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Abstract

Dengue virus (DENV) is a mosquito-transmitted RNA virus responsible for 390 million infections each year and significant morbidity and mortality throughout tropical and subtropical regions of the world. Efforts to develop a DENV vaccine span 70 years and include the work of luminaries of the virus vaccine field. Although vaccines have been used to reduce the global health burden of other flaviviruses, the unique requirement for a single vaccine to protect against four different groups of dengue viruses, and the link between secondary infections and DENV disease pathogenesis, has limited success to date. In this review, we discuss several promising DENV vaccine candidates in clinical trials and assess how recent advances in understanding of DENV biology and immunity may expedite efforts toward the development of safe and effective vaccines.

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2014-09-29
2024-04-19
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Literature Cited

  1. Rush AB. 1.  1789. An account of the bilious remitting fever, as it appeared in Philadelphia, in the summer and autumn of the year 1780. Medical Inquiries and Observations104–17 Philadelphia: Prichard & Hall [Google Scholar]
  2. Kuno G. 2.  2007. Research on dengue and dengue-like illness in East Asia and the Western Pacific during the first half of the 20th century. Rev. Med. Virol. 17:327–41 [Google Scholar]
  3. Mackenzie JS, Gubler DJ, Petersen LR. 3.  2004. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10:S98–109 [Google Scholar]
  4. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW. 4.  et al. 2013. The global distribution and burden of dengue. Nature 496:504–7 [Google Scholar]
  5. Hammon WM, Rudnick A, Sather G, Rogers KD, Morse LJ. 5.  1960. New hemorrhagic fevers of children in the Philippines and Thailand. Trans. Assoc. Am. Physicians 73:140–55 [Google Scholar]
  6. Kouri GP, Guzman MG, Bravo JR, Triana C. 6.  1989. Dengue haemorrhagic fever/dengue shock syndrome: lessons from the Cuban epidemic, 1981. Bull. World Health Organ. 67:375–80 [Google Scholar]
  7. Pierson TC, Kielian M. 7.  2013. Flaviviruses: braking the entering. Curr. Opin. Virol. 3:3–12 [Google Scholar]
  8. Zaitseva E, Yang ST, Melikov K, Pourmal S, Chernomordik LV. 8.  2010. Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog. 6:e1001131 [Google Scholar]
  9. Lindenbach BD, Rice CM. 9.  2003. Molecular biology of flaviviruses. Adv. Virus Res. 59:23–61 [Google Scholar]
  10. Elshuber S, Allison SL, Heinz FX, Mandl CW. 10.  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]
  11. Stadler K, Allison SL, Schalich J, Heinz FX. 11.  1997. Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71:8475–81 [Google Scholar]
  12. Kaufmann B, Rossmann MG. 12.  2011. Molecular mechanisms involved in the early steps of flavivirus cell entry. Microbes Infect. 13:1–9 [Google Scholar]
  13. Nelson S, Jost CA, Xu Q, Ess J, Martin JE. 13.  et al. 2008. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog. 4:e1000060 [Google Scholar]
  14. Li L, Lok SM, Yu IM, Zhang Y, Kuhn RJ. 14.  et al. 2008. The flavivirus precursor membrane–envelope protein complex: structure and maturation. Science 319:1830–34 [Google Scholar]
  15. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J. 15.  et al. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717–25 [Google Scholar]
  16. Nybakken G, Oliphant T, Johnson S, Burke S, Diamond MS, Fremont DH. 16.  2005. Structural basis for neutralization of a therapeutic antibody against West Nile virus. Nature 437:764–69 [Google Scholar]
  17. Kaufmann B, Nybakken G, Chipman PR, Zhang W, Fremont DH. 17.  et al. 2006. West Nile virus in complex with a neutralizing monoclonal antibody. Proc. Natl. Acad. Sci. USA 103:12400–4 [Google Scholar]
  18. Kaufmann B, Vogt MR, Goudsmit J, Holdaway HA, Aksyuk AA. 18.  et al. 2010. Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. Proc. Natl. Acad. Sci. USA 107:18950–55 [Google Scholar]
  19. de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP. 19.  et al. 2012. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc. Natl. Acad. Sci. USA 109:7439–44 [Google Scholar]
  20. Teoh EP, Kukkaro P, Teo EW, Lim AP, Tan TT. 20.  et al. 2012. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med. 4:139ra183 [Google Scholar]
  21. Balmaseda A, Hammond SN, Tellez Y, Imhoff L, Rodriguez Y. 21.  et al. 2006. High seroprevalence of antibodies against dengue virus in a prospective study of schoolchildren in Managua, Nicaragua. Trop. Med. Int. Health 11:935–42 [Google Scholar]
  22. Burke DS, Nisalak A, Johnson DE, Scott RM. 22.  1988. A prospective study of dengue infections in Bangkok. Am. J. Trop. Med. Hyg. 38:172–80 [Google Scholar]
  23. Endy TP, Chunsuttiwat S, Nisalak A, Libraty DH, Green S. 23.  et al. 2002. Epidemiology of inapparent and symptomatic acute dengue virus infection: a prospective study of primary school children in Kamphaeng Phet, Thailand. Am. J. Epidemiol. 156:40–51 [Google Scholar]
  24. Sabin AB. 24.  1952. Research on dengue during World War II. Am. J. Trop. Med. Hyg. 1:30–50 [Google Scholar]
  25. Seet RC, Quek AM, Lim EC. 25.  2007. Post-infectious fatigue syndrome in dengue infection. J. Clin. Virol. 38:1–6 [Google Scholar]
  26. Halstead SB. 26.  2007. Dengue. Lancet 370:1644–52 [Google Scholar]
  27. World Health Organ. (WHO) 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control Geneva: WHO, 3rd ed..
  28. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S. 28.  et al. 2000. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J. Infect. Dis. 181:2–9 [Google Scholar]
  29. Murgue B, Roche C, Chungue E, Deparis X. 29.  2000. Prospective study of the duration and magnitude of viraemia in children hospitalised during the 1996–1997 dengue-2 outbreak in French Polynesia. J. Med. Virol. 60:432–38 [Google Scholar]
  30. Libraty DH, Endy TP, Houng HS, Green S, Kalayanarooj S. 30.  et al. 2002. Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J. Infect. Dis. 185:1213–21 [Google Scholar]
  31. Ngo NT, Cao XT, Kneen R, Wills B, Nguyen VM. 31.  et al. 2001. Acute management of dengue shock syndrome: a randomized double-blind comparison of 4 intravenous fluid regimens in the first hour. Clin. Infect. Dis. 32:204–13 [Google Scholar]
  32. Guzman MG, Kouri G, Valdes L, Bravo J, Vazquez S, Halstead SB. 32.  2002. Enhanced severity of secondary dengue-2 infections: death rates in 1981 and 1997 Cuban outbreaks. Rev. Panam. Salud Publica 11:223–27 [Google Scholar]
  33. Halstead SB, Nimmannitya S, Cohen SN. 33.  1970. Observations related to pathogenesis of dengue hemorrhagic fever. IV. Relation of disease severity to antibody response and virus recovered. Yale J. Biol. Med. 42:311–28 [Google Scholar]
  34. Graham RR, Juffrie M, Tan R, Hayes CG, Laksono I. 34.  et al. 1999. A prospective seroepidemiologic study on dengue in children four to nine years of age in Yogyakarta, Indonesia. I. Studies in 1995–1996. Am. J. Trop. Med. Hyg. 61:412–19 [Google Scholar]
  35. Jain A, Chaturvedi UC. 35.  2010. Dengue in infants: an overview. FEMS Immunol. Med. Microbiol. 59:119–30 [Google Scholar]
  36. Simmons CP, Chau TN, Thuy TT, Tuan NM, Hoang DM. 36.  et al. 2007. Maternal antibody and viral factors in the pathogenesis of dengue virus in infants. J. Infect. Dis. 196:416–24 [Google Scholar]
  37. Kliks SC, Nimmanitya S, Nisalak A, Burke DS. 37.  1988. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am. J. Trop. Med. Hyg. 38:411–19 [Google Scholar]
  38. Libraty DH, Acosta LP, Tallo V, Segubre-Mercado E, Bautista A. 38.  et al. 2009. A prospective nested case-control study of dengue in infants: rethinking and refining the antibody-dependent enhancement dengue hemorrhagic fever model. PLoS Med. 6:e1000171 [Google Scholar]
  39. Bharaj P, Chahar HS, Pandey A, Diddi K, Dar L. 39.  et al. 2008. Concurrent infections by all four dengue virus serotypes during an outbreak of dengue in 2006 in Delhi, India. Virol. J. 5:1 [Google Scholar]
  40. Wilder-Smith A, Gubler DJ. 40.  2008. Geographic expansion of dengue: the impact of international travel. Med. Clin. N. Am. 92:1377–90 [Google Scholar]
  41. Kyle JL, Harris E. 41.  2008. Global spread and persistence of dengue. Annu. Rev. Microbiol. 62:71–92 [Google Scholar]
  42. Sabin AB, Schlesinger RW. 42.  1945. Production of immunity to dengue with virus modified by propagation in mice. Science 101:640–42 [Google Scholar]
  43. Theiler M, Smith HH. 43.  1937. The use of yellow fever virus modified by in vitro cultivation for human immunization. J. Exp. Med. 65:787–800 [Google Scholar]
  44. Yauch LE, Shresta S. 44.  2014. Dengue virus vaccine development. Adv. Virus Res. 88:315–72 [Google Scholar]
  45. Barrett AD, Teuwen DE. 45.  2009. Yellow fever vaccine—how does it work and why do rare cases of serious adverse events take place?. Curr. Opin. Immunol. 21:308–13 [Google Scholar]
  46. Guy B, Barrere B, Malinowski C, Saville M, Teyssou R, Lang J. 46.  2011. From research to phase III: preclinical, industrial and clinical development of the Sanofi Pasteur tetravalent dengue vaccine. Vaccine 29:7229–41 [Google Scholar]
  47. Monath TP. 47.  2005. Yellow fever vaccine. Expert Rev. Vaccines 4:553–74 [Google Scholar]
  48. Beck A, Tesh RB, Wood TG, Widen SG, Ryman KD, Barrett AD. 48.  2013. Comparison of the live attenuated yellow fever vaccine 17D-204 strain to its virulent parental strain Asibi by deep sequencing. J. Infect. Dis. 209:334–44 [Google Scholar]
  49. Whitehead SS, Hanley KA, Blaney JE Jr, Gilmore LE, Elkins WR, Murphy BR. 49.  2003. Substitution of the structural genes of dengue virus type 4 with those of type 2 results in chimeric vaccine candidates which are attenuated for mosquitoes, mice, and rhesus monkeys. Vaccine 21:4307–16 [Google Scholar]
  50. Guirakhoo F, Kitchener S, Morrison D, Forrat R, McCarthy K. 50.  et al. 2006. Live attenuated chimeric yellow fever dengue type 2 (ChimeriVaxTM-DEN2) vaccine: phase I clinical trial for safety and immunogenicity: effect of yellow fever pre-immunity in induction of cross neutralizing antibody responses to all 4 dengue serotypes. Hum. Vaccines 2:60–67 [Google Scholar]
  51. Morrison D, Legg TJ, Billings CW, Forrat R, Yoksan S, Lang J. 51.  2010. A novel tetravalent dengue vaccine is well tolerated and immunogenic against all 4 serotypes in flavivirus-naive adults. J. Infect. Dis. 201:370–77 [Google Scholar]
  52. Sabchareon A, Wallace D, Sirivichayakul C, Limkittikul K, Chanthavanich P. 52.  et al. 2012. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380:1559–67 [Google Scholar]
  53. Durbin AP, Kirkpatrick BD, Pierce KK, Schmidt AC, Whitehead SS. 53.  2011. Development and clinical evaluation of multiple investigational monovalent DENV vaccines to identify components for inclusion in a live attenuated tetravalent DENV vaccine. Vaccine 29:7242–50 [Google Scholar]
  54. Troyer JM, Hanley KA, Whitehead SS, Strickman D, Karron RA. 54.  et al. 2001. A live attenuated recombinant dengue-4 virus vaccine candidate with restricted capacity for dissemination in mosquitoes and lack of transmission from vaccinees to mosquitoes. Am. J. Trop. Med. Hyg. 65:414–19 [Google Scholar]
  55. Durbin AP, Karron RA, Sun W, Vaughn DW, Reynolds MJ. 55.  et al. 2001. Attenuation and immunogenicity in humans of a live dengue virus type-4 vaccine candidate with a 30 nucleotide deletion in its 3′-untranslated region. Am. J. Trop. Med. Hyg. 65:405–13 [Google Scholar]
  56. Durbin AP, Kirkpatrick BD, Pierce KK, Elwood D, Larsson CJ. 56.  et al. 2013. A single dose of any of four different live attenuated tetravalent dengue vaccines is safe and immunogenic in flavivirus-naive adults: a randomized, double-blind clinical trial. J. Infect. Dis. 207:957–65 [Google Scholar]
  57. Vaughn DW, Hoke CH Jr, Yoksan S, LaChance R, Innis BL. 57.  et al. 1996. Testing of a dengue 2 live-attenuated vaccine (strain 16681 PDK 53) in ten American volunteers. Vaccine 14:329–36 [Google Scholar]
  58. Butrapet S, Huang CY, Pierro DJ, Bhamarapravati N, Gubler DJ, Kinney RM. 58.  2000. Attenuation markers of a candidate dengue type 2 vaccine virus, strain 16681 (PDK-53), are defined by mutations in the 5′ noncoding region and nonstructural proteins 1 and 3. J. Virol. 74:3011–19 [Google Scholar]
  59. Huang CY, Kinney RM, Livengood JA, Bolling B, Arguello JJ. 59.  et al. 2013. Genetic and phenotypic characterization of manufacturing seeds for a tetravalent dengue vaccine (DENVax). PLoS Negl. Trop. Dis. 7:e2243 [Google Scholar]
  60. Coller BA, Clements DE, Bett AJ, Sagar SL, Ter Meulen JH. 60.  2011. The development of recombinant subunit envelope-based vaccines to protect against dengue virus induced disease. Vaccine 29:7267–75 [Google Scholar]
  61. Kitchener S, Nissen M, Nasveld P, Forrat R, Yoksan S. 61.  et al. 2006. Immunogenicity and safety of two live-attenuated tetravalent dengue vaccine formulations in healthy Australian adults. Vaccine 24:1238–41 [Google Scholar]
  62. Clements DE, Coller BA, Lieberman MM, Ogata S, Wang G. 62.  et al. 2010. Development of a recombinant tetravalent dengue virus vaccine: immunogenicity and efficacy studies in mice and monkeys. Vaccine 28:2705–15 [Google Scholar]
  63. Danko JR, Beckett CG, Porter KR. 63.  2011. Development of dengue DNA vaccines. Vaccine 29:7261–66 [Google Scholar]
  64. Kochel T, Wu SJ, Raviprakash K, Hobart P, Hoffman S. 64.  et al. 1997. Inoculation of plasmids expressing the dengue-2 envelope gene elicit neutralizing antibodies in mice. Vaccine 15:547–52 [Google Scholar]
  65. Porter KR, Kochel TJ, Wu SJ, Raviprakash K, Phillips I, Hayes CG. 65.  1998. Protective efficacy of a dengue 2 DNA vaccine in mice and the effect of CpG immuno-stimulatory motifs on antibody responses. Arch. Virol. 143:997–1003 [Google Scholar]
  66. Konishi E, Yamaoka M, Kurane I, Mason PW. 66.  2000. A DNA vaccine expressing dengue type 2 virus premembrane and envelope genes induces neutralizing antibody and memory B cells in mice. Vaccine 18:1133–39 [Google Scholar]
  67. Ferlenghi I, Clarke M, Ruttan T, Allison SL, Schalich J. 67.  et al. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593–602 [Google Scholar]
  68. Hughes HR, Crill WD, Chang GJ. 68.  2012. Manipulation of immunodominant dengue virus E protein epitopes reduces potential antibody-dependent enhancement. Virol. J. 9:115 [Google Scholar]
  69. Beckett CG, Tjaden J, Burgess T, Danko JR, Tamminga C. 69.  et al. 2011. Evaluation of a prototype dengue-1 DNA vaccine in a phase 1 clinical trial. Vaccine 29:960–68 [Google Scholar]
  70. Pierson TC, Diamond MS. 70.  2013. Flaviviruses. Fields Virology DM Knipe, PM Howley 747–94 Philadelphia: Lippincott Williams & Wilkins, 6th ed.. [Google Scholar]
  71. Pierson TC, Fremont DH, Kuhn RJ, Diamond MS. 71.  2008. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4:229–38 [Google Scholar]
  72. Rico-Hesse R. 72.  1990. Molecular evolution and distribution of dengue viruses type 1 and 2 in nature. Virology 174:479–93 [Google Scholar]
  73. Holmes EC, Twiddy SS. 73.  2003. The origin, emergence and evolutionary genetics of dengue virus. Infect. Genet. Evol. 3:19–28 [Google Scholar]
  74. Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S. 74.  et al. 2010. Genotype specific neutralization and protection by antibodies against dengue virus type 3. J. Virol. 84:10630–43 [Google Scholar]
  75. Wahala WM, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, de Silva AM. 75.  2010. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog. 6:e1000821 [Google Scholar]
  76. Cherrier MV, Kaufmann B, Nybakken GE, Lok SM, Warren JT. 76.  et al. 2009. Structural basis for the preferential binding of immature flaviviruses by a fusion-loop specific antibody. EMBO J. 28:3269–76 [Google Scholar]
  77. Junjhon J, Edwards TJ, Utaipat U, Bowman VD, Holdaway HA. 77.  et al. 2010. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J. Virol. 84:8353–58 [Google Scholar]
  78. Pierson TC, Diamond MS. 78.  2012. Degrees of maturity: the complex structure and biology of flaviviruses. Curr. Opin. Virol. 2:168–75 [Google Scholar]
  79. Mukherjee S, Lin TY, Dowd KA, Manhart CJ, Pierson TC. 79.  2011. The infectivity of prM-containing partially mature West Nile virus does not require the activity of cellular furin-like proteases. J. Virol. 85:12067–72 [Google Scholar]
  80. Boehr DD, Wright PE. 80.  2008. How do proteins interact?. Science 320:1429–30 [Google Scholar]
  81. Mateu MG. 81.  2013. Assembly, stability and dynamics of virus capsids. Arch. Biochem. Biophys. 531:65–79 [Google Scholar]
  82. Lewis JK, Bothner B, Smith TJ, Siuzdak G. 82.  1998. Antiviral agent blocks breathing of the common cold virus. Proc. Natl. Acad. Sci. USA 95:6774–78 [Google Scholar]
  83. Austin SK, Dowd KA, Shrestha B, Nelson CA, Edeling MA. 83.  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]
  84. Cockburn JJ, Navarro Sanchez ME, Fretes N, Urvoas A, Staropoli I. 84.  et al. 2012. Mechanism of dengue virus broad cross-neutralization by a monoclonal antibody. Structure 20:303–14 [Google Scholar]
  85. Lok SM, Kostyuchenko V, Nybakken GE, Holdaway HA, Battisti AJ. 85.  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]
  86. Dowd KA, Jost CA, Durbin AP, Whitehead SS, Pierson TC. 86.  2011. A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLoS Pathog. 7:e1002111 [Google Scholar]
  87. Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, Rossmann MG. 87.  2013. Dengue structure differs at the temperatures of its human and mosquito hosts. Proc. Natl. Acad. Sci. USA 110:6795–99 [Google Scholar]
  88. Fibriansah G, Ng TS, Kostyuchenko VA, Lee J, Lee S. 88.  et al. 2013. Structural changes of dengue virus when exposed to 37°C. J. Virol. 87:7585–92 [Google Scholar]
  89. Bothner B, Dong XF, Bibbs L, Johnson JE, Siuzdak G. 89.  1998. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J. Biol. Chem. 273:673–76 [Google Scholar]
  90. Katpally U, Fu TM, Freed DC, Casimiro DR, Smith TJ. 90.  2009. Antibodies to the buried N terminus of rhinovirus VP4 exhibit cross-serotypic neutralization. J. Virol. 83:7040–48 [Google Scholar]
  91. Mukherjee S, Dowd KA, Manhart CJ, Ledgerwood JE, Durbin AP. 91.  et al. 2014. The mechanism and significance of cell type–dependent neutralization of flaviviruses. J. Virol. In press. doi: 10.1128/JVI.03690-13
  92. Morens DM. 92.  1994. Antibody-dependent enhancement of infection and the pathogenesis of viral disease. Clin. Infect. Dis. 19:500–12 [Google Scholar]
  93. Guzman MG, Alvarez M, Halstead SB. 93.  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]
  94. Sun P, Bauza K, Pal S, Liang Z, Wu SJ. 94.  et al. 2011. Infection and activation of human peripheral blood monocytes by dengue viruses through the mechanism of antibody-dependent enhancement. Virology 421:245–52 [Google Scholar]
  95. Kou Z, Lim JY, Beltramello M, Quinn M, Chen H. 95.  et al. 2011. Human antibodies against dengue enhance dengue viral infectivity without suppressing type I interferon secretion in primary human monocytes. Virology 410:240–47 [Google Scholar]
  96. Pierson TC, Xu Q, Nelson S, Oliphant T, Nybakken GE. 96.  et al. 2007. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1:135–45 [Google Scholar]
  97. Moi ML, Lim CK, Chua KB, Takasaki T, Kurane I. 97.  2012. Dengue virus infection-enhancing activity in serum samples with neutralizing activity as determined by using FcγR-expressing cells. PLoS Negl. Trop. Dis. 6:e1536 [Google Scholar]
  98. Rodrigo WW, Jin X, Blackley SD, Rose RC, Schlesinger JJ. 98.  2006. Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human FcγRIA (CD64) or FcγRIIA (CD32). J. Virol. 80:10128–38 [Google Scholar]
  99. Rodrigo WW, Block OK, Lane C, Sukupolvi-Petty S, Goncalvez AP. 99.  et al. 2009. Dengue virus neutralization is modulated by IgG antibody subclass and Fcγ receptor subtype. Virology 394:175–82 [Google Scholar]
  100. Chawla T, Chan KR, Zhang SL, Tan HC, Lim AP. 100.  et al. 2013. Dengue virus neutralization in cells expressing Fcγ receptors. PLoS ONE 8:e65231 [Google Scholar]
  101. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S. 101.  et al. 2010. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328:745–48 [Google Scholar]
  102. Beltramello M, Williams KL, Simmons CP, Macagno A, Simonelli L. 102.  et al. 2010. The human immune response to dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8:271–83 [Google Scholar]
  103. Tassaneetrithep B, Burgess T, Granelli-Piperno A, Trumpfheller C, Finke J. 103.  et al. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823–29 [Google Scholar]
  104. Kraus AA, Messer W, Haymore LB, de Silva AM. 104.  2007. Comparison of plaque- and flow cytometry–based methods for measuring dengue virus neutralization. J. Clin. Microbiol. 45:3777–80 [Google Scholar]
  105. Nimmerjahn F, Ravetch JV. 105.  2011. FcγRs in health and disease. Curr. Top. Microbiol. Immunol. 350:105–25 [Google Scholar]
  106. Schlesinger JJ, Foltzer M, Chapman S. 106.  1993. The Fc portion of antibody to yellow fever virus NS1 is a determinant of protection against YF encephalitis in mice. Virology 192:132–41 [Google Scholar]
  107. Mehlhop E, Ansarah-Sobrinho C, Johnson S, Engle M, Fremont DH. 107.  et al. 2007. Complement protein C1q inhibits antibody-dependent enhancement of flavivirus infection in an IgG subclass-specific manner. Cell Host Microbe 2:417–26 [Google Scholar]
  108. Mehlhop E, Nelson S, Jost CA, Gorlatov S, Johnson S. 108.  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]
  109. Oliphant T, Engle M, Nybakken G, Doane C, Johnson S. 109.  et al. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 11:522–30 [Google Scholar]
  110. Vogt MR, Dowd KA, Engle M, Tesh RB, Johnson S. 110.  et al. 2011. Poorly neutralizing cross-reactive antibodies against the fusion loop of West Nile virus envelope protein protect in vivo via Fc-γ receptor and complement-dependent effector mechanisms. J. Virol. 22:11567–80 [Google Scholar]
  111. Chung KM, Thompson BS, Fremont DH, Diamond MS. 111.  2007. Antibody recognition of cell surface–associated NS1 triggers Fc-γ receptor mediated phagocytosis and clearance of WNV infected cells. J. Virol. 81:9551–55 [Google Scholar]
  112. Yamanaka A, Kosugi S, Konishi E. 112.  2008. Infection-enhancing and -neutralizing activities of mouse monoclonal antibodies against dengue type 2 and 4 viruses are controlled by complement levels. J. Virol. 82:927–37 [Google Scholar]
  113. Laoprasopwattana K, Libraty DH, Endy TP, Nisalak A, Chunsuttiwat S. 113.  et al. 2007. Antibody-dependent cellular cytotoxicity mediated by plasma obtained before secondary dengue virus infections: potential involvement in early control of viral replication. J. Infect. Dis. 195:1108–16 [Google Scholar]
  114. Flamand M, Megret F, Mathieu M, Lepault J, Rey FA, Deubel V. 114.  1999. Dengue virus type 1 nonstructural glycoprotein NS1 is secreted from mammalian cells as a soluble hexamer in a glycosylation-dependent fashion. J. Virol. 73:6104–10 [Google Scholar]
  115. Alcon S, Talarmin A, Debruyne M, Falconar A, Deubel V, Flamand M. 115.  2002. Enzyme-linked immunosorbent assay specific to dengue virus type 1 nonstructural protein NS1 reveals circulation of the antigen in the blood during the acute phase of disease in patients experiencing primary or secondary infections. J. Clin. Microbiol. 40:376–81 [Google Scholar]
  116. Libraty DH, Young PR, Pickering D, Endy TP, Kalayanarooj S. 116.  et al. 2002. High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J. Infect. Dis. 186:1165–68 [Google Scholar]
  117. Young PR, Hilditch PA, Bletchly C, Halloran W. 117.  2000. An antigen capture enzyme-linked immunosorbent assay reveals high levels of the dengue virus protein NS1 in the sera of infected patients. J. Clin. Microbiol. 38:1053–57 [Google Scholar]
  118. Despres P, Dietrich J, Girard M, Bouloy M. 118.  1991. Recombinant baculoviruses expressing yellow fever virus E and NS1 proteins elicit protective immunity in mice. J. Gen. Virol. 72:2811–16 [Google Scholar]
  119. Schlesinger JJ, Brandriss MW, Cropp CB, Monath TP. 119.  1986. Protection against yellow fever in monkeys by immunization with yellow fever virus nonstructural protein NS1. J. Virol. 60:1153–55 [Google Scholar]
  120. Putnak JR, Schlesinger JJ. 120.  1990. Protection of mice against yellow fever virus encephalitis by immunization with a vaccinia virus recombinant encoding the yellow fever virus non-structural proteins, NS1, NS2a and NS2b. J. Gen. Virol. 71:1697–702 [Google Scholar]
  121. Henchal EA, Henchal LS, Schlesinger JJ. 121.  1988. Synergistic interactions of anti-NS1 monoclonal antibodies protect passively immunized mice from lethal challenge with dengue 2 virus. J. Gen. Virol. 69:2101–7 [Google Scholar]
  122. Falgout B, Bray M, Schlesinger JJ, Lai CJ. 122.  1990. Immunization of mice with recombinant vaccinia virus expressing authentic dengue virus nonstructural protein NS1 protects against lethal dengue virus encephalitis. J. Virol. 64:4356–63 [Google Scholar]
  123. Chung KM, Nybakken GE, Thompson BS, Engle MJ, Marri A. 123.  et al. 2006. Antibodies against West Nile virus non-structural (NS)-1 protein prevent lethal infection through Fcγ receptor–dependent and independent mechanisms. J. Virol. 80:1340–51 [Google Scholar]
  124. Akey DL, Brown WC, Dutta S, Konwerski J, Jose J. 124.  et al. 2014. Flavivirus NS1 structures reveal surfaces for associations with membranes and the immune system. Science 343:881–85 [Google Scholar]
  125. Edeling MA, Diamond MS, Fremont DH. 125.  2014. Structural basis of flavivirus NS1 assembly and antibody recognition. Proc. Natl. Acad. Sci. USA 111:4285–90 [Google Scholar]
  126. Radbruch A, Muehlinghaus G, Luger EO, Inamine A, Smith KG. 126.  et al. 2006. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat. Rev. Immunol. 6:741–50 [Google Scholar]
  127. Good-Jacobson KL, Shlomchik MJ. 127.  2010. Plasticity and heterogeneity in the generation of memory B cells and long-lived plasma cells: the influence of germinal center interactions and dynamics. J. Immunol. 185:3117–25 [Google Scholar]
  128. Luther SA, Maillard I, Luthi F, Scarpellino L, Diggelmann H, Acha-Orbea H. 128.  1997. Early neutralizing antibody response against mouse mammary tumor virus: critical role of viral infection and superantigen-reactive T cells. J. Immunol. 159:2807–14 [Google Scholar]
  129. Diamond MS, Sitati E, Friend L, Shrestha B, Higgs S, Engle M. 129.  2003. A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 198:1853–62 [Google Scholar]
  130. Wrammert J, Onlamoon N, Akondy RS, Perng GC, Polsrila K. 130.  et al. 2012. Rapid and massive virus-specific plasmablast responses during acute dengue virus infection in humans. J. Virol. 86:2911–18 [Google Scholar]
  131. Zompi S, Montoya M, Pohl MO, Balmaseda A, Harris E. 131.  2012. Dominant cross-reactive B cell response during secondary acute dengue virus infection in humans. PLoS Negl. Trop. Dis. 6:e1568 [Google Scholar]
  132. Finke D, Baribaud F, Diggelmann H, Acha-Orbea H. 132.  2001. Extrafollicular plasmablast B cells play a key role in carrying retroviral infection to peripheral organs. J. Immunol. 166:6266–75 [Google Scholar]
  133. Jacob J, Kelsoe G, Rajewsky K, Weiss U. 133.  1991. Intraclonal generation of antibody mutants in germinal centres. Nature 354:389–92 [Google Scholar]
  134. Manz RA, Thiel A, Radbruch A. 134.  1997. Lifetime of plasma cells in the bone marrow. Nature 388:133–34 [Google Scholar]
  135. Slifka MK, Matloubian M, Ahmed R. 135.  1995. Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 69:1895–902 [Google Scholar]
  136. Slifka MK, Antia R, Whitmire JK, Ahmed R. 136.  1998. Humoral immunity due to long-lived plasma cells. Immunity 8:363–72 [Google Scholar]
  137. Balakrishnan T, Bela-Ong DB, Toh YX, Flamand M, Devi S. 137.  et al. 2011. Dengue virus activates polyreactive, natural IgG B cells after primary and secondary infection. PLoS ONE 6:e29430 [Google Scholar]
  138. Wahala WM, Silva AM. 138.  2011. The human antibody response to dengue virus infection. Viruses 3:2374–95 [Google Scholar]
  139. Chan KR, Zhang SL, Tan HC, Chan YK, Chow A. 139.  et al. 2011. Ligation of Fcγ receptor IIB inhibits antibody-dependent enhancement of dengue virus infection. Proc. Natl. Acad. Sci. USA 108:12479–84 [Google Scholar]
  140. Imrie A, Meeks J, Gurary A, Sukhbaatar M, Truong TT. 140.  et al. 2007. Antibody to dengue 1 detected more than 60 years after infection. Viral Immunol. 20:672–75 [Google Scholar]
  141. Purtha WE, Tedder TF, Johnson S, Bhattacharya D, Diamond MS. 141.  2011. Memory B cells but not long-lived plasma cells possess antigen specificities for viral escape mutants. J. Exp. Med. 208:2599–606 [Google Scholar]
  142. Halstead SB. 142.  2013. Identifying protective dengue vaccines: guide to mastering an empirical process. Vaccine 31:4501–7 [Google Scholar]
  143. Yauch LE, Prestwood TR, May MM, Morar MM, Zellweger RM. 143.  et al. 2010. CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J. Immunol. 185:5405–16 [Google Scholar]
  144. Yauch LE, Zellweger RM, Kotturi MF, Qutubuddin A, Sidney J. 144.  et al. 2009. A protective role for dengue virus-specific CD8+ T cells. J. Immunol. 182:4865–73 [Google Scholar]
  145. An J, Zhou DS, Zhang JL, Morida H, Wang JL, Yasui K. 145.  2004. Dengue-specific CD8+ T cells have both protective and pathogenic roles in dengue virus infection. Immunol. Lett. 95:167–74 [Google Scholar]
  146. Gil L, Lopez C, Lazo L, Valdes I, Marcos E. 146.  et al. 2009. Recombinant nucleocapsid-like particles from dengue-2 virus induce protective CD4+ and CD8+ cells against viral encephalitis in mice. Int. Immunol. 21:1175–83 [Google Scholar]
  147. Lazo L, Gil L, Lopez C, Valdes I, Marcos E. 147.  et al. 2010. Nucleocapsid-like particles of dengue-2 virus enhance the immune response against a recombinant protein of dengue-4 virus. Arch. Virol. 155:1587–95 [Google Scholar]
  148. Gunther VJ, Putnak R, Eckels KH, Mammen MP, Scherer JM. 148.  et al. 2011. A human challenge model for dengue infection reveals a possible protective role for sustained interferon γ levels during the acute phase of illness. Vaccine 29:3895–904 [Google Scholar]
  149. Duangchinda T, Dejnirattisai W, Vasanawathana S, Limpitikul W, Tangthawornchaikul N. 149.  et al. 2010. Immunodominant T-cell responses to dengue virus NS3 are associated with DHF. Proc. Natl. Acad. Sci. USA 107:16922–27 [Google Scholar]
  150. Weiskopf D, Angelo MA, de Azeredo EL, Sidney J, Greenbaum JA. 150.  et al. 2013. Comprehensive analysis of dengue virus–specific responses supports an HLA-linked protective role for CD8+ T cells. Proc. Natl. Acad. Sci. USA 110:E2046–53 [Google Scholar]
  151. Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N. 151.  et al. 2003. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat. Med. 9:921–27 [Google Scholar]
  152. Rothman AL. 152.  2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11:532–43 [Google Scholar]
  153. Dung NT, Duyen HT, Thuy NT, Ngoc TV, Chau NV. 153.  et al. 2010. Timing of CD8+ T cell responses in relation to commencement of capillary leakage in children with dengue. J. Immunol. 184:7281–87 [Google Scholar]
  154. Friberg H, Bashyam H, Toyosaki-Maeda T, Potts JA, Greenough T. 154.  et al. 2011. Cross-reactivity and expansion of dengue-specific T cells during acute primary and secondary infections in humans. Sci. Rep. 1:51 [Google Scholar]
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