Paradoxical role of antibodies in dengue virus infections: considerations for prophylactic vaccine development

References

• Guzman A, Isturiz RE. Update on the global spread of dengue. Int J Antimicrob Agents. 2010;36(Suppl 1):S40–2.
   PubMed Web of Science ®Google Scholar
• Guzman MG, Harris E. Dengue. Lancet. 2015;385:453–465.
   PubMed Web of Science ®Google Scholar
• Bhatt S, Gething PW, Brady OJ, et al. The global distribution and burden of dengue. Nature. 2013;496:504–507.
   PubMed Web of Science ®Google Scholar
• Holmes EC, Twiddy SS. The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol. 2003;3:19–28.
   PubMed Web of Science ®Google Scholar
• Chen R, Vasilakis N. Dengue–quo tu et quo vadis? Viruses. 2011;3:1562–1608.
   PubMed Web of Science ®Google Scholar
• Jessie K, Fong MY, Devi S, et al. Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis. 2004;189:1411–1418.
   PubMed Web of Science ®Google Scholar
• Balsitis SJ, Coloma J. Castro G et al. Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. Am J Trop Med Hyg. 2009;80:416–424.
   PubMed Web of Science ®Google Scholar
• Durbin AP, Vargas MJ, Wanionek K, et al. Phenotyping of peripheral blood mononuclear cells during acute dengue illness demonstrates infection and increased activation of monocytes in severe cases compared to classic dengue fever. Virology. 2008;376:429–435.
   PubMed Web of Science ®Google Scholar
• Wu SJ, Grouard-Vogel G, Sun W, et al. Human skin Langerhans cells are targets of dengue virus infection. Nat Med. 2000;6:816–820.
   PubMed Web of Science ®Google Scholar
• Cohen SN, Halstead SB. Shock associated with dengue infection. I. Clinical and physiologic manifestations of dengue hemorrhagic fever in Thailand, 1964. J Pediatr. 1966;68:448–456.
   PubMed Web of Science ®Google Scholar
• Green S, Vaughn DW, Kalayanarooj S, et al. Elevated plasma interleukin-10 levels in acute dengue correlate with disease severity. J Med Virol. 1999;59:329–334.
   PubMed Web of Science ®Google Scholar
• Vaughn DW, Green S, Kalayanarooj S, et al. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis. 2000;181:2–9.
   PubMed Web of Science ®Google Scholar
• Libraty DH, Endy TP, Houng HS, et al. Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis. 2002;185:1213–1221.
   PubMed Web of Science ®Google Scholar
• Guzman MG, Alvarez M, Halstead SB. 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. 2013;158:1445–1459.
   PubMed Web of Science ®Google Scholar
• Kuhn RJ, Zhang W, Rossmann MG, et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell. 2002;108:717–725.
   PubMed Web of Science ®Google Scholar
• Johnson AJ, Guirakhoo F, Roehrig JT. The envelope glycoproteins of dengue 1 and dengue 2 viruses grown in mosquito cells differ in their utilization of potential glycosylation sites. Virology. 1994;203:241–249.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay S, Kuhn RJ, Rossmann MG. A structural perspective of the flavivirus life cycle. Nat Rev Microbiol. 2005;3:13–22.
   PubMed Web of Science ®Google Scholar
• Modis Y, Ogata S, Clements D, et al. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci USA. 2003;100:6986–6991.
   PubMed Web of Science ®Google Scholar
• Chin JF, Chu JJ, Ng ML. The envelope glycoprotein domain III of dengue virus serotypes 1 and 2 inhibit virus entry. Microbes Infect. 2007;9:1–6.
   PubMed Web of Science ®Google Scholar
• Hung JJ, Hsieh MT, Young MJ, et al. An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells. J Virol. 2004;78:378–388.
   PubMed Web of Science ®Google Scholar
• Watterson D, Kobe B, Young PR. Residues in domain III of the dengue virus envelope glycoprotein involved in cell-surface glycosaminoglycan binding. J Gen Virol. 2012;93:72–82.
   PubMed Web of Science ®Google Scholar
• Bhardwaj S, Holbrook M, Shope RE, et al. Biophysical characterization and vector-specific antagonist activity of domain III of the tick-borne flavivirus envelope protein. J Virol. 2001;75:4002–4007.
   PubMed Web of Science ®Google Scholar
• Chu JJ, Rajamanonmani R, Li J, et al. Inhibition of West Nile virus entry by using a recombinant domain III from the envelope glycoprotein. J Gen Virol. 2005;86:405–412.
   PubMed Web of Science ®Google Scholar
• Modis Y, Ogata S, Clements D, et al. Structure of the dengue virus envelope protein after membrane fusion. Nature. 2004;427:313–319.
   PubMed Web of Science ®Google Scholar
• Zhang X, Sheng J, Austin SK, et al. Structure of acidic pH dengue virus showing the fusogenic glycoprotein trimers. J Virol. 2015;89:743–750.
   PubMed Web of Science ®Google Scholar
• Acosta EG, Kumar A, Bartenschlager R. Revisiting dengue virus-host cell interaction: new insights into molecular and cellular virology. Adv Virus Res. 2014;88:1–109.
   PubMed Web of Science ®Google Scholar
• Young PR, Hilditch PA, Bletchly C, et al. 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. 2000;38:1053–1057.
   PubMed Web of Science ®Google Scholar
• Libraty DH, Young PR, Pickering D, et al. 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. 2002;186:1165–1168.
   PubMed Web of Science ®Google Scholar
• Gutsche I, Coulibaly F, Voss JE, et al. Secreted dengue virus nonstructural protein NS1 is an atypical barrel-shaped high-density lipoprotein. Proc Natl Acad Sci USA. 2011;108:8003–8008.
   PubMed Web of Science ®Google Scholar
• Chatel-Chaix L, Bartenschlager R. Dengue virus- and hepatitis C virus-induced replication and assembly compartments: the enemy inside–caught in the web. J Virol. 2014;88:5907–5911.
   PubMed Web of Science ®Google Scholar
• Welsch S, Miller S, Romero-Brey I, et al. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe. 2009;5:365–375.
   PubMed Web of Science ®Google Scholar
• Junjhon J, Pennington JG, Edwards TJ, et al. Ultrastructural characterization and three-dimensional architecture of replication sites in dengue virus-infected mosquito cells. J Virol. 2014;88:4687–4697.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Corver J, Chipman PR, et al. Structures of immature flavivirus particles. Embo J. 2003;22:2604–2613.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Kaufmann B, Chipman PR, et al. Structure of immature West Nile virus. J Virol. 2007;81:6141–6145.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Hunke C, Yau YH, et al. The stem region of premembrane protein plays an important role in the virus surface protein rearrangement during dengue maturation. J Biol Chem. 2012;287:40525–40534.
   PubMed Web of Science ®Google Scholar
• Yu IM, Zhang W, Holdaway HA, et al. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science. 2008;319:1834–1837.
   PubMed Web of Science ®Google Scholar
• Zheng A, Yuan F, Kleinfelter LM, et al. A toggle switch controls the low pH-triggered rearrangement and maturation of the dengue virus envelope proteins. Nat Commun. 2014;5:3877.
   PubMed Web of Science ®Google Scholar
• Zybert IA, van der Ende-Metselaar H, Wilschut J, et al. Functional importance of dengue virus maturation: infectious properties of immature virions. J Gen Virol. 2008;89:3047–3051.
   PubMed Web of Science ®Google Scholar
• Yu IM, Holdaway HA, Chipman PR, et al. Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. J Virol. 2009;83:12101–12107.
   PubMed Web of Science ®Google Scholar
• Fibriansah G, Ng TS, Kostyuchenko VA, et al. Structural changes in dengue virus when exposed to a temperature of 37 degrees C. J Virol. 2013;87:7585–7592.
   PubMed Web of Science ®Google Scholar
• Zhang X, Sheng J, Plevka P, et al. Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci USA. 2013;110:6795–6799.
   PubMed Web of Science ®Google Scholar
• Kostyuchenko VA, Chew PL, Ng TS, et al. Near-atomic resolution cryo-electron microscopic structure of dengue serotype 4 virus. J Virol. 2014;88:477–482.
   PubMed Web of Science ®Google Scholar
• Junjhon J, Edwards TJ, Utaipat U, et al. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J Virol. 2010;84:8353–8358.
   PubMed Web of Science ®Google Scholar
• Cardosa MJ, Wang SM, Sum MS, et al. Antibodies against prM protein distinguish between previous infection with dengue and Japanese encephalitis viruses. BMC Microbiol. 2002;2:9.
   PubMed Web of Science ®Google Scholar
• Se-Thoe SY, Ng MM, Ling AE. Retrospective study of Western blot profiles in immune sera of natural dengue virus infections. J Med Virol. 1999;57:322–330.
   PubMed Web of Science ®Google Scholar
• Dejnirattisai W, Jumnainsong A, Onsirisakul N, et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science. 2010;328:745–748.
   PubMed Web of Science ®Google Scholar
• van der Schaar HM, Rust MJ, Waarts BL, et al. Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J Virol. 2007;81:12019–12028.
   PubMed Web of Science ®Google Scholar
• Junjhon J, Lausumpao M, Supasa S, et al. Differential modulation of prM cleavage, extracellular particle distribution, and virus infectivity by conserved residues at nonfurin consensus positions of the dengue virus pr-M junction. J Virol. 2008;82:10776–10791.
   PubMed Web of Science ®Google Scholar
• Plevka P, Battisti AJ, Junjhon J, et al. Maturation of flaviviruses starts from one or more icosahedrally independent nucleation centres. EMBO Rep. 2011;12:602–606.
   PubMed Web of Science ®Google Scholar
• Halstead SB. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res. 2003;60:421–467.
   PubMed Web of Science ®Google Scholar
• Sangkawibha N, Rojanasuphot S, Ahandrik S, et al. Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol. 1984;120:653–669.
   PubMed Web of Science ®Google Scholar
• Halstead SB, O’Rourke EJ. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med. 1977;146:201–217.
   PubMed Web of Science ®Google Scholar
• Kliks SC, Nimmanitya S, Nisalak A, et al. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg. 1988;38:411–419.
   PubMed Web of Science ®Google Scholar
• Kliks SC, Nisalak A, Brandt WE, et al. Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg. 1989;40:444–451.
   PubMed Web of Science ®Google Scholar
• Goncalvez AP, Engle RE, St Claire M, et al. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA. 2007;104:9422–9427.
   PubMed Web of Science ®Google Scholar
• Halstead SB. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis. 1979;140:527–533.
   PubMed Web of Science ®Google Scholar
• Balsitis SJ, Williams KL, Lachica R, et al. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 2010;6:e1000790.
   PubMed Web of Science ®Google Scholar
• Zellweger RM, Prestwood TR, Shresta S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe. 2010;7:128–139.
   PubMed Web of Science ®Google Scholar
• de Alwis R, Williams KL, Schmid MA, et al. Dengue viruses are enhanced by distinct populations of serotype cross-reactive antibodies in human immune sera. PLoS Pathog. 2014;10:e1004386.
   PubMed Web of Science ®Google Scholar
• Ng JK, Zhang SL, Tan HC, et al. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog. 2014;10:e1004031.
   PubMed Web of Science ®Google Scholar
• Boonnak K, Slike BM, Burgess TH, et al. Role of dendritic cells in antibody-dependent enhancement of dengue virus infection. J Virol. 2008;82:3939–3951.
   PubMed Web of Science ®Google Scholar
• Rodenhuis-Zybert IA, Van Der Schaar HM, Da Silva Voorham JM, et al. Immature dengue virus: a veiled pathogen? PLoS Pathog. 2010;6:e1000718.
   PubMed Web of Science ®Google Scholar
• Chan KR, Zhang SL, Tan HC, et al. Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection. Proc Natl Acad Sci USA. 2011;108:12479–12484.
   PubMed Web of Science ®Google Scholar
• Rodenhuis-Zybert IA, Moesker B, Da Silva Voorham JM, et al. A fusion-loop antibody enhances the infectious properties of immature flavivirus particles. J Virol. 2011;85:11800–11808.
   PubMed Web of Science ®Google Scholar
• Moi ML, Lim CK, Kotaki A, et al. Development of an antibody-dependent enhancement assay for dengue virus using stable BHK-21 cell lines expressing Fc gammaRIIA. J Virol Methods. 2010;163:205–209.
   PubMed Web of Science ®Google Scholar
• Rodrigo WW, Jin X, Blackley SD, et al. Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human Fcgamma RIA (CD64) or FcgammaRIIA (CD32). J Virol. 2006;80:10128–10138.
   PubMed Web of Science ®Google Scholar
• Boonnak K, Slike BM, Donofrio GC, et al. Human FcgammaRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J Immunol. 2013;190:5659–5665.
   PubMed Web of Science ®Google Scholar
• Moi ML, Lim CK, Takasaki T, et al. Involvement of the Fc gamma receptor IIA cytoplasmic domain in antibody-dependent enhancement of dengue virus infection. J Gen Virol. 2010;91:103–111.
   PubMed Web of Science ®Google Scholar
• Perera-Lecoin M, Meertens L, Carnec X, et al. Flavivirus entry receptors: an update. Viruses. 2014;6:69–88.
   Web of Science ®Google Scholar
• Navarro-Sanchez E, Altmeyer R, Amara A, et al. 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. 2003;4:723–728.
   PubMed Web of Science ®Google Scholar
• Lozach PY, Burleigh L, Staropoli I, et al. 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. 2005;280:23698–23708.
   PubMed Web of Science ®Google Scholar
• Cruz-Oliveira C, Freire JM, Conceicao TM, et al. Receptors and routes of dengue virus entry into the host cells. FEMS Microbiol Rev. 2015;39:155–170.
   PubMed Web of Science ®Google Scholar
• Mercer J, Helenius A. Gulping rather than sipping: macropinocytosis as a way of virus entry. Curr Opin Microbiol. 2012;15:490–499.
   PubMed Web of Science ®Google Scholar
• Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis. Annu Rev Biochem. 2010;79:803–833.
   PubMed Web of Science ®Google Scholar
• Acosta EG, Castilla V, Damonte EB. Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. J Gen Virol. 2008;89:474–484.
   PubMed Web of Science ®Google Scholar
• Acosta EG, Castilla V, Damonte EB. Infectious dengue-1 virus entry into mosquito C6/36 cells. Virus Res. 2011;160:173–179.
   PubMed Web of Science ®Google Scholar
• Mosso C, Galvan-Mendoza IJ, Ludert JE, et al. Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT. Virology. 2008;378:193–199.
   PubMed Web of Science ®Google Scholar
• Krishnan MN, Sukumaran B, Pal U, et al. Rab 5 is required for the cellular entry of dengue and West Nile viruses. J Virol. 2007;81:4881–4885.
   PubMed Web of Science ®Google Scholar
• Van Der Schaar HM, Rust MJ, Chen C,et al. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells.PLoS Pathog.2008;4:e1000244.
   PubMed Web of Science ®Google Scholar
• Ang F, Wong AP, Ng MM, et al. Small interference RNA profiling reveals the essential role of human membrane trafficking genes in mediating the infectious entry of dengue virus. Virol J. 2010;7:24.
   PubMed Web of Science ®Google Scholar
• Acosta EG, Castilla V, Damonte EB. Alternative infectious entry pathways for dengue virus serotypes into mammalian cells. Cell Microbiol. 2009;11:1533–1549.
   PubMed Web of Science ®Google Scholar
• Acosta EG, Piccini LE, Talarico LB, et al. Changes in antiviral susceptibility to entry inhibitors and endocytic uptake of dengue-2 virus serially passaged in Vero or C6/36 cells. Virus Res. 2014;184:39–43.
   PubMed Web of Science ®Google Scholar
• Zaitseva E, Yang ST, Melikov K, et al. Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog. 2010;6:e1001131.
   PubMed Web of Science ®Google Scholar
• Acosta EG, Castilla V, Damonte EB. Differential requirements in endocytic trafficking for penetration of dengue virus. PLoS One. 2012;7:e44835.
   PubMed Web of Science ®Google Scholar
• Littaua R, Kurane I, Ennis FA. Human IgG Fc receptor II mediates antibody-dependent enhancement of dengue virus infection. J Immunol. 1990;144:3183–3186.
   PubMed Web of Science ®Google Scholar
• Gollins SW, Porterfield JS. Flavivirus infection enhancement in macrophages: an electron microscopic study of viral cellular entry. J Gen Virol. 1985;66(Pt 9):1969–1982.
   PubMed Web of Science ®Google Scholar
• Tse SM, Furuya W, Gold E, et al. Differential role of actin, clathrin, and dynamin in Fc gamma receptor-mediated endocytosis and phagocytosis. J Biol Chem. 2003;278:3331–3338.
   PubMed Web of Science ®Google Scholar
• Da Silva Voorham JM, Rodenhuis-Zybert IA, Ayala Nunez NV, et al. Antibodies against the envelope glycoprotein promote infectivity of immature dengue virus serotype 2. PLoS One. 2012;7:e29957.
   PubMed Web of Science ®Google Scholar
• Ubol S, Halstead SB. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin Vaccine Immunol. 2010;17:1829–1835.
   PubMed Web of Science ®Google Scholar
• Halstead SB, Mahalingam S, Marovich MA, et al. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis. 2010;10:712–722.
   PubMed Web of Science ®Google Scholar
• Ubol S, Phuklia W, Kalayanarooj S, et al. Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis. 2010;201:923–935.
   PubMed Web of Science ®Google Scholar
• Modhiran N, Kalayanarooj S, Ubol S. Subversion of innate defenses by the interplay between DENV and pre-existing enhancing antibodies: TLRs signaling collapse. PLoS Negl Trop Dis. 2010;4:e924.
   PubMed Web of Science ®Google Scholar
• Chareonsirisuthigul T, Kalayanarooj S, Ubol S. Dengue virus (DENV) antibody-dependent enhancement of infection upregulates the production of anti-inflammatory cytokines, but suppresses anti-DENV free radical and pro-inflammatory cytokine production, in THP-1 cells. J Gen Virol. 2007;88:365–375.
   PubMed Web of Science ®Google Scholar
• Chan KR, Ong EZ, Tan HC, et al. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA. 2014;111:2722–2727.
   PubMed Web of Science ®Google Scholar
• Nybakken GE, Oliphant T, Johnson S, et al. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature. 2005;437:764–769.
   PubMed Web of Science ®Google Scholar
• Sukupolvi-Petty S, Austin SK, Purtha WE, et al. Type- and subcomplex-specific neutralizing antibodies against domain III of dengue virus type 2 envelope protein recognize adjacent epitopes. J Virol. 2007;81:12816–12826.
   PubMed Web of Science ®Google Scholar
• Hughes HR, Crill WD, Chang GJ. Manipulation of immunodominant dengue virus E protein epitopes reduces potential antibody-dependent enhancement. Virol J. 2012;9:115.
   PubMed Web of Science ®Google Scholar
• Tang CT, Li PC, Liu IJ, et al. An epitope-substituted DNA vaccine improves safety and immunogenicity against dengue virus type 2. PLoS Negl Trop Dis. 2015;9:e0003903.
   Web of Science ®Google Scholar
• Morens DM, Halstead SB. Measurement of antibody-dependent infection enhancement of four dengue virus serotypes by monoclonal and polyclonal antibodies. J Gen Virol. 1990;71(Pt 12):2909–2914.
   PubMed Web of Science ®Google Scholar
• Pierson TC, Xu Q, Nelson S, et al. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe. 2007;1:135–145.
   PubMed Web of Science ®Google Scholar
• Pierson TC, Fremont DH, Kuhn RJ, et al. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe. 2008;4:229–238.
   PubMed Web of Science ®Google Scholar
• Lok SM, Kostyuchenko V, Nybakken GE, et al. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat Struct Mol Biol. 2008;15:312–317.
   PubMed Web of Science ®Google Scholar
• Austin SK, Dowd KA, Shrestha B, et al. Structural basis of differential neutralization of DENV-1 genotypes by an antibody that recognizes a cryptic epitope. PLoS Pathog. 2012;8:e1002930.
   PubMed Web of Science ®Google Scholar
• Kuhn RJ, Dowd KA, Beth Post C, et al. Shake, rattle, and roll: impact of the dynamics of flavivirus particles on their interactions with the host. Virology. 2015;479-480:508–517.
   PubMed Web of Science ®Google Scholar
• Midgley CM, Flanagan A, Tran HB, et al. Structural analysis of a dengue cross-reactive antibody complexed with envelope domain III reveals the molecular basis of cross-reactivity. J Immunol. 2012;188:4971–4979.
   PubMed Web of Science ®Google Scholar
• Sukupolvi-Petty S, Brien JD, Austin SK, et al. Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection. J Virol. 2013;87:8826–8842.
   PubMed Web of Science ®Google Scholar
• Crill WD, Roehrig JT. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J Virol. 2001;75:7769–7773.
   PubMed Web of Science ®Google Scholar
• He RT, Innis BL, Nisalak A, et al. 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. 1995;45:451–461.
   PubMed Web of Science ®Google Scholar
• Roehrig JT, Bolin RA, Kelly RG. Monoclonal antibody mapping of the envelope glycoprotein of the dengue 2 virus, Jamaica. Virology. 1998;246:317–328.
   PubMed Web of Science ®Google Scholar
• Cockburn JJ, Navarro Sanchez ME, Goncalvez AP, et al. Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus. Embo J. 2012;31:767–779.
   PubMed Web of Science ®Google Scholar
• Schieffelin JS, Costin JM, Nicholson CO, et al. Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient. Virol J. 2010;7:28.
   PubMed Web of Science ®Google Scholar
• Crill WD, Hughes HR, Delorey MJ, et al. Humoral immune responses of dengue fever patients using epitope-specific serotype-2 virus-like particle antigens. PLoS One. 2009;4:e4991.
   PubMed Web of Science ®Google Scholar
• Crill WD, Hughes HR. Trainor NB et al. Sculpting humoral immunity through dengue vaccination to enhance protective immunity. Front Immunol. 2012:3:334.
   PubMed Web of Science ®Google Scholar
• Lai CY, Tsai WY, Lin SR, et al. Antibodies to envelope glycoprotein of dengue virus during the natural course of infection are predominantly cross-reactive and recognize epitopes containing highly conserved residues at the fusion loop of domain II. J Virol. 2008;82:6631–6643.
   PubMed Web of Science ®Google Scholar
• Omokoko MD, Pambudi S, Phanthanawiboon S, et al. A highly conserved region between amino acids 221 and 266 of dengue virus non-structural protein 1 is a major epitope region in infected patients. Am J Trop Med Hyg. 2014;91:146–155.
   PubMed Web of Science ®Google Scholar
• Masrinoul P, Omokoko MD, Pambudi S, et al. Serotype-specific anti-Dengue virus NS1 mouse antibodies cross-react with prM and are potentially involved in virus production. Viral Immunol. 2013;26:250–258.
   PubMed Web of Science ®Google Scholar
• Mathew A, West K, Kalayanarooj S, et al. B-cell responses during primary and secondary dengue virus infections in humans. J Infect Dis. 2011;204:1514–1522.
   PubMed Web of Science ®Google Scholar
• Falconar AK. The dengue virus nonstructural-1 protein (NS1) generates antibodies to common epitopes on human blood clotting, integrin/adhesin proteins and binds to human endothelial cells: potential implications in haemorrhagic fever pathogenesis. Arch Virol. 1997;142:897–916.
   PubMed Web of Science ®Google Scholar
• Schlesinger JJ, Brandriss MW, Walsh EE. Protection of mice against dengue 2 virus encephalitis by immunization with the dengue 2 virus non-structural glycoprotein NS1. J Gen Virol. 1987;68(Pt 3):853–857.
   PubMed Web of Science ®Google Scholar
• Henchal EA, Henchal LS, Schlesinger JJ. Synergistic interactions of anti-NS1 monoclonal antibodies protect passively immunized mice from lethal challenge with dengue 2 virus. J Gen Virol. 1988;69(Pt 8):2101–2107.
   PubMed Web of Science ®Google Scholar
• Traggiai E, Becker S, Subbarao K, et al. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat Med. 2004;10:871–875.
   PubMed Web of Science ®Google Scholar
• Beltramello M, Williams KL, Simmons CP, et al. The human immune response to dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe. 2010;8:271–283.
   PubMed Web of Science ®Google Scholar
• De Alwis R, Beltramello M, Messer WB, et al. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl Trop Dis. 2011;5:e1188.
   PubMed Web of Science ®Google Scholar
• Smith SA, Zhou Y, Olivarez NP, et al. Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J Virol. 2012;86:2665–2675.
   PubMed Web of Science ®Google Scholar
• Tsai WY, Lai CY, Wu YC, et al. High-avidity and potently neutralizing cross-reactive human monoclonal antibodies derived from secondary dengue virus infection. J Virol. 2013;87:12562–12575.
   PubMed Web of Science ®Google Scholar
• Wahala WM, Kraus AA, Haymore LB, et al. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology. 2009;392:103–113.
   PubMed Web of Science ®Google Scholar
• Fibriansah G, Tan JL, Smith SA, et al. A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol Med. 2014;6:358–371.
   PubMed Web of Science ®Google Scholar
• Teoh EP, Kukkaro P, Teo EW, et al. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci Transl Med. 2012;4:139ra83.
   PubMed Web of Science ®Google Scholar
• Fibriansah G, Tan JL, Smith SA, et al. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat Commun. 2015;6:6341.
   PubMed Web of Science ®Google Scholar
• Dejnirattisai W, Wongwiwat W, Supasa S, et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol. 2015;16:170–177.
   PubMed Web of Science ®Google Scholar
• Rouvinski A, Guardado-Calvo P, Barba-Spaeth G, et al. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature. 2015;520:109–113.
   PubMed Web of Science ®Google Scholar
• Fibriansah G, Ibarra KD, Ng TS, et al. DENGUE VIRUS. Cryo-EM structure of an antibody that neutralizes dengue virus type 2 by locking E protein dimers. Science. 2015;349:88–91.
   PubMed Web of Science ®Google Scholar
• Sabchareon A, Wallace D, Sirivichayakul C, et al. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet. 2012;380:1559–1567.
   PubMed Web of Science ®Google Scholar
• Capeding MR, Tran NH, Hadinegoro SR, et al. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet. 2014;384:1358–1365.
   PubMed Web of Science ®Google Scholar
• Hss AS, Koh MT, Tan KK, et al. Safety and immunogenicity of a tetravalent dengue vaccine in healthy children aged 2-11 years in Malaysia: a randomized, placebo-controlled, Phase III study. Vaccine. 2013;31:5814–5821.
   PubMed Web of Science ®Google Scholar
• Villar L, Dayan GH, Arredondo-Garcia JL, et al. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med. 2015;372:113–123.
   PubMed Web of Science ®Google Scholar
• Rodenhuis-Zybert IA, Da Silva Voorham JM, Torres S, et al. Antibodies against immature virions are not a discriminating factor for dengue disease severity. PLoS Negl Trop Dis. 2015;9:e0003564.
   Web of Science ®Google Scholar
• Sirivichayakul C, Sabchareon A, Limkittikul K, et al. Plaque reduction neutralization antibody test does not accurately predict protection against dengue infection in Ratchaburi cohort, Thailand. Virol J. 2014;11:48.
   PubMed Web of Science ®Google Scholar
• Moi ML, Lim CK, Kotaki A, et al. Discrepancy in dengue virus neutralizing antibody titers between plaque reduction neutralizing tests with Fcgamma receptor (FcgammaR)-negative and FcgammaR-expressing BHK-21 cells. Clin Vaccine Immunol. 2010;17:402–407.
   PubMed Web of Science ®Google Scholar
• Brien JD, Austin SK, Sukupolvi-Petty S, et al. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol. 2010;84:10630–10643.
   PubMed Web of Science ®Google Scholar
• Shrestha B, Brien JD, Sukupolvi-Petty S, et al. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog. 2010;6:e1000823.
   PubMed Web of Science ®Google Scholar
• Hadinegoro SR, Arredondo-Garcia JL, Capeding MR, et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med. 2015;373:1195–1206.
   PubMed Web of Science ®Google Scholar
• Guy B, Briand O, Lang J, et al. Development of the Sanofi Pasteur tetravalent dengue vaccine: One more step forward. Vaccine. 2015. DOI:10.1016/j.vaccine.2015.09.108.
   Web of Science ®Google Scholar
• McArthur MA, Sztein MB, Edelman R. Dengue vaccines: recent developments, ongoing challenges and current candidates. Expert Rev Vaccines. 2013;12:933–953.
   PubMed Web of Science ®Google Scholar
• George SL, Wong MA, Dube TJ, et al. Safety and immunogenicity of a live attenuated tetravalent dengue vaccine candidate in flavivirus-naive adults: a randomized, double-blind Phase I clinical trial. J Infect Dis. 2015;212:1032–1041.
   Web of Science ®Google Scholar
• Kirkpatrick BD, Durbin AP, Pierce KK, et al. Robust and balanced immune responses to all 4 dengue virus serotypes following administration of a single dose of a live attenuated tetravalent dengue vaccine to healthy, flavivirus-naive adults. J Infect Dis. 2015;212:702–710.
   PubMed Web of Science ®Google Scholar