular dynamics and protein function. PNAS 102:6679–85
    [Google Scholar]
  85. 85.  Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M et al. 2005. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117–21
    [Google Scholar]
  86. 86.  Hogle JM, Chow M, Filman DJ 1985. Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229:1358–65
    [Google Scholar]
  87. 87.  Rossmann MG, Arnold E, Erickson JW, Frankenberger EA, Griffith JP et al. 1985. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145–53
    [Google Scholar]
  88. 88.  Basavappa R, Syed R, Flore O, Icenogle JP, Filman DJ, Hogle JM 1994. Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 Å resolution. Protein Sci 3:1651–69
    [Google Scholar]
  89. 89.  Hogle JM 2002. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56:677–702
    [Google Scholar]
  90. 90.  Belnap DM, Filman DJ, Trus BL, Cheng N, Booy FP et al. 2000. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74:1342–54
    [Google Scholar]
  91. 91.  Bubeck D, Filman DJ, Cheng N, Steven AC, Hogle JM, Belnap DM 2005. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79:7745–55
    [Google Scholar]
  92. 92.  Butan C, Filman DJ, Hogle JM 2014. Cryo-electron microscopy reconstruction shows poliovirus 135S particles poised for membrane interaction and RNA release. J. Virol. 88:1758–70
    [Google Scholar]
  93. 93.  Curry S, Chow M, Hogle JM 1996. The poliovirus 135S particle is infectious. J. Virol. 70:7125–31
    [Google Scholar]
  94. 94.  Fricks CE, Hogle JM 1990. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64:1934–45
    [Google Scholar]
  95. 95.  Roivainen M, Piirainen L, Rysa T, Narvanen A, Hovi T 1993. An immunodominant N-terminal region of VP1 protein of poliovirion that is buried in crystal structure can be exposed in solution. Virology 195:762–65
    [Google Scholar]
  96. 96.  Diana GD, Otto MJ, McKinlay MA 1985. Inhibitors of picornavirus uncoating as antiviral agents. Pharmacol. Ther. 29:287–97
    [Google Scholar]
  97. 97.  Hayden FG, Herrington DT, Coats TL, Kim K, Cooper EC et al. 2003. Efficacy and safety of oral pleconaril for treatment of colds due to picornaviruses in adults: results of 2 double-blind, randomized, placebo-controlled trials. Clin. Infect. Dis. 36:1523–32
    [Google Scholar]
  98. 98.  Abzug MJ, Michaels MG, Wald E, Jacobs RF, Romero JR et al. 2016. A randomized, double-blind, placebo-controlled trial of pleconaril for the treatment of neonates with enterovirus sepsis. J. Pediatr. Infect. Dis. Soc. 5:53–62
    [Google Scholar]
  99. 99.  Reisdorph N, Thomas JJ, Katpally U, Chase E, Harris K et al. 2003. Human rhinovirus capsid dynamics is controlled by canyon flexibility. Virology 314:34–44
    [Google Scholar]
  100. 100.  Austin SK, Dowd KA, Shrestha B, Nelson CA, Edeling MA et al. 2012. Structural basis of differential neutralization of DENV-1 genotypes by an antibody that recognizes a cryptic epitope. PLOS Pathog 8:e1002930
    [Google Scholar]
  101. 101.  Lok SM, Kostyuchenko V, Nybakken GE, Holdaway HA, Battisti AJ et al. 2008. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 15:312–17
    [Google Scholar]
  102. 102.  Oliphant T, Engle M, Nybakken GE, Doane C, Johnson S et al. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 11:522–30
    [Google Scholar]
  103. 103.  Dowd KA, DeMaso CR, Pierson TC 2015. Genotypic differences in dengue virus neutralization are explained by a single amino acid mutation that modulates virus breathing. mBio 6:e01559–15
    [Google Scholar]
  104. 104.  Dowd KA, Mukherjee S, Kuhn RJ, Pierson TC 2014. Combined effects of the structural heterogeneity and dynamics of flaviviruses on antibody recognition. J. Virol. 88:11726–37
    [Google Scholar]
  105. 105.  Goo L, DeMaso CR, Pelc RS, Ledgerwood JE, Graham BS et al. 2018. The Zika virus envelope protein glycan loop regulates virion antigenicity. Virology 515:191–202
    [Google Scholar]
  106. 106.  Roehrig JT, Bolin RA, Kelly RG 1998. Monoclonal antibody mapping of the envelope glycoprotein of the dengue 2 virus, Jamaica. Virology 246:317–28
    [Google Scholar]
  107. 107.  de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP et al. 2012. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. PNAS 109:7439–44
    [Google Scholar]
  108. 108.  Fibriansah G, Tan JL, Smith SA, de Alwis AR, Ng TS et al. 2014. A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol. Med. 6:358–71
    [Google Scholar]
  109. 109.  Fibriansah G, Tan JL, Smith SA, de Alwis R, Ng TS et al. 2015. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat. Commun. 6:6341
    [Google Scholar]
  110. 110.  Kaufmann B, Vogt MR, Goudsmit J, Holdaway HA, Aksyuk AA et al. 2010. Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. PNAS 107:18950–55
    [Google Scholar]
  111. 111.  Teoh EP, Kukkaro P, Teo EW, Lim AP, Tan TT et al. 2012. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med. 4:139ra83
    [Google Scholar]
  112. 112.  Hasan SS, Miller A, Sapparapu G, Fernandez E, Klose T et al. 2017. A human antibody against Zika virus crosslinks the E protein to prevent infection. Nat. Commun. 8:14722
    [Google Scholar]
  113. 113.  Gallichotte EN, Widman DG, Yount BL, Wahala WM, Durbin A et al. 2015. A new quaternary structure epitope on dengue virus serotype 2 is the target of durable type-specific neutralizing antibodies. mBio 6:e01461–15
    [Google Scholar]
  114. 114.  Jarmer J, Zlatkovic J, Tsouchnikas G, Vratskikh O, Strauss J et al. 2014. Variation of the specificity of the human antibody responses after tick-borne encephalitis virus infection and vaccination. J. Virol. 88:13845–57
    [Google Scholar]
  115. 115.  Kiermayr S, Stiasny K, Heinz FX 2009. Impact of quaternary organization on the antigenic structure of the tick-borne encephalitis virus envelope glycoprotein E. J. Virol. 83:8482–91
    [Google Scholar]
  116. 116.  Rouvinski A, Guardado-Calvo P, Barba-Spaeth G, Duquerroy S, Vaney MC et al. 2015. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 520:109–13
    [Google Scholar]
  117. 117.  Barba-Spaeth G, Dejnirattisai W, Rouvinski A, Vaney MC, Medits I et al. 2016. Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nature 536:48–53
    [Google Scholar]
  118. 118.  Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G et al. 2016. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with Zika virus. Nat. Immunol. 17:1102–8
    [Google Scholar]
  119. 119.  Swanstrom JA, Plante JA, Plante KS, Young EF, McGowan E et al. 2016. Dengue virus envelope dimer epitope monoclonal antibodies isolated from dengue patients are protective against Zika virus. mBio 7:e01123–16
    [Google Scholar]
  120. 120.  Rey FA, Stiasny K, Vaney MC, Dellarole M, Heinz FX 2017. The bright and the dark side of human antibody responses to flaviviruses: lessons for vaccine design. EMBO Rep 19:206–24
    [Google Scholar]
  121. 121.  Metz SW, Gallichotte EN, Brackbill A, Premkumar L, Miley MJ et al. 2017. In vitro assembly and stabilization of dengue and Zika virus envelope protein homo-dimers. Sci. Rep. 7:4524
    [Google Scholar]
  122. 122.  Rouvinski A, Dejnirattisai W, Guardado-Calvo P, Vaney MC, Sharma A et al. 2017. Covalently linked dengue virus envelope glycoprotein dimers reduce exposure of the immunodominant fusion loop epitope. Nat. Commun. 8:15411
    [Google Scholar]
  123. 123.  Moller-Tank S, Maury W 2014. Phosphatidylserine receptors: enhancers of enveloped virus entry and infection. Virology 468–70:565–80
    [Google Scholar]
  124. 124.  Jemielity S, Wang JJ, Chan YK, Ahmed AA, Li W et al. 2013. TIM-family proteins promote infection of multiple enveloped viruses through virion-associated phosphatidylserine. PLOS Pathog 9:e1003232
    [Google Scholar]
  125. 125.  Richard AS, Zhang A, Park SJ, Farzan M, Zong M, Choe H 2015. Virion-associated phosphatidylethanolamine promotes TIM1-mediated infection by Ebola, dengue, and West Nile viruses. PNAS 112:14682–87
    [Google Scholar]
  126. 126.  Zhang Y, Corver J, Chipman PR, Zhang W, Pletnev SV et al. 2003. Structures of immature flavivirus particles. EMBO J 22:2604–13
    [Google Scholar]
  127. 127.  Goo L, Dowd KA, Smith AR, Pelc RS, DeMaso CR, Pierson TC 2016. Zika virus is not uniquely stable at physiological temperatures compared to other flaviviruses. mBio 7:e01396–16
    [Google Scholar]
  128. 128.  Xie X, Yang Y, Muruato AE, Zou J, Shan C et al. 2017. Understanding Zika virus stability and developing a chimeric vaccine through functional analysis. mBio 8:e02134–16
    [Google Scholar]
  129. 129.  Carson SD 2014. Kinetic models for receptor-catalyzed conversion of coxsackievirus B3 to A-particles. J. Virol. 88:11568–75
    [Google Scholar]
  130. 130.  Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS et al. 1989. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J. Gen. Virol. 70:Pt. 137–43
    [Google Scholar]
  131. 131.  Katzelnick LC, Fonville JM, Gromowski GD, Bustos Arriaga J, Green A et al. 2015. Dengue viruses cluster antigenically but not as discrete serotypes. Science 349:1338–43
    [Google Scholar]
  132. 132.  Holmes EC, Twiddy SS 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect. Genet. Evol. 3:19–28
    [Google Scholar]
  133. 133.  Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA et al. 2010. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLOS Pathog 6:e1000823
    [Google Scholar]
  134. 134.  Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S et al. 2010. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J. Virol. 84:10630–43
    [Google Scholar]
  135. 135.  Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA et al. 2010. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 84:9227–39
    [Google Scholar]
  136. 136.  Sukupolvi-Petty S, Brien JD, Austin SK, Shrestha B, Swayne S et al. 2013. Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection. J. Virol. 87:8826–42
    [Google Scholar]
  137. 137.  Wahala WM, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, de Silva AM 2010. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLOS Pathog 6:e1000821
    [Google Scholar]
  138. 138.  Goo L, VanBlargan LA, Dowd KA, Diamond MS, Pierson TC 2017. A single mutation in the envelope protein modulates flavivirus antigenicity, stability, and pathogenesis. PLOS Pathog 13:e1006178
    [Google Scholar]
  139. 139.  Nybakken GE, Nelson CA, Chen BR, Diamond MS, Fremont DH 2006. Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 80:11467–74
    [Google Scholar]
  140. 140.  Luca VC, AbiMansour J, Nelson CA, Fremont DH 2012. Crystal structure of the Japanese encephalitis virus envelope protein. J. Virol. 86:2337–46
    [Google Scholar]
  141. 141.  Ansarah-Sobrinho C, Nelson S, Jost CA, Whitehead SS, Pierson TC 2008. Temperature-dependent production of pseudoinfectious dengue reporter virus particles by complementation. Virology 381:67–74
    [Google Scholar]
  142. 142.  Zhang X, Ge P, Yu X, Brannan JM, Bi G et al. 2013. Cryo-EM structure of the mature dengue virus at 3.5-Å resolution. Nat. Struct. Mol. Biol. 20:105–10
    [Google Scholar]
  143. 143.  Vogt MR, Dowd KA, Engle M, Tesh RB, Johnson S et al. 2011. Poorly neutralizing cross-reactive antibodies against the fusion loop of West Nile virus envelope protein protect in vivo via Fcγ receptor and complement-dependent effector mechanisms. J. Virol. 85:11567–80
    [Google Scholar]
  144. 144.  Murray JM, Aaskov JG, Wright PJ 1993. Processing of the dengue virus type 2 proteins prM and C-prM. J. Gen. Virol. 74:Pt. 2175–82
    [Google Scholar]
  145. 145.  Scherwitzl I, Mongkolsapaja J, Screaton G 2017. Recent advances in human flavivirus vaccines. Curr. Opin. Virol. 23:95–101
    [Google Scholar]
  146. 146.  Schalich J, Allison SL, Stiasny K, Mandl CW, Kunz C, Heinz FX 1996. Recombinant subviral particles from tick-borne encephalitis virus are fusogenic and provide a model system for studying flavivirus envelope glycoprotein functions. J. Virol. 70:4549–57
    [Google Scholar]
  147. 147.  Ferlenghi I, Clarke M, Ruttan T, Allison SL, Schalich J et al. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593–602
    [Google Scholar]
  148. 148.  Allison SL, Tao YJ, O'Riordain G, Mandl CW, Harrison SC, Heinz FX 2003. Two distinct size classes of immature and mature subviral particles from tick-borne encephalitis virus. J. Virol. 77:11357–66
    [Google Scholar]
  149. 149.  Konishi E, Pincus S, Paoletti E, Shope RE, Burrage T, Mason PW 1992. Mice immunized with a subviral particle containing the Japanese encephalitis virus prM/M and E proteins are protected from lethal JEV infection. Virology 188:714–20
    [Google Scholar]
  150. 150.  Konishi E, Fujii A 2002. Dengue type 2 virus subviral extracellular particles produced by a stably transfected mammalian cell line and their evaluation for a subunit vaccine. Vaccine 20:1058–67
    [Google Scholar]
  151. 151.  Kroeger MA, McMinn PC 2002. Murray Valley encephalitis virus recombinant subviral particles protect mice from lethal challenge with virulent wild-type virus. Arch. Virol. 147:1155–72
    [Google Scholar]
  152. 152.  Mason PW, Pincus S, Fournier MJ, Mason TL, Shope RE, Paoletti E 1991. Japanese encephalitis virus-vaccinia recombinants produce particulate forms of the structural membrane proteins and induce high levels of protection against lethal JEV infection. Virology 180:294–305
    [Google Scholar]
  153. 153.  Pincus S, Mason PW, Konishi E, Fonseca BA, Shope RE et al. 1992. Recombinant vaccinia virus producing the prM and E proteins of yellow fever virus protects mice from lethal yellow fever encephalitis. Virology 187:290–97
    [Google Scholar]
  154. 154.  Fonseca BA, Pincus S, Shope RE, Paoletti E, Mason PW 1994. Recombinant vaccinia viruses co-expressing dengue-1 glycoproteins prM and E induce neutralizing antibodies in mice. Vaccine 12:279–85
    [Google Scholar]
  155. 155.  Dowd KA, Ko SY, Morabito KM, Yang ES, Pelc RS et al. 2016. Rapid development of a DNA vaccine for Zika virus. Science 354:237–40
    [Google Scholar]
  156. 156.  Griffin BD, Muthumani K, Warner BM, Majer A, Hagan M et al. 2017. DNA vaccination protects mice against Zika virus-induced damage to the testes. Nat. Commun. 8:15743
    [Google Scholar]
  157. 157.  Pardi N, Hogan MJ, Pelc RS, Muramatsu H, Andersen H et al. 2017. Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination. Nature 543:248–51
    [Google Scholar]
  158. 158.  Richner JM, Himansu S, Dowd KA, Butler SL, Salazar V et al. 2017. Modified mRNA vaccines protect against Zika virus infection. Cell 169:176
    [Google Scholar]
  159. 159.  Tebas P, Roberts CC, Muthumani K, Reuschel EL, Kudchodkar SB et al. 2017. Safety and immunogenicity of an anti-Zika virus DNA vaccine—preliminary report. N. Engl. J. Med. In press. https://doi.org/10.1056/NEJMoa1708120
    [Crossref] [Google Scholar]
  160. 160.  Gaudinski MR, Houser KV, Morabito KM, Hu Z, Yamshchikov G et al. 2018. Safety, tolerability, and immunogenicity of two Zika virus DNA vaccine candidates in healthy adults: randomised, open-label, phase 1 clinical trials. Lancet 391:552–62
    [Google Scholar]
  161. 161.  Allison SL, Stiasny K, Stadler K, Mandl CW, Heinz FX 1999. Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein E. J. Virol. 73:5605–12
    [Google Scholar]
  162. 162.  Aberle JH, Aberle SW, Allison SL, Stiasny K, Ecker M et al. 1999. A DNA immunization model study with constructs expressing the tick-borne encephalitis virus envelope protein E in different physical forms. J. Immunol. 163:6756–61
    [Google Scholar]
  163. 163.  Heinz FX, Allison SL, Stiasny K, Schalich J, Holzmann H et al. 1995. Recombinant and virion-derived soluble and particulate immunogens for vaccination against tick-borne encephalitis. Vaccine 13:1636–42
    [Google Scholar]
  164. 164.  Vogt MR, Moesker B, Goudsmit J, Jongeneelen M, Austin SK et al. 2009. Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J. Virol. 83:6494–507
    [Google Scholar]
  165. 165.  Monath TP, Nichols R, Archambault WT, Moore L, Marchesani R et al. 2002. Comparative safety and immunogenicity of two yellow fever 17D vaccines (ARILVAX and YF-VAX) in a phase III multicenter, double-blind clinical trial. Am. J. Trop. Med. Hyg. 66:533–41
    [Google Scholar]
  166. 166.  Heinz FX, Holzmann H, Essl A, Kundi M 2007. Field effectiveness of vaccination against tick-borne encephalitis. Vaccine 25:7559–67
    [Google Scholar]
  167. 167.  Markoff L 2000. Points to consider in the development of a surrogate for efficacy of novel Japanese encephalitis virus vaccines. Vaccine 18:Suppl. 226–32
    [Google Scholar]
  168. 168.  Montoya M, Collins M, Dejnirattisai W, Katzelnick LC, Puerta-Guardo H et al. 2018. Longitudinal analysis of antibody cross-neutralization following Zika and dengue virus infection in Asia and the Americas. J. Infect. Dis. 218:536–45
    [Google Scholar]
  169. 169.  Patel B, Longo P, Miley MJ, Montoya M, Harris E, de Silva AM 2017. Dissecting the human serum antibody response to secondary dengue virus infections. PLOS Negl. Trop. Dis. 11:e0005554
    [Google Scholar]
  170. 170.  de Alwis R, Williams KL, Schmid MA, Lai CY, Patel B et al. 2014. Dengue viruses are enhanced by distinct populations of serotype cross-reactive antibodies in human immune sera. PLOS Pathog 10:e1004386
    [Google Scholar]
  171. 171.  Katzelnick LC, Gresh L, Halloran ME, Mercado JC, Kuan G et al. 2017. Antibody-dependent enhancement of severe dengue disease in humans. Science 358:929–32
    [Google Scholar]
  172. 172.  Hadinegoro SR, Arredondo-Garcia JL, Capeding MR, Deseda C, Chotpitayasunondh T et al. 2015. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N. Engl. J. Med. 373:1195–206
    [Google Scholar]
  173. 173.  World Health Organ 2017. Dengue vaccine: WHO position paper, July 2016—recommendations. Vaccine 35:1200–1
    [Google Scholar]
  174. 174.  Munro JB, Gorman J, Ma X, Zhou Z, Arthos J et al. 2014. Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346:759–63
    [Google Scholar]
  175. 175.  Seaman MS, Janes H, Hawkins N, Grandpre LE, Devoy C et al. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84:1439–52
    [Google Scholar]
  176. 176.  Guttman M, Cupo A, Julien JP, Sanders RW, Wilson IA et al. 2015. Antibody potency relates to the ability to recognize the closed, pre-fusion form of HIV Env. Nat. Commun. 6:6144
    [Google Scholar]
  177. 177.  VanBlargan LA, Goo L, Pierson TC 2016. Deconstructing the antiviral neutralizing-antibody response: implications for vaccine development and immunity. Microbiol. Mol. Biol. Rev. 80:989–1010
    [Google Scholar]
  178. 178.  Lim XX, Chandramohan A, Lim XE, Crowe JE Jr., Lok SM, Anand GS 2017. Epitope and paratope mapping reveals temperature-dependent alterations in the dengue-antibody interface. Structure 25:1391–402.e3
    [Google Scholar]
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