1932

Abstract

Zika virus (ZIKV) emerged at a global level when it spread to the Americas and began causing congenital malformations and microcephaly in 2015. A rapid response by academia, government, public health infrastructure, and industry has enabled the expedited development and testing of a suite of vaccine platforms aiming to control and eliminate ZIKV-induced disease. Analysis of key immunization and pathogenesis studies in multiple animal models, including during pregnancy, has begun to define immune correlates of protection. Nonetheless, the deployment of ZIKV vaccines, along with the confirmation of their safety and efficacy, still has major challenges, one of which is related to the waning of the epidemic. In this review, we discuss the measures that enabled rapid progress and highlight the path forward for successful deployment of ZIKV vaccines.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-med-040717-051127
2019-01-27
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/med/70/1/annurev-med-040717-051127.html?itemId=/content/journals/10.1146/annurev-med-040717-051127&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Weaver SC, Costa F, Garcia-Blanco MA et al. 2016. Zika virus: history, emergence, biology, and prospects for control. Antivir. Res. 130:69–80
    [Google Scholar]
  2. 2.  Musso D, Nilles EJ, Cao-Lormeau VM 2014. Rapid spread of emerging Zika virus in the Pacific area. Clin. Microbiol. Infect. 20:O595–96
    [Google Scholar]
  3. 3.  Oehler E, Watrin L, Larre P et al. 2014. Zika virus infection complicated by Guillain-Barré syndrome—case report. French Polynesia, December 2013 Eur. Commun. Dis. Bull. 19:20720
    [Google Scholar]
  4. 4.  Faria NR, Quick J, Claro IM et al. 2017. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature 546:406–10
    [Google Scholar]
  5. 5.  Zhang Q, Sun K, Chinazzi M et al. 2017. Spread of Zika virus in the Americas. PNAS 114:E4334–43
    [Google Scholar]
  6. 6.  Hills SL, Fischer M, Petersen LR 2017. Epidemiology of Zika virus infection. J. Infect. Dis. 216:S868–74
    [Google Scholar]
  7. 7.  Russell K, Hills SL, Oster AM et al. 2017. Male-to-female sexual transmission of Zika virus—United States. January–April 2016 Clin. Infect. Dis. 64:211–13
    [Google Scholar]
  8. 8.  Davidson A, Slavinski S, Komoto K et al. 2016. Suspected female-to-male sexual transmission of Zika virus—New York City, 2016. Morb. Mortal. Wkly. Rep. 65:716–17
    [Google Scholar]
  9. 9.  Deckard DT, Chung WM, Brooks JT et al. 2016. Male-to-male sexual transmission of Zika virus—Texas, January 2016. Morb. Mortal. Wkly. Rep. 65:372–74
    [Google Scholar]
  10. 10.  Gao D, Lou Y, He D et al. 2016. Prevention and control of Zika as a mosquito-borne and sexually transmitted disease: a mathematical modeling analysis. Sci. Rep. 6:28070
    [Google Scholar]
  11. 11.  Allard A, Althouse BM, Hebert-Dufresne L et al. 2017. The risk of sustained sexual transmission of Zika is underestimated. PLOS Pathog 13:e1006633
    [Google Scholar]
  12. 12.  Mansuy JM, Suberbielle E, Chapuy-Regaud S et al. 2016. Zika virus in semen and spermatozoa. Lancet Infect. Dis. 16:1106–7
    [Google Scholar]
  13. 13.  Murray KO, Gorchakov R, Carlson AR et al. 2017. Prolonged detection of Zika virus in vaginal secretions and whole blood. Emerg. Infect. Dis. 23:99–101
    [Google Scholar]
  14. 14.  Mlakar J, Korva M, Tul N et al. 2016. Zika virus associated with microcephaly. N. Engl. J. Med. 374:951–58
    [Google Scholar]
  15. 15.  de Paula Freitas B, de Oliveira Dias JR, Prazeres J et al. 2016. Ocular findings in infants with microcephaly associated with presumed Zika virus congenital infection in Salvador, Brazil. JAMA Ophthalmol 134:5529–35
    [Google Scholar]
  16. 16.  Leal MC, Muniz LF, Ferreira TS et al. 2016. Hearing loss in infants with microcephaly and evidence of congenital Zika virus infection—Brazil, November 2015–May 2016. Morb. Mortal. Wkly. Rep. 65:917–19
    [Google Scholar]
  17. 17.  Cauchemez S, Besnard M, Bompard P et al. 2016. Association between Zika virus and microcephaly in French Polynesia, 2013–15: a retrospective study. Lancet 387:2125–32
    [Google Scholar]
  18. 18.  Brasil P, Pereira JP Jr, Moreira ME et al. 2016. Zika virus infection in pregnant women in Rio de Janeiro. N. Engl. J. Med. 375:2321–34
    [Google Scholar]
  19. 19.  Hoen B, Schaub B, Funk AL et al. 2018. Pregnancy outcomes after ZIKV infection in French territories in the Americas. N. Engl. J. Med. 378:985–94
    [Google Scholar]
  20. 20.  Honein MA, Dawson AL, Petersen EE et al. 2017. Birth defects among fetuses and infants of US women with evidence of possible Zika virus infection during pregnancy. JAMA 317:59–68
    [Google Scholar]
  21. 21.  Liu Y, Liu J, Du S et al. 2017. Evolutionary enhancement of Zika virus infectivity in Aedesaegypti mosquitoes. Nature 545:482–86
    [Google Scholar]
  22. 22.  Yuan L, Huang XY, Liu ZY et al. 2017. A single mutation in the prM protein of Zika virus contributes to fetal microcephaly. Science 358:933–36
    [Google Scholar]
  23. 23.  Dowd KA, DeMaso CR, Pelc RS et al. 2016. Broadly neutralizing activity of Zika virus-immune sera identifies a single viral serotype. Cell Rep 16:1485–91
    [Google Scholar]
  24. 24.  Culshaw A, Mongkolsapaya J, Screaton GR 2017. The immunopathology of dengue and Zika virus infections. Curr. Opin. Immunol. 48:1–6
    [Google Scholar]
  25. 25.  Sirohi D, Kuhn RJ 2017. Zika virus structure, maturation, and receptors. J. Infect. Dis. 216:S935–44
    [Google Scholar]
  26. 26.  Sirohi D, Chen Z, Sun L et al. 2016. The 3.8 Å resolution cryo-EM structure of Zika virus. Science 352:467–70
    [Google Scholar]
  27. 27.  Kostyuchenko VA, Lim EX, Zhang S et al. 2016. Structure of the thermally stable Zika virus. Nature 533:425–28
    [Google Scholar]
  28. 28.  Sapparapu G, Fernandez E, Kose N et al. 2016. Neutralizing human antibodies prevent Zika virus replication and fetal disease in mice. Nature 540:443–47
    [Google Scholar]
  29. 29.  Robbiani DF, Bozzacco L, Keeffe JR et al. 2017. Recurrent potent human neutralizing antibodies to Zika virus in Brazil and Mexico. Cell 169:597–609.e11
    [Google Scholar]
  30. 30.  Zhao H, Fernandez E, Dowd KA et al. 2016. Structural basis of Zika virus-specific antibody protection. Cell 166:1016–27
    [Google Scholar]
  31. 31.  Wang J, Bardelli M, Espinosa DA et al. 2017. A human bi-specific antibody against Zika virus with high therapeutic potential. Cell 171:229–41.e15
    [Google Scholar]
  32. 32.  Swanstrom JA, Plante JA, Plante KS 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]
  33. 33.  Fernandez E, Dejnirattisai W, Cao B et al. 2017. Human antibodies to the dengue virus E-dimer epitope have therapeutic activity against Zika virus infection. Nat. Immunol. 18:1261–69
    [Google Scholar]
  34. 34.  Wang Q, Yang H, Liu X et al. 2016. Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci. Transl. Med. 8:369ra179
    [Google Scholar]
  35. 35.  Dai L, Song J, Lu X et al. 2016. Structures of the Zika virus envelope protein and its complex with a flavivirus broadly protective antibody. Cell Host Microbe 19:696–704
    [Google Scholar]
  36. 36.  Barba-Spaeth G, Dejnirattisai W, Rouvinski A et al. 2016. Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nature 536:48–53
    [Google Scholar]
  37. 37.  Abbink P, Larocca RA, Dejnirattisai W et al. 2018. Therapeutic and protective efficacy of a dengue antibody against Zika infection in rhesus monkeys. Nat. Med. 24:721–23
    [Google Scholar]
  38. 38.  Hasan SS, Miller A, Sapparapu G et al. 2017. A human antibody against Zika virus crosslinks the E protein to prevent infection. Nat. Commun. 8:14722
    [Google Scholar]
  39. 39.  Priyamvada L, Quicke KM, Hudson WH et al. 2016. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. PNAS 113:7852–57
    [Google Scholar]
  40. 40.  Halstead SB 1988. Pathogenesis of dengue: challenges to molecular biology. Science 239:476–81
    [Google Scholar]
  41. 41.  Bardina SV, Bunduc P, Tripathi S et al. 2017. Enhancement of Zika virus pathogenesis by preexisting antiflavivirus immunity. Science 356:175–80
    [Google Scholar]
  42. 42.  Dejnirattisai W, Supasa P, Wongwiwat W et al. 2016. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with Zika virus. Nat. Immunol. 17:1102–8
    [Google Scholar]
  43. 43.  Stettler K, Beltramello M, Espinosa DA et al. 2016. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353:823–26
    [Google Scholar]
  44. 44.  McCracken MK, Gromowski GD, Friberg HL et al. 2017. Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques. PLOS Pathog 13:e1006487
    [Google Scholar]
  45. 45.  Terzian ACB, Schanoski AS, Mota MTO et al. 2017. Viral load and cytokine response profile does not support antibody-dependent enhancement in dengue-primed Zika virus-infected patients. Clin. Infect. Dis. 65:1260–65
    [Google Scholar]
  46. 46.  Pardy RD, Rajah MM, Condotta SA et al. 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]
  47. 47.  Grifoni A, Pham J, Sidney J et al. 2017. Prior dengue virus exposure shapes T cell immunity to Zika virus in humans. J. Virol. 91:e01469–17
    [Google Scholar]
  48. 48.  Elong Ngono A, Vizcarra EA, Tang WW 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]
  49. 49.  Dudley DM, Aliota MT, Mohr EL et al. 2016. A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun. 7:12204
    [Google Scholar]
  50. 50.  Wen J, Tang WW, Sheets N 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]
  51. 51.  Badolato-Correa J, Sanchez-Arcila JC, Alves de Souza TM et al. 2017. Human T cell responses to Dengue and Zika virus infection compared to Dengue/Zika coinfection. Immunity Inflamm. Dis. 6:194–206
    [Google Scholar]
  52. 52.  Weiskopf D, Angelo MA, de Azeredo EL 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]
  53. 53.  Huang H, Li S, Zhang Y et al. 2017. CD8+ T cell immune response in immunocompetent mice during Zika virus infection. J. Virol. 91. pii:e00900–17
    [Google Scholar]
  54. 54.  Wen J, Elong Ngono A, Regla-Nava JA et al. 2017. Dengue virus-reactive CD8+ T cells mediate cross-protection against subsequent Zika virus challenge. Nat. Commun. 8:1459
    [Google Scholar]
  55. 55.  Jurado KA, Yockey LJ, Wong PW et al. 2017. Antiviral CD8 T cells induce Zika-virus-associated paralysis in mice. Nat. Microbiol. 3:141–47
    [Google Scholar]
  56. 56.  Lucas CGO, Kitoko JZ, Ferreira FM et al. 2018. Critical role of CD4+ T cells and IFNγ signaling in antibody-mediated resistance to Zika virus infection. Nature Commun 9:3136
    [Google Scholar]
  57. 57.  Lai L, Rouphael N, Xu Y et al. 2017. Innate, T and B cell responses in acute human Zika patients. Clin. Infect. Dis. 66:1–10
    [Google Scholar]
  58. 58.  Cimini E, Castilletti C, Sacchi A et al. 2017. Human Zika infection induces a reduction of IFN-γ producing CD4 T-cells and a parallel expansion of effector Vδ2 T-cells. Sci. Rep. 7:6313
    [Google Scholar]
  59. 59.  Rey FA, Stiasny K, Vaney MC et al. 2018. The bright and the dark side of human antibody responses to flaviviruses: lessons for vaccine design. EMBO Rep 19:206–24
    [Google Scholar]
  60. 60.  Schalich J, Allison SL, Stiasny K et al. 1996. Recombinant subviral particles from tick-borne encephalitis virus are fusogenic and provide a model system for studying flavivirus envelope glycoprotein functions. J. Virol. 70:4549–57
    [Google Scholar]
  61. 61.  Ferlenghi I, Clarke M, Ruttan T et al. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593–602
    [Google Scholar]
  62. 62.  Plevka P, Battisti AJ, Junjhon J et al. 2011. Maturation of flaviviruses starts from one or more icosahedrally independent nucleation centres. EMBO Rep 12:602–6
    [Google Scholar]
  63. 63.  Pierson TC, Diamond MS 2012. Degrees of maturity: the complex structure and biology of flaviviruses. Curr. Opin. Virol. 2:168–75
    [Google Scholar]
  64. 64.  Dowd KA, Ko SY, Morabito KM et al. 2016. Rapid development of a DNA vaccine for Zika virus. Science 354:237–40
    [Google Scholar]
  65. 65.  Davis BS, Chang GJ, Cropp B et al. 2001. West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J. Virol. 75:4040–47
    [Google Scholar]
  66. 66.  Ledgerwood JE, Pierson TC, Hubka SA et al. 2011. A West Nile virus DNA vaccine utilizing a modified promoter induces neutralizing antibody in younger and older healthy adults in a phase I clinical trial. J. Infect. Dis. 203:1396–404
    [Google Scholar]
  67. 67.  Gaudinski MR, Houser KV, Morabito KM et al. 2017. Safety, tolerability, and immunogenicity of two Zika virus DNA vaccine candidates in healthy adults: randomised, open-label, phase 1 clinical trials. Lancet 391:552–62
    [Google Scholar]
  68. 68.  Griffin BD, Muthumani K, Warner BM et al. 2017. DNA vaccination protects mice against Zika virus-induced damage to the testes. Nat. Commun. 8:15743
    [Google Scholar]
  69. 69.  Tebas P, Roberts CC, Muthumani K et al. 2017. Safety and immunogenicity of an anti-Zika virus DNA vaccine—preliminary report. N. Engl. J. Med. https://www.nejm.org/doi/10.1056/NEJMoa1708120
  70. 70.  Abbink P, Larocca RA, De La Barrera RA et al. 2016. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science 353:1129–32
    [Google Scholar]
  71. 71.  Larocca RA, Abbink P, Peron JP et al. 2016. Vaccine protection against Zika virus from Brazil. Nature 536:474–78
    [Google Scholar]
  72. 72.  Pardi N, Hogan MJ, Porter FW et al. 2018. mRNA vaccines—a new era in vaccinology. Nat. Rev. Drug Discov. 17:261–79
    [Google Scholar]
  73. 73.  Pardi N, Hogan MJ, Pelc RS et al. 2017. Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination. Nature 543:248–51
    [Google Scholar]
  74. 74.  Richner JM, Himansu S, Dowd KA et al. 2017. Modified mRNA vaccines protect against Zika virus infection. Cell 168:1114–25.e10
    [Google Scholar]
  75. 75.  Richner JM, Jagger BW, Shan C et al. 2017. Vaccine mediated protection against Zika virus-induced congenital disease. Cell 170:273–83.e12
    [Google Scholar]
  76. 76.  Pardi N, Hogan MJ, Pelc RS et al. 2017. Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination. Nature 543:248–51
    [Google Scholar]
  77. 77.  Richner JM, Himansu S, Dowd KA et al. 2017. Modified mRNA vaccines protect against Zika virus infection. Cell 169:176
    [Google Scholar]
  78. 78.  Sumathy K, Kulkarni B, Gondu RK et al. 2017. Protective efficacy of Zika vaccine in AG129 mouse model. Sci. Rep. 7:46375
    [Google Scholar]
  79. 79.  Larocca RA, Abbink P, Peron JP et al. 2016. Vaccine protection against Zika virus from Brazil. Nature 536:474–78
    [Google Scholar]
  80. 80.  Abbink P, Larocca RA, Visitsunthorn K et al. 2017. Durability and correlates of vaccine protection against Zika virus in rhesus monkeys. Sci. Transl. Med 9:eaao4163
    [Google Scholar]
  81. 81.  Xie X, Yang Y, Muruato AE et al. 2017. Understanding Zika virus stability and developing a chimeric vaccine through functional analysis. mBio 8:e02134–16
    [Google Scholar]
  82. 82.  Shan C, Muruato AE, Nunes BTD et al. 2017. A live-attenuated Zika virus vaccine candidate induces sterilizing immunity in mouse models. Nat. Med. 23:763–67
    [Google Scholar]
  83. 83.  Shan C, Xie X, Muruato AE et al. 2016. An infectious cDNA clone of Zika virus to study viral virulence, mosquito transmission, and antiviral inhibitors. Cell Host Microbe 19:891–900
    [Google Scholar]
  84. 84.  Shan C, Muruato AE, Jagger BW et al. 2017. A single-dose live-attenuated vaccine prevents Zika virus pregnancy transmission and testis damage. Nat. Commun. 8:676
    [Google Scholar]
  85. 85.  Betancourt D, de Queiroz NM, Xia T et al. 2017. Cutting edge: innate immune augmenting vesicular stomatitis virus expressing Zika virus proteins confers protective immunity. J. Immunol. 198:3023–28
    [Google Scholar]
  86. 86.  Prow NA, Liu L, Nakayama E et al. 2018. A vaccinia-based single vector construct multi-pathogen vaccine protects against both Zika and chikungunya viruses. Nat. Commun. 9:1230
    [Google Scholar]
  87. 87.  Guo Q, Chan JF, Poon VK et al. 2018. Immunization with a novel human type 5 adenovirus-vectored vaccine expressing the premembrane and envelope proteins of Zika virus provides consistent and sterilizing protection in multiple immunocompetent and immunocompromised animal models. J. Infect. Dis. 218:365–77
    [Google Scholar]
  88. 88.  Xu K, Song Y, Dai L et al. 2018. Recombinant chimpanzee adenovirus vaccine AdC7-M/E protects against Zika virus infection and testis damage. J. Virol. 92:e01722–17
    [Google Scholar]
  89. 89.  Brault AC, Domi A, McDonald EM et al. 2017. A Zika vaccine targeting NS1 protein protects immunocompetent adult mice in a lethal challenge model. Sci. Rep. 7:14769
    [Google Scholar]
  90. 90.  Li A, Yu J, Lu M, Ma Y, Attia Z et al. 2018. A Zika virus vaccine expressing premembrane-envelope-NS1 polyprotein. Nature Commun 9:3067
    [Google Scholar]
  91. 91.  Konishi E, Pincus S, Fonseca BA et al. 1991. Comparison of protective immunity elicited by recombinant vaccinia viruses that synthesize E or NS1 of Japanese encephalitis virus. Virology 185:401–10
    [Google Scholar]
  92. 92.  Asher J, Barker C, Chen G et al. 2017. Preliminary results of models to predict areas in the Americas with increased likelihood of Zika virus transmission in 2017. bioRxiv. https://doi.org/10.1101/187591
    [Crossref]
  93. 93.  Martin JE, Pierson TC, Hubka S et al. 2007. A West Nile virus DNA vaccine induces neutralizing antibody in healthy adults during a phase 1 clinical trial. J. Infect. Dis. 196:1732–40
    [Google Scholar]
  94. 94.  Osuna CE, Lim SY, Deleage C et al. 2016. Zika viral dynamics and shedding in rhesus and cynomolgus macaques. Nat. Med. 22:1448–55
    [Google Scholar]
  95. 95.  Modjarrad K, Lin L, George SL et al. 2017. Preliminary aggregate safety and immunogenicity results from three trials of a purified inactivated Zika virus vaccine candidate: phase 1, randomised, double-blind, placebo-controlled clinical trials. Lancet 391:563–71
    [Google Scholar]
  96. 96.  Adams Waldorf KM, Nelson BR, Stencel-Baerenwald JE et al. 2018. Congenital Zika virus infection as a silent pathology with loss of neurogenic output in the fetal brain. Nat. Med. 24:368–74
    [Google Scholar]
  97. 97.  Ribeiro GS, Kikuti M, Tauro LB et al. 2018. Does immunity after Zika virus infection cross-protect against dengue?. Lancet Glob. Health 6:e140–41
    [Google Scholar]
  98. 98.  George J, Valiant WG, Mattapallil MJ et al. 2017. Prior exposure to Zika virus significantly enhances peak dengue-2 viremia in rhesus macaques. Sci. Rep. 7:10498
    [Google Scholar]
  99. 99.  Halstead SB 2018. Safety issues from a Phase 3 clinical trial of a live-attenuated chimeric yellow fever tetravalent dengue vaccine. Hum. Vaccines Immunother. 26:1–5
    [Google Scholar]
/content/journals/10.1146/annurev-med-040717-051127
Loading
/content/journals/10.1146/annurev-med-040717-051127
Loading

Data & Media loading...

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