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Abstract

Flaviviruses such as dengue (DENV), yellow fever (YFV), West Nile (WNV), and Zika (ZIKV) are human pathogens of global significance. In particular, DENV causes the most prevalent mosquito-borne viral diseases in humans, and ZIKV emerged from obscurity into the spotlight in 2016 as the etiologic agent of congenital Zika syndrome. Owing to the recent emergence of ZIKV as a global pandemic threat, the roles of the immune system during ZIKV infections are as yet unclear. In contrast, decades of DENV research implicate a dual role for the immune system in protection against and pathogenesis of DENV infection. As DENV and ZIKV are closely related, knowledge based on DENV studies has been used to prioritize investigation of ZIKV immunity and pathogenesis, and to accelerate ZIKV diagnostic, therapeutic, and vaccine design. This review discusses the following topics related to innate and adaptive immune responses to DENV and ZIKV: the interferon system as the key mechanism of host defense and viral target for immune evasion, antibody-mediated protection versus antibody-dependent enhancement, and T cell–mediated protection versus original T cell antigenic sin. Understanding the mechanisms that regulate the balance between immune-mediated protection and pathogenesis during DENV and ZIKV infections is critical toward development of safe and effective DENV and ZIKV therapeutics and vaccines.

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2018-04-26
2024-06-25
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Literature Cited

  1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW. 1.  et al. 2013. The global distribution and burden of dengue. Nature 496:504–7 [Google Scholar]
  2. Gubler DJ. 2.  2012. The economic burden of dengue. Am. J. Trop. Med. Hyg. 86:743–44 [Google Scholar]
  3. Solomon T, Dung NM, Vaughn DW, Kneen R, Thao LT. 3.  et al. 2000. Neurological manifestations of dengue infection. Lancet 355:1053–59 [Google Scholar]
  4. Messer WB, Gubler DJ, Harris E, Sivananthan K, de Silva AM. 4.  2003. Emergence and global spread of a dengue serotype 3, subtype III virus. Emerg. Infect. Dis. 9:800–9 [Google Scholar]
  5. Manokaran G, Finol E, Wang C, Gunaratne J, Bahl J. 5.  et al. 2015. Dengue subgenomic RNA binds TRIM25 to inhibit interferon expression for epidemiological fitness. Science 350:217–21 [Google Scholar]
  6. Cologna R, Rico-Hesse R. 6.  2003. American genotype structures decrease dengue virus output from human monocytes and dendritic cells. J. Virol. 77:3929–38 [Google Scholar]
  7. Halstead SB. 7.  2007. Dengue. Lancet 370:1644–52 [Google Scholar]
  8. Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR. 8.  2016. Zika virus and birth defects—reviewing the evidence for causality. N. Engl. J. Med. 374:1981–87 [Google Scholar]
  9. Watrin L, Ghawche F, Larre P, Neau JP, Mathis S, Fournier E. 9.  2016. Guillain-Barre syndrome (42 cases) occurring during a Zika virus outbreak in French Polynesia. Medicine 95:e3257 [Google Scholar]
  10. Parra B, Lizarazo J, Jimenez-Arango JA, Zea-Vera AF, Gonzalez-Manrique G. 10.  et al. 2016. Guillain-Barre syndrome associated with Zika virus infection in Colombia. N. Engl. J. Med. 375:1513–23 [Google Scholar]
  11. Cao-Lormeau VM, Blake A, Mons S, Lastere S, Roche C. 11.  et al. 2016. Guillain-Barre syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387:1531–39 [Google Scholar]
  12. Malkki H. 12.  2016. CNS infections: Zika virus infection could trigger Guillain-Barre syndrome. Nat. Rev. Neurol. 12:187 [Google Scholar]
  13. D'Ortenzio E, Matheron S, Yazdanpanah Y, de Lamballerie X, Hubert B. 13.  et al. 2016. Evidence of sexual transmission of Zika virus. N. Engl. J. Med. 374:2195–98 [Google Scholar]
  14. Moreira J, Peixoto TM, Siqueira AM, Lamas CC. 14.  2017. Sexually acquired Zika virus: a systematic review. Clin. Microbiol. Infect. 23:296–305 [Google Scholar]
  15. Barzon L, Pacenti M, Franchin E, Lavezzo E, Trevisan M. 15.  et al. 2016. Infection dynamics in a traveller with persistent shedding of Zika virus RNA in semen for six months after returning from Haiti to Italy, January 2016.. Eurosurveillance 21:30316 [Google Scholar]
  16. Froeschl G, Huber K, von Sonnenburg F, Nothdurft HD, Bretzel G. 16.  et al. 2017. Long-term kinetics of Zika virus RNA and antibodies in body fluids of a vasectomized traveller returning from Martinique: a case report. BMC Infect. Dis. 17:55 [Google Scholar]
  17. Murray KO, Gorchakov R, Carlson AR, Berry R, Lai L. 17.  et al. 2017. Prolonged detection of Zika virus in vaginal secretions and whole blood. Emerg. Infect. Dis. 23:99–101 [Google Scholar]
  18. Pierson TC, Graham BS. 18.  2016. Zika virus: immunity and vaccine development. Cell 167:625–31 [Google Scholar]
  19. Barouch DH, Thomas SJ, Michael NL. 19.  2017. Prospects for a Zika virus vaccine. Immunity 46:176–82 [Google Scholar]
  20. Xu X, Vaughan K, Weiskopf D, Grifoni A, Diamond MS. 20.  et al. 2016. Identifying candidate targets of immune responses in Zika virus based on homology to epitopes in other flavivirus species. PLOS Currents Outbreaks Nov. 15. https://dx.doi.org/10.1371/currents.outbreaks.9aa2e1fb61b0f632f58a098773008c4b [Crossref] [Google Scholar]
  21. Dowd KA, DeMaso CR, Pelc RS, Speer SD, Smith AR. 21.  et al. 2016. Broadly neutralizing activity of Zika virus-immune sera identifies a single viral serotype. Cell Rep 16:1485–91 [Google Scholar]
  22. Lindenbach BD, Rice CM. 22.  2003. Molecular biology of flaviviruses. Adv. Virus Res. 59:23–61 [Google Scholar]
  23. Mukhopadhyay S, Kuhn RJ, Rossmann MG. 23.  2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13–22 [Google Scholar]
  24. Zybert IA, van der Ende-Metselaar H, Wilschut J, Smit JM. 24.  2008. Functional importance of dengue virus maturation: infectious properties of immature virions. J. Gen. Virol. 89:3047–51 [Google Scholar]
  25. Junjhon J, Lausumpao M, Supasa S, Noisakran S, Songjaeng A. 25.  et al. 2008. 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. 82:10776–91 [Google Scholar]
  26. Modis Y, Ogata S, Clements D, Harrison SC. 26.  2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313–19 [Google Scholar]
  27. Modis Y, Ogata S, Clements D, Harrison SC. 27.  2005. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79:1223–31 [Google Scholar]
  28. Gack MU, Diamond MS. 28.  2016. Innate immune escape by Dengue and West Nile viruses. Curr. Opin. Virol. 20:119–28 [Google Scholar]
  29. Bidet K, Dadlani D, Garcia-Blanco MA. 29.  2014. G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA. PLOS Pathog 10:e1004242 [Google Scholar]
  30. Donald CL, Brennan B, Cumberworth SL, Rezelj VV, Clark JJ. 30.  et al. 2016. Full genome sequence and sfRNA interferon antagonist activity of Zika virus from Recife, Brazil. PLOS Negl. Trop. Dis. 10:e0005048 [Google Scholar]
  31. Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD. 31.  et al. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3:866–71 [Google Scholar]
  32. Prestwood TR, Prigozhin DM, Sharar KL, Zellweger RM, Shresta S. 32.  2008. A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J. Virol. 82:8411–21 [Google Scholar]
  33. Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J. 33.  et al. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823–29 [Google Scholar]
  34. Navarro-Sanchez E, Altmeyer R, Amara A, Schwartz O, Fieschi F. 34.  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 4:1–6 [Google Scholar]
  35. Dejnirattisai W, Webb AI, Chan V, Jumnainsong A, Davidson A. 35.  et al. 2011. Lectin switching during dengue virus infection. J. Infect. Dis. 203:1775–83 [Google Scholar]
  36. Miller JL, de Wet BJ, Martinez-Pomares L, Radcliffe CM, Dwek RA. 36.  et al. 2008. The mannose receptor mediates dengue virus infection of macrophages. PLOS Pathog 4:e17 [Google Scholar]
  37. Meertens L, Carnec X, Lecoin MP, Ramdasi R, Guivel-Benhassine F. 37.  et al. 2012. The TIM and TAM families of phosphatidylserine receptors mediate dengue virus entry. Cell Host Microbe 12:544–57 [Google Scholar]
  38. Carnec X, Meertens L, Dejarnac O, Perera-Lecoin M, Hafirassou ML. 38.  et al. 2015. The phosphatidylserine and phosphatidylethanolamine receptor CD300a binds dengue virus and enhances infection. J. Virol. 90:92–102 [Google Scholar]
  39. Wells MF, Salick MR, Wiskow O, Ho DJ, Worringer KA. 39.  et al. 2016. Genetic ablation of AXL does not protect human neural progenitor cells and cerebral organoids from Zika virus infection. Cell Stem Cell 19:703–8 [Google Scholar]
  40. Govero J, Esakky P, Scheaffer SM, Fernandez E, Drury A. 40.  et al. 2016. Zika virus infection damages the testes in mice. Nature 540:438–42 [Google Scholar]
  41. Hastings AK, Yockey LJ, Jagger BW, Hwang J, Uraki R. 41.  et al. 2017. TAM receptors are not required for Zika virus infection in mice. Cell Rep 19:558–68 [Google Scholar]
  42. Miner JJ, Sene A, Richner JM, Smith AM, Santeford A. 42.  et al. 2016. Zika virus infection in mice causes panuveitis with shedding of virus in tears. Cell Rep 16:3208–18 [Google Scholar]
  43. Prasad VM, Miller AS, Klose T, Sirohi D, Buda G. 43.  et al. 2017. Structure of the immature Zika virus at 9 Å resolution. Nat. Struct. Mol. Biol. 24:184–86 [Google Scholar]
  44. Rodenhuis-Zybert IA, van der Schaar HM, da Silva Voorham JM, van der Ende-Metselaar H, Lei HY. 44.  et al. 2010. Immature dengue virus: a veiled pathogen?. PLOS Pathog 6:e1000718 [Google Scholar]
  45. Hall WC, Crowell TP, Watts DM, Barros VL, Kruger H. 45.  et al. 1991. Demonstration of yellow fever and dengue antigens in formalin-fixed paraffin-embedded human liver by immunohistochemical analysis. Am. J. Trop. Med. Hyg. 45:408–17 [Google Scholar]
  46. Bhoopat L, Bhamarapravati N, Attasiri C, Yoksarn S, Chaiwun B. 46.  et al. 1996. Immunohistochemical characterization of a new monoclonal antibody reactive with dengue virus-infected cells in frozen tissue using immunoperoxidase technique. Asian Pac. J. Allergy Immunol. 14:107–13 [Google Scholar]
  47. Jessie K, Fong MY, Devi S, Lam SK, Wong KT. 47.  2004. Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J. Infect. Dis. 189:1411–18 [Google Scholar]
  48. Balsitis SJ, Coloma J, Castro G, Alava A, Flores D. 48.  et al. 2009. Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. Am. J. Trop. Med. Hyg. 80:416–24 [Google Scholar]
  49. Couvelard A, Marianneau P, Bedel C, Drouet MT, Vachon F. 49.  et al. 1999. Report of a fatal case of dengue infection with hepatitis: demonstration of dengue antigens in hepatocytes and liver apoptosis. Hum. Pathol. 30:1106–10 [Google Scholar]
  50. Huerre MR, Lan NT, Marianneau P, Hue NB, Khun H. 50.  et al. 2001. Liver histopathology and biological correlates in five cases of fatal dengue fever in Vietnamese children. Virchows Arch 438:107–15 [Google Scholar]
  51. Ramos C, Sanchez G, Pando RH, Baquera J, Hernandez D. 51.  et al. 1998. Dengue virus in the brain of a fatal case of hemorrhagic dengue fever. J. Neurovirol. 4:465–68 [Google Scholar]
  52. Durbin AP, Vargas MJ, Wanionek K, Hammond SN, Gordon A. 52.  et al. 2008. 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 376:429–35 [Google Scholar]
  53. Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E. 53.  et al. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 6:816–20 [Google Scholar]
  54. Cerny D, Haniffa M, Shin A, Bigliardi P, Tan BK. 54.  et al. 2014. Selective susceptibility of human skin antigen presenting cells to productive dengue virus infection. PLOS Pathog 10:e1004548 [Google Scholar]
  55. Blackley S, Kou Z, Chen H, Quinn M, Rose RC. 55.  et al. 2007. Primary human splenic macrophages, but not T or B cells, are the principal target cells for dengue virus infection in vitro. J. Virol. 81:13325–34 [Google Scholar]
  56. Schmid MA, Harris E. 56.  2014. Monocyte recruitment to the dermis and differentiation to dendritic cells increases the targets for dengue virus replication. PLOS Pathog 10:e1004541 [Google Scholar]
  57. Prestwood TR, May MM, Plummer EM, Morar MM, Yauch LE, Shresta S. 57.  2012. Trafficking and replication patterns reveal splenic macrophages as major targets of dengue virus in mice. J. Virol. 86:12138–47 [Google Scholar]
  58. Zellweger RM, Prestwood TR, Shresta S. 58.  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]
  59. van der Eijk AA, van Genderen PJ, Verdijk RM, Reusken CB, Mögling R. 59.  et al. 2016. Miscarriage associated with Zika virus infection. N. Engl. J. Med. 375:1002–4 [Google Scholar]
  60. Rosenberg AZ, Yu W, Hill DA, Reyes CA, Schwartz DA. 60.  2017. Placental pathology of Zika virus: Viral infection of the placenta induces villous stromal macrophage (Hofbauer cell) proliferation and hyperplasia. Arch. Pathol. Lab. Med. 141:43–48 [Google Scholar]
  61. Schwartz DA. 61.  2017. Viral infection, proliferation, and hyperplasia of Hofbauer cells and absence of inflammation characterize the placental pathology of fetuses with congenital Zika virus infection. Arch. Gynecol. Obstet. 295:1361–68 [Google Scholar]
  62. Bhatnagar J, Rabeneck DB, Martines RB, Reagan-Steiner S, Ermias Y. 62.  et al. 2017. Zika virus RNA replication and persistence in brain and placental tissue. Emerg. Infect. Dis. 23:405–14 [Google Scholar]
  63. Miner JJ, Diamond MS. 63.  2017. Zika virus pathogenesis and tissue tropism. Cell Host Microbe 21:134–42 [Google Scholar]
  64. Retallack H, Di Lullo E, Arias C, Knopp KA, Laurie MT. 64.  et al. 2016. Zika virus cell tropism in the developing human brain and inhibition by azithromycin. PNAS 113:14408–13 [Google Scholar]
  65. Aagaard KM, Lahon A, Suter MA, Arya RP, Seferovic MD. 65.  et al. 2017. Primary human placental trophoblasts are permissive for Zika virus (ZIKV) replication. Sci. Rep. 7:41389 [Google Scholar]
  66. Tabata T, Petitt M, Puerta-Guardo H, Michlmayr D, Wang C. 66.  et al. 2016. Zika virus targets different primary human placental cells, suggesting two routes for vertical transmission. Cell Host Microbe 20:155–66 [Google Scholar]
  67. Chen JC, Wang Z, Huang H, Weitz SH, Wang A. 67.  et al. 2016. Infection of human uterine fibroblasts by Zika virus in vitro: implications for viral transmission in women. Int. J. Infect. Dis. 51:139–40 [Google Scholar]
  68. Hou W, Armstrong N, Obwolo LA, Thomas M, Pang X. 68.  et al. 2017. Determination of the cell permissiveness spectrum, mode of RNA replication, and RNA-protein interaction of Zika virus. BMC Infect. Dis. 17:239 [Google Scholar]
  69. Azevedo RS, Araujo MT, Martins Filho AJ, Oliveira CS, Nunes BT. 69.  et al. 2016. Zika virus epidemic in Brazil: I. Fatal disease in adults; clinical and laboratorial aspects. J. Clin. Virol. 85:56–64 [Google Scholar]
  70. Noronha L, Zanluca C, Azevedo ML, Luz KG, Santos CN. 70.  2016. Zika virus damages the human placental barrier and presents marked fetal neurotropism. Mem. Inst. Oswaldo Cruz 111:287–93 [Google Scholar]
  71. Martines RB, Bhatnagar J, de Oliveira Ramos AM, Davi HP, Iglezias SD. 71.  et al. 2016. Pathology of congenital Zika syndrome in Brazil: a case series. Lancet 388:898–904 [Google Scholar]
  72. El Costa H, Gouilly J, Mansuy JM, Chen Q, Levy C. 72.  et al. 2016. ZIKA virus reveals broad tissue and cell tropism during the first trimester of pregnancy. Sci. Rep. 6:35296 [Google Scholar]
  73. Tang H, Hammack C, Ogden SC, Wen Z, Qian X. 73.  et al. 2016. Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18:587–90 [Google Scholar]
  74. Jurado KA, Simoni MK, Tang Z, Uraki R, Hwang J. 74.  et al. 2016. Zika virus productively infects primary human placenta-specific macrophages. JCI Insight 1:e88461 [Google Scholar]
  75. Quicke KM, Bowen JR, Johnson EL, McDonald CE, Ma H. 75.  et al. 2016. Zika virus infects human placental macrophages. Cell Host Microbe 20:83–90 [Google Scholar]
  76. Alcendor DJ. 76.  2017. Zika virus infection of the human glomerular cells: implications for viral reservoirs and renal pathogenesis. J. Infect. Dis. 216:162–71 [Google Scholar]
  77. Pagani I, Ghezzi S, Ulisse A, Rubio A, Turrini F. 77.  et al. 2017. Human endometrial stromal cells are highly permissive to productive infection by Zika virus. Sci. Rep. 7:44286 [Google Scholar]
  78. Roach T, Alcendor DJ. 78.  2017. Zika virus infection of cellular components of the blood-retinal barriers: implications for viral associated congenital ocular disease. J. Neuroinflamm. 14:43 [Google Scholar]
  79. Hamel R, Dejarnac O, Wichit S, Ekchariyawat P, Neyret A. 79.  et al. 2015. Biology of Zika virus infection in human skin cells. J. Virol. 89:8880–96 [Google Scholar]
  80. Liu S, DeLalio LJ, Isakson BE, Wang TT. 80.  2016. AXL-mediated productive infection of human endothelial cells by Zika virus. Circ. Res. 119:1183–89 [Google Scholar]
  81. Nguyen SM, Antony KM, Dudley DM, Kohn S, Simmons HA. 81.  et al. 2017. Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLOS Pathog 13:e1006378 [Google Scholar]
  82. Osuna CE, Lim SY, Deleage C, Griffin BD, Stein D. 82.  et al. 2016. Zika viral dynamics and shedding in rhesus and cynomolgus macaques. Nat. Med. 22:1448–55 [Google Scholar]
  83. Hirsch AJ, Smith JL, Haese NN, Broeckel RM, Parkins CJ. 83.  et al. 2017. Zika virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLOS Pathog 13:e1006219 [Google Scholar]
  84. Aid M, Abbink P, Larocca RA, Boyd M, Nityanandam R. 84.  et al. 2017. Zika virus persistence in the central nervous system and lymph nodes of rhesus monkeys. Cell 169:610–20.e14 [Google Scholar]
  85. Li H, Saucedo-Cuevas L, Regla-Nava JA, Chai G, Sheets N. 85.  et al. 2016. Zika virus infects neural progenitors in the adult mouse brain and alters proliferation. Cell Stem Cell 19:593–98 [Google Scholar]
  86. Brault JB, Khou C, Basset J, Coquand L, Fraisier V. 86.  et al. 2016. Comparative analysis between flaviviruses reveals specific neural stem cell tropism for Zika virus in the mouse developing neocortex. EBioMedicine 10:71–76 [Google Scholar]
  87. Singh PK, Guest JM, Kanwar M, Boss J, Gao N. 87.  et al. 2017. Zika virus infects cells lining the blood-retinal barrier and causes chorioretinal atrophy in mouse eyes. JCI Insight 2:e92340 [Google Scholar]
  88. Uraki R, Hwang J, Jurado KA, Householder S, Yockey LJ. 88.  et al. 2017. Zika virus causes testicular atrophy. Sci. Adv. 3:e1602899 [Google Scholar]
  89. Tang WW, Young MP, Mamidi A, Regla-Nava JA, Kim K, Shresta S. 89.  2016. A mouse model of Zika virus sexual transmission and vaginal viral replication. Cell Rep 17:3091–98 [Google Scholar]
  90. Bingham AM, Cone M, Mock V, Heberlein-Larson L, Stanek D. 90.  et al. 2016. Comparison of test results for Zika virus RNA in urine, serum, and saliva specimens from persons with travel-associated Zika virus disease—Florida, 2016.. MMWR 65:475–78 [Google Scholar]
  91. Tan JJL, Balne PK, Leo YS, Tong L, Ng LFP, Agrawal R. 91.  2017. Persistence of Zika virus in conjunctival fluid of convalescence patients. Sci. Rep. 7:11194 [Google Scholar]
  92. Furtado JM, Esposito DL, Klein TM, Teixeira-Pinto T, da Fonseca BA. 92.  2016. Uveitis associated with Zika virus infection. New Eng. J. Med. 375:394–96 [Google Scholar]
  93. Colt S, Garcia-Casal MN, Pena-Rosas JP, Finkelstein JL, Rayco-Solon P. 93.  et al. 2017. Transmission of Zika virus through breast milk and other breastfeeding-related bodily-fluids: a systematic review. PLOS Negl. Trop. Dis. 11:e0005528 [Google Scholar]
  94. van den Broek MF, Muller U, Huang S, Zinkernagel RM, Aguet M. 94.  1995. Immune defence in mice lacking type I and/or type II interferon receptors. Immunol. Rev. 148:5–18 [Google Scholar]
  95. Zevini A, Olagnier D, Hiscott J. 95.  2017. Crosstalk between cytoplasmic RIG-I and STING sensing pathways. Trends Immunol 38:194–205 [Google Scholar]
  96. Schneider WM, Chevillotte MD, Rice CM. 96.  2014. Interferon-stimulated genes: a complex web of host defenses. Annu. Rev. Immunol. 32:513–45 [Google Scholar]
  97. Kurane I, Innis BL, Nimmannitya S, Nisalak A, Meager A, Ennis FA. 97.  1993. High levels of interferon alpha in the sera of children with dengue virus infection. Am. J. Trop. Med. Hyg. 48:222–29 [Google Scholar]
  98. Becquart P, Wauquier N, Nkoghe D, Ndjoyi-Mbiguino A, Padilla C. 98.  et al. 2010. Acute dengue virus 2 infection in Gabonese patients is associated with an early innate immune response, including strong interferon alpha production. BMC Infect. Dis. 10:356 [Google Scholar]
  99. Sun P, Garcia J, Comach G, Vahey MT, Wang Z. 99.  et al. 2013. Sequential waves of gene expression in patients with clinically defined dengue illnesses reveal subtle disease phases and predict disease severity. PLOS Negl. Trop. Dis. 7:e2298 [Google Scholar]
  100. Simmons CP, Popper S, Dolocek C, Chau TN, Griffiths M. 100.  et al. 2007. Patterns of host genome-wide gene transcript abundance in the peripheral blood of patients with acute dengue hemorrhagic fever. J. Infect. Dis. 195:1097–107 [Google Scholar]
  101. Tolfvenstam T, Lindblom A, Schreiber MJ, Ling L, Chow A. 101.  et al. 2011. Characterization of early host responses in adults with dengue disease. BMC Infect. Dis. 11:209 [Google Scholar]
  102. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O. 102.  et al. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82:335–45 [Google Scholar]
  103. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S. 103.  et al. 2013. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 38:437–49 [Google Scholar]
  104. Diamond MS, Roberts TG, Edgil D, Lu B, Ernst J, Harris E. 104.  2000. Modulation of dengue virus infection in human cells by alpha, beta, and gamma interferons. J. Virol. 74:4957–66 [Google Scholar]
  105. Diamond MS, Harris E. 105.  2001. Interferon inhibits dengue virus infection by preventing translation of viral RNA through a PKR-independent mechanism. Virology 289:297–311 [Google Scholar]
  106. Schmid B, Rinas M, Ruggieri A, Acosta EG, Bartenschlager M. 106.  et al. 2015. Live cell analysis and mathematical modeling identify determinants of attenuation of dengue virus 2′-O-methylation mutant. PLOS Pathog 11:e1005345 [Google Scholar]
  107. Jiang D, Weidner JM, Qing M, Pan XB, Guo H. 107.  et al. 2010. Identification of five interferon-induced cellular proteins that inhibit West Nile virus and dengue virus infections. J. Virol. 84:8332–41 [Google Scholar]
  108. Helbig KJ, Carr JM, Calvert JK, Wati S, Clarke JN. 108.  et al. 2013. Viperin is induced following dengue virus type-2 (DENV-2) infection and has anti-viral actions requiring the C-terminal end of viperin. PLOS Negl. Trop. Dis. 7:e2178 [Google Scholar]
  109. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN. 109.  et al. 2009. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139:1243–54 [Google Scholar]
  110. Schoggins JW, Dorner M, Feulner M, Imanaka N, Murphy MY. 110.  et al. 2012. Dengue reporter viruses reveal viral dynamics in interferon receptor-deficient mice and sensitivity to interferon effectors in vitro. PNAS 109:14610–15 [Google Scholar]
  111. Suzuki Y, Chin WX, Han Q, Ichiyama K, Lee CH. 111.  et al. 2016. Characterization of RyDEN (C19orf66) as an interferon-stimulated cellular inhibitor against dengue virus replication. PLOS Pathog 12:e1005357 [Google Scholar]
  112. Balinsky CA, Schmeisser H, Wells AI, Ganesan S, Jin T. 112.  et al. 2017. IRAV (FLJ11286), an interferon-stimulated gene with antiviral activity against dengue virus, interacts with MOV10. J. Virol. 91:e01606–16 [Google Scholar]
  113. Lin RJ, Yu HP, Chang BL, Tang WC, Liao CL, Lin YL. 113.  2009. Distinct antiviral roles for human 2′,5′-oligoadenylate synthetase family members against dengue virus infection. J. Immunol. 183:8035–43 [Google Scholar]
  114. Savidis G, Perreira JM, Portmann JM, Meraner P, Guo Z. 114.  et al. 2016. The IFITMs inhibit Zika virus replication. Cell Rep 15:2323–30 [Google Scholar]
  115. Fu B, Wang L, Li S, Dorf ME. 115.  2017. ZMPSTE24 defends against influenza and other pathogenic viruses. J. Exp. Med. 214:919–29 [Google Scholar]
  116. Shresta S, Kyle JL, Snider HM, Basavapatna M, Beatty PR, Harris E. 116.  2004. Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J. Virol. 78:2701–10 [Google Scholar]
  117. Johnson AJ, Roehrig JT. 117.  1999. New mouse model for dengue virus vaccine testing. J. Virol. 73:783–86 [Google Scholar]
  118. Yockey LJ, Varela L, Rakib T, Khoury-Hanold W, Fink SL. 118.  et al. 2016. Vaginal exposure to Zika virus during pregnancy leads to fetal brain infection. Cell 166:1247–56.e4 [Google Scholar]
  119. Suthar MS, Aguirre S, Fernandez-Sesma A. 119.  2013. Innate immune sensing of flaviviruses. PLOS Pathog 9:e1003541 [Google Scholar]
  120. Perry ST, Prestwood TR, Lada SM, Benedict CA, Shresta S. 120.  2009. Cardif-mediated signaling controls the initial innate response to dengue virus in vivo. J. Virol. 83:8276–81 [Google Scholar]
  121. Chen HW, King K, Tu J, Sanchez M, Luster AD, Shresta S. 121.  2013. The roles of IRF-3 and IRF-7 in innate antiviral immunity against dengue virus. J. Immunol. 191:4194–201 [Google Scholar]
  122. Wang JP, Liu P, Latz E, Golenbock DT, Finberg RW, Libraty DH. 122.  2006. Flavivirus activation of plasmacytoid dendritic cells delineates key elements of TLR7 signaling beyond endosomal recognition. J. Immunol. 177:7114–21 [Google Scholar]
  123. Nasirudeen AM, Wong HH, Thien P, Xu S, Lam KP, Liu DX. 123.  2011. RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection. PLOS Negl. Trop. Dis. 5:e926 [Google Scholar]
  124. Lazear HM, Lancaster A, Wilkins C, Suthar MS, Huang A. 124.  et al. 2013. IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLOS Pathog 9:e1003118 [Google Scholar]
  125. Lazear HM, Govero J, Smith AM, Platt DJ, Fernandez E. 125.  et al. 2016. A mouse model of Zika virus pathogenesis. Cell Host Microbe 19:720–30 [Google Scholar]
  126. Brien JD, Daffis S, Lazear HM, Cho H, Suthar MS. 126.  et al. 2011. Interferon regulatory factor-1 (IRF-1) shapes both innate and CD8+ T cell immune responses against West Nile virus infection. PLOS Pathog 7:e1002230 [Google Scholar]
  127. Prestwood TR, Morar MM, Zellweger RM, Miller R, May MM. 127.  et al. 2012. Gamma interferon (IFN-γ) receptor restricts systemic dengue virus replication and prevents paralysis in IFN-α/β receptor-deficient mice. J. Virol. 86:12561–70 [Google Scholar]
  128. Orozco S, Schmid MA, Parameswaran P, Lachica R, Henn MR. 128.  et al. 2012. Characterization of a model of lethal dengue virus 2 infection in C57BL/6 mice deficient in the alpha/beta interferon receptor. J. Gen. Virol. 93:2152–57 [Google Scholar]
  129. Pinto AK, Brien JD, Lam CY, Johnson S, Chiang C. 129.  et al. 2015. Defining new therapeutics using a more immunocompetent mouse model of antibody-enhanced dengue virus infection. mBio 6:e01316–15 [Google Scholar]
  130. Zust R, Toh YX, Valdes I, Cerny D, Heinrich J. 130.  et al. 2014. Type I interferon signals in macrophages and dendritic cells control dengue virus infection: implications for a new mouse model to test dengue vaccines. J. Virol. 88:7276–85 [Google Scholar]
  131. Shresta S, Sharar KL, Prigozhin DM, Snider HM, Beatty PR, Harris E. 131.  2005. Critical roles for both STAT1-dependent and STAT1-independent pathways in the control of primary dengue virus infection in mice. J. Immunol. 175:3946–54 [Google Scholar]
  132. Perry ST, Buck MD, Lada SM, Schindler C, Shresta S. 132.  2011. STAT2 mediates innate immunity to dengue virus in the absence of STAT1 via the type I interferon receptor. PLOS Pathog 7:e1001297 [Google Scholar]
  133. Tripathi S, Balasubramaniam VR, Brown JA, Mena I, Grant A. 133.  et al. 2017. A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses. PLOS Pathog 13:e1006258 [Google Scholar]
  134. Rossi SL, Tesh RB, Azar SR, Muruato AE, Hanley KA. 134.  et al. 2016. Characterization of a novel murine model to study Zika virus. Am. J. Trop. Med. Hyg. 94:1362–69 [Google Scholar]
  135. Dowall SD, Graham VA, Rayner E, Atkinson B, Hall G. 135.  et al. 2016. A susceptible mouse model for Zika virus infection. PLOS Negl. Trop. Dis. 10:e0004658 [Google Scholar]
  136. Ashour J, Morrison J, Laurent-Rolle M, Belicha-Villanueva A, Plumlee CR. 136.  et al. 2010. Mouse STAT2 restricts early dengue virus replication. Cell Host Microbe 8:410–21 [Google Scholar]
  137. Olagnier D, Scholte FE, Chiang C, Albulescu IC, Nichols C. 137.  et al. 2014. Inhibition of dengue and chikungunya virus infections by RIG-I-mediated type I interferon-independent stimulation of the innate antiviral response. J. Virol. 88:4180–94 [Google Scholar]
  138. Bayer A, Lennemann NJ, Ouyang Y, Bramley JC, Morosky S. 138.  et al. 2016. Type III interferons produced by human placental trophoblasts confer protection against Zika virus infection. Cell Host Microbe 19:705–12 [Google Scholar]
  139. Odendall C, Dixit E, Stavru F, Bierne H, Franz KM. 139.  et al. 2014. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 15:717–26 [Google Scholar]
  140. Decembre E, Assil S, Hillaire ML, Dejnirattisai W, Mongkolsapaya J. 140.  et al. 2014. Sensing of immature particles produced by dengue virus infected cells induces an antiviral response by plasmacytoid dendritic cells. PLOS Pathog 10:e1004434 [Google Scholar]
  141. Dang J, Tiwari SK, Lichinchi G, Qin Y, Patil VS. 141.  et al. 2016. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19:258–65 [Google Scholar]
  142. Beatty PR, Puerta-Guardo H, Killingbeck SS, Glasner DR, Hopkins K, Harris E. 142.  2015. Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci. Transl. Med. 7:304ra141 [Google Scholar]
  143. Chen J, Ng MM, Chu JJ. 143.  2015. Activation of TLR2 and TLR6 by dengue NS1 protein and its implications in the immunopathogenesis of dengue virus infection. PLOS Pathog 11:e1005053 [Google Scholar]
  144. Modhiran N, Watterson D, Muller DA, Panetta AK, Sester DP. 144.  et al. 2015. Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci. Transl. Med. 7:304ra142 [Google Scholar]
  145. Grant A, Ponia SS, Tripathi S, Balasubramaniam V, Miorin L. 145.  et al. 2016. Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe 19:882–90 [Google Scholar]
  146. Dalrymple NA, Cimica V, Mackow ER. 146.  2015. Dengue virus NS proteins inhibit RIG-I/MAVS signaling by blocking TBK1/IRF3 phosphorylation: Dengue virus serotype 1 NS4A is a unique interferon-regulating virulence determinant. mBio 6:e00553–15 [Google Scholar]
  147. He Z, Zhu X, Wen W, Yuan J, Hu Y. 147.  et al. 2016. Dengue virus subverts host innate immunity by targeting adaptor protein MAVS. J. Virol. 90:7219–30 [Google Scholar]
  148. Chatel-Chaix L, Cortese M, Romero-Brey I, Bender S, Neufeldt CJ. 148.  et al. 2016. Dengue virus perturbs mitochondrial morphodynamics to dampen innate immune responses. Cell Host Microbe 20:342–56 [Google Scholar]
  149. Yu CY, Liang JJ, Li JK, Lee YL, Chang BL. 149.  et al. 2015. Dengue virus impairs mitochondrial fusion by cleaving mitofusins. PLOS Pathog 11:e1005350 [Google Scholar]
  150. Chan YK, Gack MU. 150.  2016. A phosphomimetic-based mechanism of dengue virus to antagonize innate immunity. Nat. Immunol. 17:523–30 [Google Scholar]
  151. Aguirre S, Maestre AM, Pagni S, Patel JR, Savage T. 151.  et al. 2012. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLOS Pathog 8:e1002934 [Google Scholar]
  152. Yu CY, Chang TH, Liang JJ, Chiang RL, Lee YL. 152.  et al. 2012. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLOS Pathog 8:e1002780 [Google Scholar]
  153. Aguirre S, Luthra P, Sanchez-Aparicio MT, Maestre AM, Patel J. 153.  et al. 2017. Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection. Nat. Microbiol. 2:17037 [Google Scholar]
  154. Liu H, Zhang L, Sun J, Chen W, Li S. 154.  et al. 2017. Endoplasmic reticulum protein SCAP inhibits dengue virus NS2B3 protease by suppressing its K27-linked polyubiquitylation. J. Virol. 91:e02234–16 [Google Scholar]
  155. Munoz-Jordan JL, Sanchez-Burgos GG, Laurent-Rolle M, Garcia-Sastre A. 155.  2003. Inhibition of interferon signaling by dengue virus. PNAS 100:14333–38 [Google Scholar]
  156. Morrison J, Laurent-Rolle M, Maestre AM, Rajsbaum R, Pisanelli G. 156.  et al. 2013. Dengue virus co-opts UBR4 to degrade STAT2 and antagonize type I interferon signaling. PLOS Pathog 9:e1003265 [Google Scholar]
  157. Bowen JR, Quicke KM, Maddur MS, O'Neal JT, McDonald CE. 157.  et al. 2017. Zika virus antagonizes type I interferon responses during infection of human dendritic cells. PLOS Pathog 13:e1006164 [Google Scholar]
  158. Schuberth-Wagner C, Ludwig J, Bruder AK, Herzner AM, Zillinger T. 158.  et al. 2015. A conserved histidine in the RNA sensor RIG-I controls immune tolerance to N1-2′O-methylated self RNA. Immunity 43:41–51 [Google Scholar]
  159. Zust R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW. 159.  et al. 2011. Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 12:137–43 [Google Scholar]
  160. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S. 160.  et al. 2010. 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468:452–56 [Google Scholar]
  161. Chang DC, Hoang LT, Mohamed Naim AN, Dong H, Schreiber MJ. 161.  et al. 2016. Evasion of early innate immune response by 2′-O-methylation of dengue genomic RNA. Virology 499:259–66 [Google Scholar]
  162. You J, Hou S, Malik-Soni N, Xu Z, Kumar A. 162.  et al. 2015. Flavivirus infection impairs peroxisome biogenesis and early antiviral signaling. J. Virol. 89:12349–61 [Google Scholar]
  163. Sabin AB. 163.  1952. Research on dengue during World War II. Am. J. Trop. Med. Hyg. 1:30–50 [Google Scholar]
  164. Guzman MG, Kouri G, Valdes L, Bravo J, Alvarez M. 164.  et al. 2000. Epidemiologic studies on dengue in Santiago de Cuba, 1997.. Am. J. Epidemiol. 152:793–99; discussion 804 [Google Scholar]
  165. Fernandez E, Diamond MS. 165.  2017. Vaccination strategies against Zika virus. Curr. Opin. Virol. 23:59–67 [Google Scholar]
  166. Wen J, Tang WW, Sheets N, Ellison J, Sette A. 166.  et al. 2017. Identification of Zika virus epitopes reveals immunodominant and protective roles for dengue virus cross-reactive CD8+ T cells. Nat. Microbiol. 2:17036 [Google Scholar]
  167. Kaufman BM, Summers PL, Dubois DR, Cohen WH, Gentry MK. 167.  et al. 1989. Monoclonal antibodies for dengue virus prM glycoprotein protect mice against lethal dengue infection. Am. J. Trop. Med. Hyg. 41:576–80 [Google Scholar]
  168. Kaufman BM, Summers PL, Dubois DR, Eckels KH. 168.  1987. Monoclonal antibodies against dengue 2 virus E-glycoprotein protect mice against lethal dengue infection. Am. J. Trop. Med. Hyg. 36:427–34 [Google Scholar]
  169. Kyle JL, Balsitis SJ, Zhang L, Beatty PR, Harris E. 169.  2008. Antibodies play a greater role than immune cells in heterologous protection against secondary dengue virus infection in a mouse model. Virology 380:296–303 [Google Scholar]
  170. Wahala WM, Silva AM. 170.  2011. The human antibody response to dengue virus infection. Viruses 3:2374–95 [Google Scholar]
  171. Tsai WY, Lai CY, Wu YC, Lin HE, Edwards C. 171.  et al. 2013. High-avidity and potently neutralizing cross-reactive human monoclonal antibodies derived from secondary dengue virus infection. J. Virol. 87:12562–75 [Google Scholar]
  172. Tsai WY, Durbin A, Tsai JJ, Hsieh SC, Whitehead S, Wang WK. 172.  2015. Complexity of neutralizing antibodies against multiple dengue virus serotypes after heterotypic immunization and secondary infection revealed by in-depth analysis of cross-reactive antibodies. J. Virol. 89:7348–62 [Google Scholar]
  173. Priyamvada L, Quicke KM, Hudson WH, Onlamoon N, Sewatanon J. 173.  et al. 2016. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. PNAS 113:7852–57 [Google Scholar]
  174. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A. 174.  et al. 2016. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353:823–26 [Google Scholar]
  175. Swanstrom JA, Plante JA, Plante KS, Young EF, McGowan E. 175.  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]
  176. Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G. 176.  et al. 2016. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with Zika virus. Nat. Immunol. 17:1102–8 [Google Scholar]
  177. Priyamvada L, Hudson W, Ahmed R, Wrammert J. 177.  2017. Humoral cross-reactivity between Zika and dengue viruses: implications for protection and pathology. Emerg. Microbes Infect. 6:e33 [Google Scholar]
  178. Sukupolvi-Petty S, Austin SK, Purtha WE, Oliphant T, Nybakken GE. 178.  et al. 2007. Type- and subcomplex-specific neutralizing antibodies against domain III of dengue virus type 2 envelope protein recognize adjacent epitopes. J. Virol. 81:12816–26 [Google Scholar]
  179. Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA. 179.  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]
  180. Wahala WM, Kraus AA, Haymore LB, Accavitti-Loper MA, de Silva AM. 180.  2009. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 392:103–13 [Google Scholar]
  181. Edeling MA, Austin SK, Shrestha B, Dowd KA, Mukherjee S. 181.  et al. 2014. Potent dengue virus neutralization by a therapeutic antibody with low monovalent affinity requires bivalent engagement. PLOS Pathog 10:e1004072 [Google Scholar]
  182. de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP. 182.  et al. 2012. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. PNAS 109:7439–44 [Google Scholar]
  183. Dejnirattisai W, Wongwiwat W, Supasa S, Zhang X, Dai X. 183.  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]
  184. Fibriansah G, Tan JL, Smith SA, de Alwis R, Ng TS. 184.  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]
  185. Sapparapu G, Fernandez E, Kose N, Bin C, Fox JM. 185.  et al. 2016. Neutralizing human antibodies prevent Zika virus replication and fetal disease in mice. Nature 540:443–47 [Google Scholar]
  186. Wang Q, Yang H, Liu X, Dai L, Ma T. 186.  et al. 2016. Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci. Transl. Med. 8:369ra179 [Google Scholar]
  187. Hasan SS, Miller A, Sapparapu G, Fernandez E, Klose T. 187.  et al. 2017. A human antibody against Zika virus crosslinks the E protein to prevent infection. Nat. Commun. 8:14722 [Google Scholar]
  188. Robbiani DF, Bozzacco L, Keeffe JR, Khouri R, Olsen PC. 188.  et al. 2017. Recurrent potent human neutralizing antibodies to Zika virus in Brazil and Mexico. Cell 169:597–609.e11 [Google Scholar]
  189. Halstead SB. 189.  1988. Pathogenesis of dengue: challenges to molecular biology. Science 239:476–81 [Google Scholar]
  190. Halstead SB, Shotwell H, Casals J. 190.  1973. Studies on the pathogenesis of dengue infection in monkeys: II. Clinical laboratory responses to heterologous infection. J. Infect. Dis. 128:15–22 [Google Scholar]
  191. Halstead SB. 191.  1979. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J. Infect. Dis. 140:527–33 [Google Scholar]
  192. Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ. 192.  2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. PNAS 104:9422–27 [Google Scholar]
  193. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL. 193.  et al. 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLOS Pathog 6:e1000790 [Google Scholar]
  194. Ng JK, Zhang SL, Tan HC, Yan B, Martinez JM. 194.  et al. 2014. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLOS Pathog 10:e1004031 [Google Scholar]
  195. Bardina SV, Bunduc P, Tripathi S, Duehr J, Frere JJ. 195.  et al. 2017. Enhancement of Zika virus pathogenesis by preexisting antiflavivirus immunity. Science 356:175–80 [Google Scholar]
  196. Pierson TC, Xu Q, Nelson S, Oliphant T, Nybakken GE. 196.  et al. 2007. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1:135–45 [Google Scholar]
  197. Yamanaka A, Kosugi S, Konishi E. 197.  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]
  198. Morens DM, Halstead SB. 198.  1987. Disease severity-related antigenic differences in dengue 2 strains detected by dengue 4 monoclonal antibodies. J. Med. Virol. 22:169–74 [Google Scholar]
  199. Pierson TC, Diamond MS. 199.  2008. Molecular mechanisms of antibody-mediated neutralisation of flavivirus infection. Expert Rev. Mol. Med. 10:e12 [Google Scholar]
  200. Rodrigo WW, Jin X, Blackley SD, Rose RC, Schlesinger JJ. 200.  2006. Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human FcγRIA (CD64) or FcgγRIIA (CD32). J. Virol. 80:10128–38 [Google Scholar]
  201. Boonnak K, Slike BM, Donofrio GC, Marovich MA. 201.  2013. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J. Immunol. 190:5659–65 [Google Scholar]
  202. Chan KR, Zhang SL, Tan HC, Chan YK, Chow A. 202.  et al. 2011. Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection. PNAS 108:12479–84 [Google Scholar]
  203. Chareonsirisuthigul T, Kalayanarooj S, Ubol S. 203.  2007. 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. 88:365–75 [Google Scholar]
  204. Boonnak K, Slike BM, Burgess TH, Mason RM, Wu SJ. 204.  et al. 2008. Role of dendritic cells in antibody-dependent enhancement of dengue virus infection. J. Virol. 82:3939–51 [Google Scholar]
  205. Chan KR, Ong EZ, Tan HC, Zhang SL, Zhang Q. 205.  et al. 2014. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. PNAS 111:2722–27 [Google Scholar]
  206. Wang TT, Sewatanon J, Memoli MJ, Wrammert J, Bournazos S. 206.  et al. 2017. IgG antibodies to dengue enhanced for FcγRIIIA binding determine disease severity. Science 355:395–98 [Google Scholar]
  207. Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N. 207.  et al. 2003. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat. Med. 9:921–27 [Google Scholar]
  208. Duangchinda T, Dejnirattisai W, Vasanawathana S, Limpitikul W, Tangthawornchaikul N. 208.  et al. 2010. Immunodominant T-cell responses to dengue virus NS3 are associated with DHF. PNAS 107:16922–27 [Google Scholar]
  209. Rothman AL. 209.  2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11:532–43 [Google Scholar]
  210. Mangada MM, Rothman AL. 210.  2005. Altered cytokine responses of dengue-specific CD4+ T cells to heterologous serotypes. J. Immunol. 175:2676–83 [Google Scholar]
  211. Mangada MM, Endy TP, Nisalak A, Chunsuttiwat S, Vaughn DW. 211.  et al. 2002. Dengue-specific T cell responses in peripheral blood mononuclear cells obtained prior to secondary dengue virus infections in Thai schoolchildren. J. Infect. Dis. 185:1697–703 [Google Scholar]
  212. Weiskopf D, Angelo MA, de Azeredo EL, Sidney J, Greenbaum JA. 212.  et al. 2013. Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. PNAS 110:E2046–53 [Google Scholar]
  213. Weiskopf D, Cerpas C, Angelo MA, Bangs DJ, Sidney J. 213.  et al. 2015. Human CD8+ T-cell responses against the 4 dengue virus serotypes are associated with distinct patterns of protein targets. J. Infect. Dis. 212:1743–51 [Google Scholar]
  214. Weiskopf D, Angelo MA, Bangs DJ, Sidney J, Paul S. 214.  et al. 2015. The human CD8+ T cell responses induced by a live attenuated tetravalent dengue vaccine are directed against highly conserved epitopes. J. Virol. 89:120–28 [Google Scholar]
  215. de Alwis R, Bangs DJ, Angelo MA, Cerpas C, Fernando A. 215.  et al. 2016. Immunodominant dengue virus-specific CD8+ T cell responses are associated with a memory PD-1+ phenotype. J. Virol. 90:4771–79 [Google Scholar]
  216. Rivino L, Kumaran EA, Thein TL, Too CT, Gan VC. 216.  et al. 2015. Virus-specific T lymphocytes home to the skin during natural dengue infection. Sci. Transl. Med. 7:278ra35 [Google Scholar]
  217. Hatch S, Endy TP, Thomas S, Mathew A, Potts J. 217.  et al. 2011. Intracellular cytokine production by dengue virus-specific T cells correlates with subclinical secondary infection. J. Infect. Dis. 203:1282–91 [Google Scholar]
  218. Rivino L, Kumaran EA, Jovanovic V, Nadua K, Teo EW. 218.  et al. 2013. Differential targeting of viral components by CD4+ versus CD8+ T lymphocytes in dengue virus infection. J. Virol. 87:2693–706 [Google Scholar]
  219. Lindow JC, Borochoff-Porte N, Durbin AP, Whitehead SS, Fimlaid KA. 219.  et al. 2012. Primary vaccination with low dose live dengue 1 virus generates a proinflammatory, multifunctional T cell response in humans. PLOS Negl. Trop. Dis. 6:e1742 [Google Scholar]
  220. Weiskopf D, Bangs DJ, Sidney J, Kolla RV, De Silva AD. 220.  et al. 2015. Dengue virus infection elicits highly polarized CX3CR1+ cytotoxic CD4+ T cells associated with protective immunity. PNAS 112:E4256–63 [Google Scholar]
  221. Zompi S, Santich BH, Beatty PR, Harris E. 221.  2012. Protection from secondary dengue virus infection in a mouse model reveals the role of serotype cross-reactive B and T cells. J. Immunol. 188:404–16 [Google Scholar]
  222. Yauch LE, Zellweger RM, Kotturi MF, Qutubuddin A, Sidney J. 222.  et al. 2009. A protective role for dengue virus-specific CD8+ T cells. J. Immunol. 182:4865–73 [Google Scholar]
  223. Yauch LE, Prestwood TR, May MM, Morar MM, Zellweger RM. 223.  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]
  224. Zellweger RM, Tang WW, Eddy WE, King K, Sanchez MC, Shresta S. 224.  2015. CD8+ T cells can mediate short-term protection against heterotypic dengue virus reinfection in mice. J. Virol. 89:6494–505 [Google Scholar]
  225. Elong Ngono A, Chen HW, Tang WW, Joo Y, King K. 225.  et al. 2016. Protective role of cross-reactive CD8 T cells against dengue virus infection. EBioMedicine 13:284–93 [Google Scholar]
  226. Zellweger RM, Miller R, Eddy WE, White LJ, Johnston RE, Shresta S. 226.  2013. Role of humoral versus cellular responses induced by a protective dengue vaccine candidate. PLOS Pathog 9:e1003723 [Google Scholar]
  227. Zellweger RM, Eddy WE, Tang WW, Miller R, Shresta S. 227.  2014. CD8+ T cells prevent antigen-induced antibody-dependent enhancement of dengue disease in mice. J. Immunol. 193:4117–24 [Google Scholar]
  228. Weiskopf D, Yauch LE, Angelo MA, John DV, Greenbaum JA. 228.  et al. 2011. Insights into HLA-restricted T cell responses in a novel mouse model of dengue virus infection point toward new implications for vaccine design. J. Immunol. 187:4268–79 [Google Scholar]
  229. Weiskopf D, Angelo MA, Sidney J, Peters B, Shresta S, Sette A. 229.  2014. Immunodominance changes as a function of the infecting dengue virus serotype and primary versus secondary infection. J. Virol. 88:11383–94 [Google Scholar]
  230. Weiskopf D, Cerpas C, Angelo MA, Bangs DJ, Sidney J. 230.  et al. 2015. Human CD8+ T-cell responses against the 4 dengue virus serotypes are associated with distinct patterns of protein targets. J. Infect. Dis. 212:1743–51 [Google Scholar]
  231. Chu H, George SL, Stinchcomb DT, Osorio JE, Partidos CD. 231.  2015. CD8+ T-cell responses in flavivirus-naive individuals following immunization with a live-attenuated tetravalent dengue vaccine candidate. J. Infect. Dis. 212:1618–28 [Google Scholar]
  232. Dudley DM, Aliota MT, Mohr EL, Weiler AM, Lehrer-Brey G. 232.  et al. 2016. A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun. 7:12204 [Google Scholar]
  233. Elong Ngono A, Vizcarra EA, Tang WW, Sheets N, Joo Y. 233.  et al. 2017. Mapping and role of the CD8+ T cell response during primary Zika virus infection in mice. Cell Host Microbe 21:35–46 [Google Scholar]
  234. Pardy RD, Rajah MM, Condotta SA, Taylor NG, Sagan SM, Richer MJ. 234.  2017. Analysis of the T cell response to Zika virus and identification of a novel CD8+ T cell epitope in immunocompetent mice. PLOS Pathog 13:e1006184 [Google Scholar]
  235. Winkler CW, Myers LM, Woods TA, Messer RJ, Carmody AB. 235.  et al. 2017. Adaptive immune responses to Zika virus are important for controlling virus infection and preventing infection in brain and testes. J. Immunol. 198:3526–35 [Google Scholar]
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