Prospects for a Zika Virus Vaccine

Immunity

Volumn 46, Issue 2, 2017, Pages 176-182

  Barouch, Dan H ^a,b   Thomas, Stephen J ^c   Michael, Nelson L ^d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; FLAVIVIRUS VACCINE; UNCLASSIFIED DRUG; VIRUS VACCINE; ZIKA VIRUS VACCINE;

HUMAN; IMMUNOLOGY; NONHUMAN; PRECLINICAL STUDY; PRIORITY JOURNAL; REVIEW; VACCINATION; ZIKA FEVER; ANIMAL; ZIKA VIRUS; ZIKA VIRUS INFECTION;

ANIMALS; HUMANS; VIRAL VACCINES; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85013977459     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.02.005     Document Type: Review

References (78)

1. Abbink, P., Larocca, R.A., De La Barrera, R.A., Bricault, C.A., Moseley, E.T., Boyd, M., Kirilova, M., Li, Z., Ng'ang'a, D., Nanayakkara, O., et al. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science 353 (2016), 1129–1132.
2. Adams Waldorf, K.M., Stencel-Baerenwald, J.E., Kapur, R.P., Studholme, C., Boldenow, E., Vornhagen, J., Baldessari, A., Dighe, M.K., Thiel, J., Merillat, S., et al. Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate. Nat. Med. 22 (2016), 1256–1259.
3. Atkinson, B., Thorburn, F., Petridou, C., Bailey, D., Hewson, R., Simpson, A.J., Brooks, T.J., Aarons, E.J., Presence and persistence of Zika virus RNA in semen, United Kingdom, 2016. Emerg. Infect. Dis., 23, 2017, 23.
4. Barba-Spaeth, G., Dejnirattisai, W., Rouvinski, A., Vaney, M.C., Medits, I., Sharma, A., Simon-Lorière, E., Sakuntabhai, A., Cao-Lormeau, V.M., Haouz, A., et al. Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nature 536 (2016), 48–53.
5. Bista, M.B., Banerjee, M.K., Shin, S.H., Tandan, J.B., Kim, M.H., Sohn, Y.M., Ohrr, H.C., Tang, J.L., Halstead, S.B., Efficacy of single-dose SA 14-14-2 vaccine against Japanese encephalitis: a case control study. Lancet 358 (2001), 791–795.
6. Brasil, P., Pereira, J.P. Jr., Moreira, M.E., Ribeiro Nogueira, R.M., Damasceno, L., Wakimoto, M., Rabello, R.S., Valderramos, S.G., Halai, U.A., Salles, T.S., et al. Zika virus infection in pregnant women in Rio de Janeiro. N. Engl. J. Med. 375 (2016), 2321–2334.
7. Brasil, P., Sequeira, P.C., Freitas, A.D., Zogbi, H.E., Calvet, G.A., de Souza, R.V., Siqueira, A.M., de Mendonca, M.C., Nogueira, R.M., de Filippis, A.M., Solomon, T., Guillain-Barré syndrome associated with Zika virus infection. Lancet, 387, 2016, 1482.
8. Burke, D.S., Nisalak, A., Johnson, D.E., Scott, R.M., A prospective study of dengue infections in Bangkok. Am. J. Trop. Med. Hyg. 38 (1988), 172–180.
9. Cao-Lormeau, V.M., Blake, A., Mons, S., Lastère, S., Roche, C., Vanhomwegen, J., Dub, T., Baudouin, L., Teissier, A., Larre, P., et al. Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387 (2016), 1531–1539.
10. Charles, A.S., Christofferson, R.C., Utility of a dengue-derived monoclonal antibody to enhance Zika infection in vitro. PLoS Curr., 8, 2016, 8.
11. Cugola, F.R., Fernandes, I.R., Russo, F.B., Freitas, B.C., Dias, J.L., Guimarães, K.P., Benazzato, C., Almeida, N., Pignatari, G.C., Romero, S., et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534 (2016), 267–271.
12. D'Ortenzio, E., Matheron, S., Yazdanpanah, Y., de Lamballerie, X., Hubert, B., Piorkowski, G., Maquart, M., Descamps, D., Damond, F., Leparc-Goffart, I., Evidence of sexual transmission of Zika virus. N. Engl. J. Med. 374 (2016), 2195–2198.
13. Dejnirattisai, W., Supasa, P., Wongwiwat, W., Rouvinski, A., Barba-Spaeth, G., Duangchinda, T., Sakuntabhai, A., Cao-Lormeau, V.M., Malasit, P., Rey, F.A., et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat. Immunol. 17 (2016), 1102–1108.
14. Dos Santos, T., Rodriguez, A., Almiron, M., Sanhueza, A., Ramon, P., de Oliveira, W.K., Coelho, G.E., Badaró, R., Cortez, J., Ospina, M., et al. Zika virus and the Guillain-Barré syndrome - case series from seven countries. N. Engl. J. Med. 375 (2016), 1598–1601.
15. Dowd, K.A., DeMaso, C.R., Pelc, R.S., Speer, S.D., Smith, A.R., Goo, L., Platt, D.J., Mascola, J.R., Graham, B.S., Mulligan, M.J., et al. Broadly neutralizing activity of Zika virus-immune sera identifies a single viral serotype. Cell Rep. 16 (2016), 1485–1491.
16. Dowd, K.A., Ko, S.Y., Morabito, K.M., Yang, E.S., Pelc, R.S., DeMaso, C.R., Castilho, L.R., Abbink, P., Boyd, M., Nityanandam, R., et al. Rapid development of a DNA vaccine for Zika virus. Science 354 (2016), 237–240.
17. Driggers, R.W., Ho, C.Y., Korhonen, E.M., Kuivanen, S., Jääskeläinen, A.J., Smura, T., Rosenberg, A., Hill, D.A., DeBiasi, R.L., Vezina, G., et al. Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N. Engl. J. Med. 374 (2016), 2142–2151.
18. Dudley, D.M., Aliota, M.T., Mohr, E.L., Weiler, A.M., Lehrer-Brey, G., Weisgrau, K.L., Mohns, M.S., Breitbach, M.E., Rasheed, M.N., Newman, C.M., et al. A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun., 7, 2016, 12204.
19. Duffy, M.R., Chen, T.H., Hancock, W.T., Powers, A.M., Kool, J.L., Lanciotti, R.S., Pretrick, M., Marfel, M., Holzbauer, S., Dubray, C., et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 360 (2009), 2536–2543.
20. Elong Ngono, A., Vizcarra, E.A., Tang, W.W., Sheets, N., Joo, Y., Kim, K., Gorman, M.J., Diamond, M.S., Shresta, S., Mapping and role of the CD8(+) T cell response during primary Zika virus infection in mice. Cell Host Microbe 21 (2017), 35–46.
21. Fauci, A.S., Morens, D.M., Zika virus in the Americas–yet another arbovirus threat. N. Engl. J. Med. 374 (2016), 601–604.
22. Garcez, P.P., Loiola, E.C., Madeiro da Costa, R., Higa, L.M., Trindade, P., Delvecchio, R., Nascimento, J.M., Brindeiro, R., Tanuri, A., Rehen, S.K., Zika virus impairs growth in human neurospheres and brain organoids. Science 352 (2016), 816–818.
23. Guirakhoo, F., Zhang, Z.X., Chambers, T.J., Delagrave, S., Arroyo, J., Barrett, A.D., Monath, T.P., Immunogenicity, genetic stability, and protective efficacy of a recombinant, chimeric yellow fever-Japanese encephalitis virus (ChimeriVax-JE) as a live, attenuated vaccine candidate against Japanese encephalitis. Virology 257 (1999), 363–372.
24. Hadinegoro, S.R., Arredondo-García, J.L., Capeding, M.R., Deseda, C., Chotpitayasunondh, T., Dietze, R., Muhammad Ismail, H.I., Reynales, H., Limkittikul, K., Rivera-Medina, D.M., et al., CYD-TDV Dengue Vaccine Working Group. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N. Engl. J. Med. 373 (2015), 1195–1206.
25. Halstead, S.B., Neutralization and antibody-dependent enhancement of dengue viruses. Adv. Virus Res. 60 (2003), 421–467.
26. Halstead, S.B., Thomas, S.J., New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev. Vaccines 10 (2011), 355–364.
27. Halstead, S.B., Chow, J.S., Marchette, N.J., Immunological enhancement of dengue virus replication. Nat. New Biol. 243 (1973), 24–26.
28. Henao-Restrepo, A.M., Longini, I.M., Egger, M., Dean, N.E., Edmunds, W.J., Camacho, A., Carroll, M.W., Doumbia, M., Draguez, B., Duraffour, S., et al. Efficacy and effectiveness of an rVSV-vectored vaccine expressing Ebola surface glycoprotein: interim results from the Guinea ring vaccination cluster-randomised trial. Lancet 386 (2015), 857–866.
29. Hombach, J., Solomon, T., Kurane, I., Jacobson, J., Wood, D., Report on a WHO consultation on immunological endpoints for evaluation of new Japanese encephalitis vaccines, WHO, Geneva, 2-3 September, 2004. Vaccine 23 (2005), 5205–5211.
30. Honein, M.A., Dawson, A.L., Petersen, E.E., Jones, A.M., Lee, E.H., Yazdy, M.M., Ahmad, N., Macdonald, J., Evert, N., Bingham, A., et al., US Zika Pregnancy Registry Collaboration. Birth defects among fetuses and infants of US women with evidence of possible Zika virus infection during pregnancy. JAMA 317 (2017), 59–68.
31. Ishikawa, T., Yamanaka, A., Konishi, E., A review of successful flavivirus vaccines and the problems with those flaviviruses for which vaccines are not yet available. Vaccine 32 (2014), 1326–1337.
32. Jarmer, J., Zlatkovic, J., Tsouchnikas, G., Vratskikh, O., Strauß, J., Aberle, J.H., Chmelik, V., Kundi, M., Stiasny, K., Heinz, F.X., Variation of the specificity of the human antibody responses after tick-borne encephalitis virus infection and vaccination. J. Virol. 88 (2014), 13845–13857.
33. Johansson, M.A., Mier-y-Teran-Romero, L., Reefhuis, J., Gilboa, S.M., Hills, S.L., Zika and the risk of microcephaly. N. Engl. J. Med. 375 (2016), 1–4.
34. Kawiecki, A.B., Christofferson, R.C., Zika virus-induced antibody response enhances dengue virus serotype 2 replication in vitro. J. Infect. Dis. 214 (2016), 1357–1360.
35. Kliks, S.C., Nimmanitya, S., Nisalak, A., Burke, D.S., Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am. J. Trop. Med. Hyg. 38 (1988), 411–419.
36. Kliks, S.C., Nisalak, A., Brandt, W.E., Wahl, L., Burke, D.S., Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am. J. Trop. Med. Hyg. 40 (1989), 444–451.
37. Kreil, T.R., Burger, I., Bachmann, M., Fraiss, S., Eibl, M.M., Antibodies protect mice against challenge with tick-borne encephalitis virus (TBEV)-infected macrophages. Clin. Exp. Immunol. 110 (1997), 358–361.
38. Laoprasopwattana, K., Libraty, D.H., Endy, T.P., Nisalak, A., Chunsuttiwat, S., Vaughn, D.W., Reed, G., Ennis, F.A., Rothman, A.L., Green, S., Dengue Virus (DV) enhancing antibody activity in preillness plasma does not predict subsequent disease severity or viremia in secondary DV infection. J. Infect. Dis. 192 (2005), 510–519.
39. Larocca, R.A., Abbink, P., Peron, J.P., Zanotto, P.M., Iampietro, M.J., Badamchi-Zadeh, A., Boyd, M., Ng'ang'a, D., Kirilova, M., Nityanandam, R., et al. Vaccine protection against Zika virus from Brazil. Nature 536 (2016), 474–478.
40. Lazear, H.M., Govero, J., Smith, A.M., Platt, D.J., Fernandez, E., Miner, J.J., Diamond, M.S., A Mouse model of Zika virus pathogenesis. Cell Host Microbe 19 (2016), 720–730.
41. Ledgerwood, J.E., Wei, C.J., Hu, Z., Gordon, I.J., Enama, M.E., Hendel, C.S., McTamney, P.M., Pearce, M.B., Yassine, H.M., Boyington, J.C., et al., VRC 306 Study Team. DNA priming and influenza vaccine immunogenicity: two phase 1 open label randomised clinical trials. Lancet Infect. Dis. 11 (2011), 916–924.
42. Li, C., Xu, D., Ye, Q., Hong, S., Jiang, Y., Liu, X., Zhang, N., Shi, L., Qin, C.F., Xu, Z., Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19 (2016), 120–126.
43. Libraty, D.H., Acosta, L.P., Tallo, V., Segubre-Mercado, E., Bautista, A., Potts, J.A., Jarman, R.G., Yoon, I.K., Gibbons, R.V., Brion, J.D., Capeding, R.Z., A prospective nested case-control study of dengue in infants: rethinking and refining the antibody-dependent enhancement dengue hemorrhagic fever model. PLoS Med., 6, 2009, e1000171.
44. Marston, H.D., Lurie, N., Borio, L.L., Fauci, A.S., Considerations for developing a Zika virus vaccine. N. Engl. J. Med. 375 (2016), 1209–1212.
45. Mason, R.A., Tauraso, N.M., Spertzel, R.O., Ginn, R.K., Yellow fever vaccine: direct challenge of monkeys given graded doses of 17D vaccine. Appl. Microbiol. 25 (1973), 539–544.
46. Matheron, S., d'Ortenzio, E., Leparc-Goffart, I., Hubert, B., de Lamballerie, X., Yazdanpanah, Y., Long-lasting persistence of Zika virus in semen. Clin. Infect. Dis., 63, 2016, 1264.
47. Melo, A.S., Aguiar, R.S., Amorim, M.M., Arruda, M.B., Melo, F.O., Ribeiro, S.T., Batista, A.G., Ferreira, T., Dos Santos, M.P., Sampaio, V.V., et al. Congenital Zika virus infection: beyond neonatal microcephaly. JAMA Neurol. 73 (2016), 1407–1416.
48. Miner, J.J., Cao, B., Govero, J., Smith, A.M., Fernandez, E., Cabrera, O.H., Garber, C., Noll, M., Klein, R.S., Noguchi, K.K., et al. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165 (2016), 1081–1091.
49. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., et al. Zika virus associated with microcephaly. N. Engl. J. Med. 374 (2016), 951–958.
50. Muthumani, K., Griffin, B.D., Agarwal, S., Kudchodkar, S.B., Reuschel, E.L., Choi, H., Kraynyak, K.A., Duperret, E.K., Keaton, A.A., Chung, C., et al. In vivo protection against ZIKV infection and pathogenesis through passive antibody transfer and active immunisation with a prMEnv DNA vaccine. NPJ Vaccines, 2016, 10.1038/npjvaccines.2016.21 Published online November 10, 2016.
51. Osuna, C.E., Lim, S.Y., Deleage, C., Griffin, B.D., Stein, D., Schroeder, L.T., Omange, R., Best, K., Luo, M., Hraber, P.T., et al. Zika viral dynamics and shedding in rhesus and cynomolgus macaques. Nat. Med. 22 (2016), 1448–1455.
52. Pardi, N., Hogan, M.J., Pelc, R.S., Muramatsu, H., Andersen, H., DeMaso, C.R., Dowd, K.A., Sutherland, L.L., Scearce, R.M., Parks, R., et al. Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination. Nature, 2017, 10.1038/nature21428.
53. Parra, B., Lizarazo, J., Jiménez-Arango, J.A., Zea-Vera, A.F., González-Manrique, G., Vargas, J., Angarita, J.A., Zuñiga, G., Lopez-Gonzalez, R., Beltran, C.L., et al. Guillain-Barré syndrome associated with Zika virus infection in Colombia. N. Engl. J. Med. 375 (2016), 1513–1523.
54. Petersen, L.R., Jamieson, D.J., Powers, A.M., Honein, M.A., Zika virus. N. Engl. J. Med. 374 (2016), 1552–1563.
55. Pierson, T.C., Graham, B.S., Zika virus: immunity and vaccine development. Cell 167 (2016), 625–631.
56. Pinto, A.K., Brien, J.D., Lam, C.Y., Johnson, S., Chiang, C., Hiscott, J., Sarathy, V.V., Barrett, A.D., Shresta, S., Diamond, M.S., Defining new therapeutics using a more immunocompetent mouse model of antibody-enhanced dengue virus infection. MBio, 6, 2015 e01316–e15.
57. Plotkin, S.A., Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47 (2008), 401–409.
58. Plotkin, S.A., Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17 (2010), 1055–1065.
59. Qian, X., Nguyen, H.N., Song, M.M., Hadiono, C., Ogden, S.C., Hammack, C., Yao, B., Hamersky, G.R., Jacob, F., Zhong, C., et al. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165 (2016), 1238–1254.
60. Rabe, I.B., Staples, J.E., Villanueva, J., Hummel, K.B., Johnson, J.A., Rose, L., Hills, S., Wasley, A., Fischer, M., Powers, A.M., MTS. Interim guidance for interpretation of Zika virus antibody test results. MMWR Morb. Mortal. Wkly. Rep. 65 (2016), 543–546.
61. Rasmussen, S.A., Jamieson, D.J., Honein, M.A., Petersen, L.R., Zika virus and birth defects–reviewing the evidence for causality. N. Engl. J. Med. 374 (2016), 1981–1987.
62. Rothman, A.L., Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11 (2011), 532–543.
63. Russell, P.K., Udomsakdi, S., Halstead, S.B., Antibody response in dengue and dengue hemorrhagic fever. Jpn. J. Med. Sci. Biol. 20:Suppl (1967), 103–108.
64. Sabchareon, A., Wallace, D., Sirivichayakul, C., Limkittikul, K., Chanthavanich, P., Suvannadabba, S., Jiwariyavej, V., Dulyachai, W., Pengsaa, K., Wartel, T.A., et al. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380 (2012), 1559–1567.
65. Sapparapu, G., Fernandez, E., Kose, N., Bin Cao, Fox, J.M., Bombardi, R.G., Zhao, H., Nelson, C.A., Bryan, A.L., Barnes, T., et al. Neutralizing human antibodies prevent Zika virus replication and fetal disease in mice. Nature 540 (2016), 443–447.
66. Savidis, G., Perreira, J.M., Portmann, J.M., Meraner, P., Guo, Z., Green, S., Brass, A.L., The IFITMs inhibit Zika virus replication. Cell Rep. 15 (2016), 2323–2330.
67. Spector, S., Tauraso, N.M., Yellow fever virus. I. Development and evaluation of a plaque neutralization test. Appl. Microbiol. 16 (1968), 1770–1775.
68. Stettler, K., Beltramello, M., Espinosa, D.A., Graham, V., Cassotta, A., Bianchi, S., Vanzetta, F., Minola, A., Jaconi, S., Mele, F., et al. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353 (2016), 823–826.
69. Swanstrom, J.A., Plante, J.A., Plante, K.S., Young, E.F., McGowan, E., Gallichotte, E.N., Widman, D.G., Heise, M.T., de Silva, A.M., Baric, R.S., Dengue virus envelope dimer epitope monoclonal antibodies isolated from dengue patients are protective against Zika virus. MBio, 7, 2016, 7.
70. Tauber, E., Kollaritsch, H., Korinek, M., Rendi-Wagner, P., Jilma, B., Firbas, C., Schranz, S., Jong, E., Klingler, A., Dewasthaly, S., Klade, C.S., Safety and immunogenicity of a Vero-cell-derived, inactivated Japanese encephalitis vaccine: a non-inferiority, phase III, randomised controlled trial. Lancet 370 (2007), 1847–1853.
71. Thomas, S.J., L'Azou, M., Barrett, A.D., Jackson, N.A., Fast-track Zika vaccine development - is it possible?. N. Engl. J. Med. 375 (2016), 1212–1216.
72. Vaughn, D.W., Green, S., Kalayanarooj, S., Innis, B.L., Nimmannitya, S., Suntayakorn, S., Endy, T.P., Raengsakulrach, B., Rothman, A.L., Ennis, F.A., Nisalak, A., Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J. Infect. Dis. 181 (2000), 2–9.
73. Venturi, G., Mel, R., Marchi, A., Mancuso, S., Russino, F., Pra, G.D., Papa, N., Bertiato, G., Fiorentini, C., Ciufolini, M.G., Humoral immunity and correlation between ELISA, hemagglutination inhibition, and neutralization tests after vaccination against tick-borne encephalitis virus in children. J. Virol. Methods 134 (2006), 136–139.
74. Villar, L., Dayan, G.H., Arredondo-García, J.L., Rivera, D.M., Cunha, R., Deseda, C., Reynales, H., Costa, M.S., Morales-Ramírez, J.O., Carrasquilla, G., et al., CYD15 Study Group. Efficacy of a tetravalent dengue vaccine in children in Latin America. N. Engl. J. Med. 372 (2015), 113–123.
75. Wang, Q., Yang, H., Liu, X., Dai, L., Ma, T., Qi, J., Wong, G., Peng, R., Liu, S., Li, J., et al. Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci. Transl. Med., 8, 2016, 369ra179.
76. WHO. Japanese Encephalitis Vaccines: WHO position paper, February 2015–Recommendations. Vaccine 34 (2016), 302–303.
77. Yockey, L.J., Varela, L., Rakib, T., Khoury-Hanold, W., Fink, S.L., Stutz, B., Szigeti-Buck, K., Van den Pol, A., Lindenbach, B.D., Horvath, T.L., Iwasaki, A., Vaginal exposure to Zika virus during pregnancy leads to fetal brain infection. Cell 166 (2016), 1247–1256.e4.
78. Zhao, H., Fernandez, E., Dowd, K.A., Speer, S.D., Platt, D.J., Gorman, M.J., Govero, J., Nelson, C.A., Pierson, T.C., Diamond, M.S., Fremont, D.H., Structural basis of Zika virus-specific antibody protection. Cell 166 (2016), 1016–1027.