Recent advances in understanding the adaptive immune response to Zika virus and the effect of previous flavivirus exposure

Virus Research

Volumn 254, Issue , 2018, Pages 27-33

  Andrade, Daniela V ^a   Harris, Eva ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibody dependent enhancement; Cross reactivity; Dengue virus; Envelope protein; Flaviviruses; Immunity; Memory B cells; Monoclonal antibody; Neutralizing antibodies; Polyclonal antibody response; Structural immunology; T cells; Zika virus

Indexed keywords

MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; POLYCLONAL ANTIBODY; STRUCTURAL PROTEIN; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN; VIRAL PROTEIN;

ADAPTIVE IMMUNITY; ANTIBODY DEPENDENT ENHANCEMENT; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; B LYMPHOCYTE; CROSS REACTION; DENGUE; DENGUE VIRUS; EXPOSURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; ZIKA FEVER; ZIKA VIRUS; ANIMAL; CROSS PROTECTION; FLAVIVIRUS; IMMUNOLOGY; VIROLOGY;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT ENHANCEMENT; CROSS PROTECTION; DENGUE VIRUS; FLAVIVIRUS; HUMANS; VIRAL PROTEINS; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85026658758     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2017.06.019     Document Type: Review

References (96)

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., Nityanandam, R., Mercado, N.B., Borducchi, E.N., Agarwal, A., Brinkman, A.L., Cabral, C., Chandrashekar, A., Giglio, P.B., Jetton, D., Jimenez, J., Lee, B.C., Mojta, S., Molloy, K., Shetty, M., Neubauer, G.H., Stephenson, K.E., Peron, J.P., Zanotto, P.M., Misamore, J., Finneyfrock, B., Lewis, M.G., Alter, G., Modjarrad, K., Jarman, R.G., Eckels, K.H., Michael, N.L., Thomas, S.J., Barouch, D.H., Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science 353:6304 (2016), 1129–1132.
2. Abd El Wahed, A., Sanabani, S.S., Faye, O., Pessôa, R., Patriota, J.V., Giorgi, R.R., Patel, P., Böhlken-Fascher, S., Landt, O., Niedrig, M., Zanotto, P.M., Czerny, C.P., Sall, A.A., Weidmann, M., Rapid molecular detection of Zika virus in acute-phase urine samples using the recombinase polymerase amplification assay. PLoS Curr., 25(9), 2017.
3. Avirutnan, P., Hauhart, R.E., Somnuke, P., Blom, A.M., Diamond, M.S., Atkinson, J.P., Binding of flavivirus nonstructural protein NS1 to C4b binding protein modulates complement activation. J. Immunol. 187:1 (2011), 424–433.
4. Balmaseda, A., Stettler, K., Carrera, R.M., Collado, D., Jin, X., Zambrana, J.V., Jaconi, S., Cameroni, E., Saborio, S., Rovida, F., Percivalle, E., Ijaz, S., Dicks, S., Ushiro-Lumb, I., Barzon, L., Siqueira, P., Brown, D.W.G., Baldanti, F., Tedder, R., Zambon, M., Bispo de Filippis, A.M., Harris, E., Corti, D, A novel antibody-based assay discriminates Zika virus infection from other flaviviruses. Proc. Natl. Acad. Sci. U. S. A., 2017, 10.1073/pnas.1704984114 published ahead of print July 17, 2017.
5. 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., England, P., Stiasny, K., Mongkolsapaya, J., Heinz, F.X., Screaton, G.R., Rey, F.A., Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nat. Commun. 536:7614 (2016), 48–53.
6. Bardina, S., Bunduc, P., Tripathi, S., Duehr, J., Frere, J.J., Brown, J.A., Nachbagauer, R., Foster, G.A., Krysztof, D., Tortorella, D., Stramer, S.L., García-Sastre, A., Krammer, F., Lim, J.K., Enhancement of Zika virus pathogenesis by preexisting antiflavivirus immunity. Science 356:6334 (2017), 175–180.
7. Barzon, L., Pacenti, M., Berto, A., Sinigaglia, A., Franchin, E., Lavezzo, E., Brugnaro, P., Palù G., Isolation of infectious Zika virus from saliva and prolonged viral RNA shedding in a traveller returning from the Dominican Republic to Italy, January 2016. Euro Surveill., 21(10), 2016, 30159.
8. Beatty, P., Puerta-Guardo, H., Killingbeck, S.S., Glasner, D.R., Hopkins, K., Harris, E., Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci. Transl. Med., 7(304), 2015, 304ra141.
9. Beltramello, M., Williams, K.L., Simmons, C.P., Macagno, A., Simonelli, L., Quyen, N.T., Sukupolvi-Petty, S., Navarro-Sanchez, E., Young, P.R., de Silva, A.M., Rey, F.A., Varani, L., Whitehead, S.S., Diamond, M.S., Harris, E., Lanzavecchia, A., Sallusto, F., The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8:3 (2010), 271–283.
10. Besnard, M., Lastere, S., Teissier, A., Cao-Lormeau, V., Musso, D., Evidence of perinatal transmission of Zika virus, French Polynesia, December 2013 and February 2014. Euro Surveill., 19(13), 2014 pii: 20751.
11. Bhatnagar, J., Rabeneck, D.B., Martines, R.B., Reagan-Steiner, S., Ermias, Y., Estetter, L.B., Suzuki, T., Ritter, J., Keating, M.K., Hale, G., Gary, J., Muehlenbachs, A., Lambert, A., Lanciotti, R., Oduyebo, T., Meaney-Delman, D., Bolaños, F., Saad, E.A., Shieh, W.J., Zaki, S.R., Zika virus RNA replication and persistence in brain and placental tissue. Emerg. Infect. Dis. 23:3 (2017), 405–414.
12. Chung, K., Liszewski, M.K., Nybakken, G., Davis, A.E., Townsend, R.R., et al. West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 19111–19116.
13. Collins, M., McGowan, E., Jadi, R., Young, E., Lopez, C.A., Baric, R.S., Lazear, H.M., de Silva, A.M., Lack of durable cross-neutralizing antibodies against Zika virus from dengue virus infection. Emerg. Infect. Dis. 23:5 (2017), 773–781.
14. Dai, L., Song, J., Lu, X., Deng, Y.Q., Musyoki, A.M., Cheng, H., Zhang, Y., Yuan, Y., Song, H., Haywood, J., Xiao, H., Yan, J., Shi, Y., Qin, C.F., Qi, J., Gao, G.F., Structures of the Zika virus envelope protein and its complex with a flavivirus broadly protective antibody. Cell Host Microbe 19:5 (2016), 696–704.
15. Dang, J., Tiwari, S.K., Lichinchi, G., Qin, Y., Patil, V.S., Eroshkin, A.M., Rana, T.M., Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19:2 (2016), 258–265.
16. de Alwis, R., Smith, S.A., Olivarez, N.P., Messer, W.B., Huynh, J.P., Wahala, W.M., White, L.J., Diamond, M.S., Baric, R.S., Crowe, J.E. Jr., de Silva, A.M., Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc. Natl. Acad. Sci. U. S. A. 109:19 (2012), 7439–7444.
17. Dejnirattisai, W., Wongwiwat, W., Supasa, S., Zhang, X., Dai, X., Rouvinski, A., Jumnainsong, A., Edwards, C., Quyen, N.T., Duangchinda, T., Grimes, J.M., Tsai, W.Y., Lai, C.Y., Wang, W.K., Malasit, P., Farrar, J., Simmons, C.P., Zhou, Z.H., Rey, F.A., Mongkolsapaya, J., Screaton, G.R., A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 16:2 (2015), 170–177.
18. Dejnirattisai, W., Supasa, P., Wongwiwat, W., Rouvinski, A., Barba-Spaeth, G., Duangchinda, T., Sakuntabhai, A., Cao-Lormeau, V.M., Malasit, P., Rey, F.A., Mongkolsapaya, J., Screaton, G.R., Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat. Immunol. 17:9 (2016), 1102–1108.
19. Deng, Y., Dai, J.X., Ji, G.H., Jiang, T., Wang, H.J., Yang, H.O., Tan, W.L., Liu, R., Yu, M., Ge, B.X., Zhu, Q.Y., Qin, E.D., Guo, Y.J., Qin, C.F., A broadly flavivirus cross-neutralizing monoclonal antibody that recognizes a novel epitope within the fusion loop of E protein. PLoS One, 6(1), 2011, 16059.
20. de Oliveira, K., Cortez-Escalante, J., de Oliveira, W.T., do Carmo, G.M., Henriques, C.M., Coelho, G.E., Araujo de Franca, G.V., Increase in reported prevalence of microcephaly in infants born to women living in areas with confirmed Zika virus transmission during the first trimester of pregnancy – Brazil, 2015. MMWR. Morb. Mortal. Wkly. Rep. 65:9 (2016), 242–247.
21. do Rosário, M., de Jesus, P.A., Vasilakis, N., Farias, D.S., Novaes, M.A., Rodrigues, S.G., Martins, L.C., Vasconcelos, P.F., Ko, A.I., Alcântara, L.C., de Siqueira, I.C., Guillain-Barré syndrome after Zika virus infection in Brazil. Am. J. Trop. Med. Hyg. 95:5 (2016), 1157–1160.
22. Driggers, R., Ho, C.Y., Korhonen, E.M., Kuivanen, S., Jääskeläinen, A.J., Smura, T., Rosenberg, A., Hill, D.A., DeBiasi, R.L., Vezina, G., Timofeev, J., Rodriguez, F.J., Levanov, L., Razak, J., Iyengar, P., Hennenfent, A., Kennedy, R., Lanciotti, R., du Plessis, A., Vapalahti, O.V., Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N. Engl. J. Med. 374:22 (2016), 2142–2151.
23. Duangchinda, T., Dejnirattisai, W., Vasanawathana, S., Limpitikul, W., Tangthawornchaikul, N., Malasit, P., Mongkolsapaya, J., Screaton, G., Immunodominant T-cell responses to dengue virus NS3 are associated with DHF. Proc. Natl. Acad. Sci. U. S. A. 107:39 (2010), 16922–16927.
24. Duffy, M., Chen, T.H., Hancock, W.T., Powers, A.M., Kool, J.L., Lanciotti, R.S., Pretrick, M., Marfel, M., Holzbauer, S., Dubray, C., Guillaumot, L., Griggs, A., Bel, M., Lambert, A.J., Laven, J., Kosoy, O., Panella, A., Biggerstaff, B.J., Fischer, M., Hayes, E.B., Zika virus outbreak on Yap island: Federated States of Micronesia. N. Engl. J. Med. 360:24 (2009), 2536–2543.
25. Dung, N.T., Duyen, H.T., Thuy, N.T., Ngoc, T.V., Chau, N.V., Hien, T.T., Rowland-Jones, S.L., Dong, T., Farrar, J., Wills, B., Simmons, C.P., Timing of CD8+ T cell responses in relation to commencement of capillary leakage in children with dengue. J. Immunol. 184:12 (2010), 7281–7287.
26. Elong, N., Vizcarra, A., Tang, E.A., Sheets, W.W., Joo, N., Kim, Y., Gorman, K., Diamond, M.J., Shresta, M.S., Mapping and role of the CD8 + T cell response during primary Zika virus infection in mice. Cell Host Microbe 21:1 (2017), 35–46.
27. European Centre for Disease Prevention and Control (ECDC) 2016. Current Zika transmission.
28. Fagbami, A., Halstead, S.B., Marchette, N.J., Larsen, K., Cross-infection enhancement among African flaviviruses by immune mouse ascitic fluids. Cytobios 49:196 (1987), 49–55.
29. Faria, N., Quick, J., Claro, I.M., Thézé J., de Jesus, J.G., Giovanetti, M., Kraemer, M.U.G., Hill, S.C., Black, A., da Costa, A.C., Franco, L.C., Silva, S.P., Wu, C.H., Raghwani, J., Cauchemez, S., du Plessis, L., Verotti, M.P., de Oliveira, W.K., Carmo, E.H., Coelho, G.E., Santelli, A.C.F., Vinhal, L.C., Henriques, C.M., Simpson, J.T., Loose, M., Andersen, K.G., Grubaugh, N.D., Somasekar, S., Chiu, C.Y., Muñoz-Medina, J.E., Gonzalez-Bonilla, C.R., Arias, C.F., Lewis-Ximenez, L.L., Baylis, S.A., Chieppe, A.O., Aguiar, S.F., Fernandes, C.A., Lemos, P.S., Nascimento, B.L.S., Monteiro, H.A.O., Siqueira, I.C., de Queiroz, M.G., de Souza, T.R., Bezerra, J.F., Lemos, M.R., Pereira, G.F., Loudal, D., Moura, L.C., Dhalia, R., França, R.F., Magalhães, T., Marques, E.T., Jaenisch, T., Wallau, G.L., de Lima, M.C., Nascimento, V., de Cerqueira, E.M., de Lima, M.M., Mascarenhas, D.L., Neto, J.P.M., Levin, A.S., Tozetto-Mendoza, T.R., Fonseca, S.N., Mendes-Correa, M.C., Milagres, F.P., Segurado, A., Holmes, E.C., Rambaut, A., Bedford, T., Nunes, M.R.T., Sabino, E.C., Alcantara, L.C.J., Loman, N.J., Pybus, O.G., Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature 546:7658 (2017), 406–410.
30. Fibriansah, G., Tan, J.L., Smith, S.A., de Alwis, A.R., Ng, T.S., Kostyuchenko, V.A., Ibarra, K.D., Wang, J., Harris, E., de Silva, A., Crowe, J.E. Jr., Lok, S.M., A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol. Med. 6:3 (2014), 358–371.
31. Fibriansah, G.T.J., Smith, S.A., de Alwis, R., Ng, T.S., Kostyuchenko, V.A., Jadi, R.S., Kukkaro, P., de Silva, A.M., Crowe, J.E., Lok, S.M., A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat. Commun., 20, 2015, 6341.
32. Gallichotte, E., Widman, D.G., Yount, B.L., Wahala, W.M., Durbin, A., Whitehead, S., Sariol, C.A., Crowe, J.E. Jr., de Silva, A.M., Baric, R.S., A new quaternary structure epitope on dengue virus serotype 2 is the target of durable type-specific neutralizing antibodies. MBio, 6(5), 2015, e01461.
33. Gourinat, A., O'Connor, O., Calvez, E., Goarant, C., Dupont-Rouzeyrol, M., Detection of Zika virus in urine. Emerg. Infect. Dis. 21:1 (2015), 84–86.
34. Govero, J., Esakky, P., Scheaffer, S.M., Fernandez, S., Drury, A., Platt, D.J., Gorman, M.J., Richner, J.M., Caine, E.A., Salazar, V., Moley, K.H., Diamond, M.S., Nature 540 (2017), 438–442.
35. Guzman, M., Alvarez, M., Halstead, S.B., Neutralization and antibody-dependent enhancement of dengue viruses. Adv. Virus Res. 60 (2003), 421–467.
36. Guzman, M., Alvarez, M., Halstead, S.B., Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch. Virol. 158:7 (2013), 1445–1459.
37. Haddow, A., Schuh, A.J., Yasuda, C.Y., Kasper, M.R., Heang, V., Huy, R., Guzman, H., Tesh, R.B., Weaver, S.C., Genetic characterization of Zika virus strains: geographic expansion of the asian lineage. PLoS Negl. Trop. Dis., 6(2), 2012, e1477.
38. Halstead, S., Yamarata, C., Recent epidemics of hemorrhagic fever in Thailand: bservations related to pathogenesis of a new dengue disease. J 55 (1965), 1386–1395.
39. Halstead, S., Nimmannitya, S., Cohen, S.N., Observations related to pathogenesis of dengue hemorrhagic fever: IV. Relation of disease severity to antibody response and virus recovered. Yale J. Biol. Med. 42 (1970), 311–328.
40. Halstead, S., Pathogenesis of dengue: challenges to molecular biology. Science 239:4839 (1988), 476–481.
41. Halstead, S., Neutralization and antibody-dependent enhancement of dengue viruses. Adv. Virus Res. 60 (2003), 421–467.
42. Hasan, S., Miller, A., Sapparapu, G., Fernandez, E., Klose, T., Long, F., Fokine, A., Porta, J.C., Jiang, W., Diamond, M.S., Crowe, J.E. Jr., Kuhn, R.J., Rossmann, M.G., A human antibody against Zika virus crosslinks the E protein to prevent infection. Nat. Commun., 8, 2017, 14722.
43. Herriman, R., 2015. Transfusion-associated Zika virus reported in Brazil. Outbreak News Today.
44. Hills, S., Russell, K., Hennessey, M., Williams, C., Oster, A.M., Fischer, M., Mead, P., Transmission of Zika virus through sexual contact with travelers to areas of ongoing transmission – continental United States, 2016. MMWR. Morb. Mortal. Wkly. Rep. 65:8 (2016), 215–216.
45. Jampol, L., Goldstein, D.A., Zika virus infection and the eye. JAMA Ophthalmol. 20 (2016), 1–6.
46. Klema, V., Padmanabhan, R., Choi, K.H., Flaviviral replication complex: coordination between RNA synthesis and 5’-RNA capping. Viruses 7:8 (2015), 4640–4656.
47. Kostyuchenko, V., Lim, E.X.Y., Zhang, S., Fibriansah, G., Ng, T.S., Ooi, J.S., et al. Structure of the thermally stable Zika virus. Nature 533 (2016), 425–428.
48. Lanciotti, R., Kosoy, O.L., Laven, J.J., Velez, J.O., Lambert, A.J., Johnson, A.J., Stanfield, S.M., Duffy, M.R., Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg. Infect. Dis. 14:8 (2008), 1232–1239.
49. Luca, V., AbiMansour, J., Nelson, C.A., Fremont, D.H., Crystal structure of the Japanese encephalitis virus envelope protein. J. Virol. 86:4 (2012), 2337–2346.
50. Ma, W., Li, S., Ma, S., Jia, L., Zhang, F., Zhang, Y., Zhang, J., Wong, G., Zhang, S., Lu, X., Liu, M., Yan, J., Li, W., Qin, C., Han, D., Qin, C., Wang, N., Li, X., Gao, G.F., Zika virus causes testis damage and leads to male infertility in mice. Cell, 168(3), 2017, 542.
51. Mansuy, J., Suberbielle, E., Chapuy-Regaud, S., Mengelle, 3, Bujan, C., Marchou, L., Delobel, B., Gonzalez-Dunia, P., Malnou, D., Izopet, C.E., Martin-Blondel, J., Zika virus in semen and spermatozoa. Lancet Infect. Dis. 16:10 (2016), 1106–1107.
52. Metsky, H., Matranga, C.B., Wohl, S., Schaffner, S.F., Freije, C.A., Winnicki, S.M., West, K., Qu, J., Baniecki, M.L., Gladden-Young, A., Lin, A.E., Tomkins-Tinch, C.H., Ye, S.H., Park, D.J., Luo, C.Y., Barnes, K.G., Shah, R.R., Chak, B., Barbosa-Lima, G., Delatorre, E., Vieira, Y.R., Paul, L.M., Tan, A.L., Barcellona, C.M., Porcelli, M.C., Vasquez, C., Cannons, A.C., Cone, M.R., Hogan, K.N., Kopp, E.W., Anzinger, J.J., Garcia, K.F., Parham, L.A., Ramírez, R.M.G., Montoya, M.C.M., Rojas, D.P., Brown, C.M., Hennigan, S., Sabina, B., Scotland, S., Gangavarapu, K., Grubaugh, N.D., Oliveira, G., Robles-Sikisaka, R., Rambaut, A., Gehrke, L., Smole, S., Halloran, M.E., Villar, L., Mattar, S., Lorenzana, I., Cerbino-Neto, J., Valim, C., Degrave, W., Bozza, P.T., Gnirke, A., Andersen, K.G., Isern, S., Michael, S.F., Bozza, F.A., Souza, T.M.L., Bosch, I., Yozwiak, N.L., MacInnis, B.L., Sabeti, P.C., Zika virus evolution and spread in the Americas. Nature 546:7658 (2017), 411–415.
53. Modhiran, N., Watterson, D., Muller, D.A., Panetta, A.K., Sester, D.P., Liu, L., Hume, D.A., Stacey, K.J., Young, P.R., Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci. Transl. Med., 7(304), 2015, 304ra142.
54. Modis, Y., Ogata, S., Clements, D., Harrison, S.C., A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 100:12 (2003), 6986–9691.
55. Musso, D., Gubler, D.J., Zika virus. Clin. Microbiol. Rev. 29:3 (2016), 487–524.
56. Nicastri, E., Castilletti, C., Balestra, P., Galgani, S., Ippolito, G., Zika virus infection in the central nervous system and female genital tract. Emerg. Infect. Dis. 22:12 (2016), 2228–2230.
57. Nishiura, H., Kinoshita, R., Mizumoto, K., Yasuda, Y., Nah, K., Zika virus, French Polynesia, South Pacific, 2013. Emerg. Infect. Dis. 20:6 (2016), 95–97.
58. Nybakken, G., Nelson, C.A., Chen, B.R., Diamond, M.S., Fremont, D.H., Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 80:23 (2006), 11467–11474.
59. Oehler, E., Watrin, L., Larre, P., Leparc-Goffart, I., Lastere, S., Valour, F., Baudouin, L., Mallet, H., Musso, D., Ghawche, F., Zika virus infection complicated by Guillain-Barre syndrome-case report, French Polynesia, December 2013. Euro Surveill., 19(9), 2014, 20720.
60. Onorati, M., Li, Z., Liu, F., Sousa, A.M., Nakagawa, N., Li, M., Dell'Anno, M.T., Gulden, F.O., Pochareddy, S., Tebbenkamp, A.T., Han, W., Pletikos, M., Gao, T., Zhu, Y., Bichsel, C., Varela, L., Szigeti-Buck, K., Lisgo, S., Zhang, Y., Testen, A., Gao, X.B., Mlakar, J., Popovic, M., Flamand, M., Strittmatter, S.M., Kaczmarek, L.K., Anton, E.S., Horvath, T.L., Lindenbach, B.D., Sestan, N., Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Rep. 16:10 (2016), 2576–2592.
61. PAHO, Epidemiological Alert. Neurological Syndrome, Congenital Malformations, and Zika Virus Infection. Implications for Public Health in the Americas. 2015, World Health Organization.
62. Patel, B., Longo, P.C., Miley, M.J., Montoya, M., Harris, E., de Silva, A.M., Dissecting the human serum antibody response to secondary dengue virus infections. PLoS Negl. Trop. Dis., 11(5), 2017, e0005554.
63. Paz-Bailey, G., Rosenberg, E.S., Doyle, K., Munoz-Jordan, J., Santiago, G.A., Klein, L., Perez-Padilla, J., Medina, F.A., Waterman, S.H., Gubern, C.G., Alvarado, L.I., Sharp, T.M., Persistence of Zika virus in body fluids - preliminary report. N. Engl. J Med., 2017, 10.1056/NEJMoa1613108.
64. Prisant, N., Bujan, L., Benichou, H., Hayot, P.H., Pavili, L., Lurel, S., Herrmann, C., Janky, E., Joguet, G., Zika virus in the female genital tract. Lancet Infect. Dis. 16:9 (2016), 1000–1001.
65. Priyamvada, L., Quicke, K.M., Hudson, W.H., Onlamoon, N., Sewatanon, J., Edupuganti, S., Pattanapanyasat, K., Chokephaibulkit, K., Mulligan, M.J., Wilson, P.C., Ahmed, R., Suthar, M.S., Wrammert, J., Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc. Natl. Acad. Sci. U. S. A. 113:28 (2016), 7582–7587.
66. Robbiani, D., Bozzacco, L., Keeffe, J.R., Khouri, R., Olsen, P.C., Gazumyan, A., Schaefer-Babajew, D., Avila-Rios, S., Nogueira, L., Patel, R., Azzopardi, S.A., Uhl, L.F.K., Saeed, M., Sevilla-Reyes, E.E., Agudelo, M., Yao, K.H., Golijanin, J., Gristick, H.B., Lee, Y.E., Hurley, A., Caskey, M., Pai, J., Oliveira, T., Wunder, E.A. Jr., Sacramento, G., Nery, N. Jr., Orge, C., Costa, F., Reis, M.G., Thomas, N.M., Eisenreich, T., Weinberger, D.M., de Almeida, A.R.P., West, A.P. Jr., Rice, C.M., Bjorkman, P.J., Reyes-Teran, G., Ko, A.I., MacDonald, M.R., Nussenzweig, M.C., Recurrent potent human neutralizing antibodies to Zika virus in Brazil and Mexico. Cell 169:4 (2017), 597–609.
67. Roehrig, J.T., Antigenic structure of flavivirus proteins. Adv. Virus Res. 59 (2003), 141–175.
68. Rothman, A.L., Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol. 11:8 (2011), 532–543.
69. Rouvinski, A., Guardado-Calvo, P., Barba-Spaeth, G., Duquerroy, S., Vaney, M.C., Kikuti, C.M., Navarro Sanchez, M.E., Dejnirattisai, W., Wongwiwat, W., Haouz, A., Girard-Blanc, C., Petres, S., Shepard, W.E., Desprès, P., Arenzana-Seisdedos, F., Dussart, P., Mongkolsapaya, J., Screaton, G.R., Rey, F.A., Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 520 (2015), 109–113.
70. Rozé B., Najioullah, F., Signate, A., Apetse, K., Brouste, Y., Gourgoudou, S., Fagour, L., Abel, S., Hochedez, P., Cesaire, R., Cabié A., Zika virus detection in cerebrospinal fluid from two patients with encephalopathy, Martinique, February 2016. Euro Surveill., 21(16), 2016.
71. Sabin, A., Research on dengue during world war II. Am. J. Trop. Med. Hyg. 1:1 (1952), 30–50.
72. Sapparapu, G., Fernandez, E., Kose, N., Bin Cao Fox, J.M., Bombardi, R.G., Zhao, H., Nelson, C.A., Bryan, A.L., Barnes, T., Davidson, E., Mysorekar, I.U., Fremont, D.H., Doranz, B.J., Diamond, M.S., Crowe, J.E., Neutralizing human antibodies prevent Zika virus replication and fetal disease in mice. Nature 540:7633 (2016), 443–447.
73. Shoenfeld, Y., George, J., Peter, J.B., Guillain-Barré as an autoimmune disease. Int. Arch. Allergy Immunol. 109:4 (1996), 318–326.
74. Simpson, D., Zika virus infection in man. Trans. R. Soc. Trop. Med. Hyg. 58 (1964), 335–338.
75. Sirohi, D., Chen, Z., Sun, L., Klose, T., Pierson, T.C., Rossmann, M.G., Kuhn, R.J., The 3.8 Å resolution cryo-EM structure of Zika virus. Science 352:6284 (2016), 467–470.
76. Siu, R., Bukhari, W., Todd, A., Gunn, W., Huang, Q.S., Timmings, P., Acute Zika infection with concurrent onset of Guillain-Barré Syndrome. Neurology 87:15 (2016), 1623–1624.
77. Song, H., Qi, J., Haywood, J., Shi, Y., Gao, G.F., Zika virus NS1 structure reveals diversity of electrostatic surfaces among flaviviruses. Nat. Struct. Mol. Biol. 23 (2016), 456–458.
78. Stettler, K., Beltramello, M., Espinosa, D.A., Graham, V., Cassotta, A., Bianchi, S., Vanzetta, F., Minola, A., Jaconi, S., Mele, F., Foglierini, M., Pedotti, M., Simonelli, L., Dowall, S., Atkinson, B., Percivalle, E., Simmons, C.P., Varani, L., Blum, J., Baldanti, F., Cameroni, E., Hewson, R., Harris, E., Lanzavecchia, A., Sallusto, F., Corti, D., Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353:6301 (2016), 823–826.
79. Suthar, M., Diamond, M.S., Gale, M. Jr., West Nile virus infection and immunity. Nat. Rev. Microbiol. 11 (2013), 115–128.
80. Suy, A., Sulleiro, E., Rodó C., Vázquez, É Bocanegra, C., Molina, I., Esperalba, J., Sánchez-Seco, M.P., Boix, H., Pumarola, T., Carreras, Eq., Prolonged Zika virus viremia during pregnancy. N. Engl. J. Med. 375:26 (2016), 2611–2613.
81. Swanstrom, J., 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 7:4 (2016), e01123–01116.
82. Tabata, T., Petitt, M., Puerta-Guardo, H., Michlmayr, D., Wang, C., Fang-Hoover, J., Harris, E., Pereira, L., Zika virus targets different primary human placental cells, suggesting two routes for vertical transmission. Cell Host Microbe 20:2 (2016), 155–166.
83. Tang, H., Hammack, C., Ogden, S.C., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E.M., Christian, K.M., Didier, R.A., Jin, P., Song, H., Ming, G.L., Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18:5 (2016), 587–590.
84. Tripathi, S., Balasubramaniam, V.R., Brown, J.A., Mena, I., Grant, A., Bardina, S.V., Maringer, K., Schwarz, M.C., Maestre, A.M., Sourisseau, M., Albrecht, R.A., Krammer, F., Evans, M.J., Fernandez-Sesma, A., Lim, J.K., García-Sastre, A., A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses. PLoS Pathog., 13(3), 2017, e1006258.
85. van der Eijk, A., van Genderen, P.J., Verdijk, R.M., Reusken, C.B., Mögling, R., van Kampen, J.J., Widagdo, W., Aron, G.I., GeurtsvanKessel, C.H., Pas, S.D., Raj, V.S., Haagmans, B.L., Koopmans, M.P., Miscarriage associated with Zika virus infection. N. Engl. J. Med. 375:10 (2016), 1002–1004.
86. Waggoner, J.J., Mohamed-Hadley, A., Ballesteros, G., Davila, M.J., Tellez y, Sahoo, M.K., Balmaseda, A., Harris, E., Pinsky, B.A., Single-reaction multiplex reverse transcription PCR for detection of Zika, Chikungunya, and Dengue viruses. Emerg. Infect. Dis. 22:7 (2016), 1295–1297.
87. Wang, Q., Hang, Y., Liu, X., Dai, L., Ma, T., Qi, J., Wong, G., Peng, R., Liu, S., Li, J., Son, J., Liu, J., He, J., Yuan, H., XiongY, Liao, Y., Li, J., Yang, J., Tong, Z., Griffin, B.D., Bi, Y., Liang, M., Xu, X., Qin, C., Cheng, G., Zhang, X., Wang, P., Qiu, X., Kobinger, G., Shi, Y., Yan, J., Gao, G.F., Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci. Transl. Med., 8(369), 2016 369ra179.
88. Weiskopf, D., Angelo, M.A., de Azeredo, E.L., Sidney, J., Greenbaum, J.A., Fernando, A.N., Broadwater, A., Kolla, R.V., De Silva, A.D., de Silva, A.M., Mattia, K.A., Doranz, B.J., Grey, H.M., Shresta, S., Peters, B., Sette, A., Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. Proc. Natl. Acad. Sci. U. S. A. 110:22 (2013), E2046–2053.
89. Weiskopf, D., Angelo, M.A., Sidney, J., Peters, B., Shresta, S., Sette, A., Immunodominance changes as a function of the infecting dengue virus serotype and primary versus secondary infection. J. Virol. 88:19 (2014), 11383–11394.
90. Weiskopf, D., Angelo, M.A., Grifoni, A., O'Rourke, P.H., Sidney, J., Paul, S., De Silva, A.D., Phillips, E., Mallal, S., Premawansa, S., Premawansa, G., Wijewickrama, A., Peters, B., Sette, A., HLA-DRB1 alleles are associated with different magnitudes of dengue virus-specific CD4+ T-cell responses. J. Infect. Dis. 214:7 (2016), 1117–1124.
91. + T cells. Nat. Microbiol., 2, 2017, 17036.
92. WHO, 2016. Zika virus and complications: 2016 Public Health Emergency of International Concern.
93. Xu, X., Song, H., Qi, J., Liu, Y., Wang, H., Su, C., Shi, Y., Gao, G.F., Contribution of intertwined loop to membrane association revealed by Zika virus full-length NS1 structure. EMBO J. 35 (2016), 2170–2178.
94. Zanluca, C., de Melo, V.C.A., Mosimann, A.L.P., dos Santos, G.I.V., dos Santos, C.N.D., Luz, K., First report of autochthonous transmission of Zika virus in Brazil. Mem. Inst. Oswaldo Cuz. 110 (2015), 659–662.
95. Zhang, Y., Zhang, W., Ogata, S., Clements, D., Strauss, J.H., Baker, T.S., Kuhn, R.J., Rossmann, M.G., Conformational changes of the flavivirus E glycoprotein. Structure 12:9 (2004), 1607–1618.
96. Zhang, X., Ge, P., Yu, X., Brannan, J.M., Bi, G., Zhang, Q., Schein, S., Zhou, Z.H., Cryo-EM structure of the mature dengue virus at 3.5-A resolution. Nat. Struct. Mol. Biol. 20 (2013), 105–110.