Structural Basis of Zika Virus-Specific Antibody Protection

Cell

Volumn 166, Issue 4, 2016, Pages 1016-1027

  Zhao, Haiyan ^a   Fernandez, Estefania ^a   Dowd, Kimberly A ^b   Speer, Scott D ^b   Platt, Derek J ^a   Gorman, Matthew J ^a   Govero, Jennifer ^a   Nelson, Christopher A ^a   Pierson, Theodore C ^b   Diamond, Michael S ^a   Fremont, Daved H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; ZIKA VIRUS VACCINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COMPETITIVE BINDING ASSAY; CONTROLLED STUDY; DRUG DESIGN; EPITOPE MAPPING; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; MOUSE; NONHUMAN; PASSIVE TRANSPORT; PRIORITY JOURNAL; VIRUS IMMUNITY; VIRUS NEUTRALIZATION; VIRUS STRAIN; X RAY CRYSTALLOGRAPHY; ZIKA FEVER; ZIKA VIRUS; ANIMAL; C57BL MOUSE; CHEMISTRY; CLASSIFICATION; IMMUNOLOGY; MOLECULAR MODEL; VIROLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; EPITOPE MAPPING; EPITOPES; MICE; MICE, INBRED C57BL; MODELS, MOLECULAR; VIRAL ENVELOPE PROTEINS; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 84981333003     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.020     Document Type: Article

References (54)

1. Austin, S.K., Dowd, K.A., Shrestha, B., Nelson, C.A., Edeling, M.A., Johnson, S., Pierson, T.C., Diamond, M.S., Fremont, D.H., Structural basis of differential neutralization of DENV-1 genotypes by an antibody that recognizes a cryptic epitope. PLoS Pathog., 8, 2012, e1002930.
2. 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, 2016 Published online June 23, 2016.
3. Beasley, D.W., Barrett, A.D., Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J. Virol. 76 (2002), 13097–13100.
4. Belmusto-Worn, V.E., Sanchez, J.L., McCarthy, K., Nichols, R., Bautista, C.T., Magill, A.J., Pastor-Cauna, G., Echevarria, C., Laguna-Torres, V.A., Samame, B.K., et al. Randomized, double-blind, phase III, pivotal field trial of the comparative immunogenicity, safety, and tolerability of two yellow fever 17D vaccines (Arilvax and YF-VAX) in healthy infants and children in Peru. Am. J. Trop. Med. Hyg. 72 (2005), 189–197.
5. 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., et al. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8 (2010), 271–283.
6. Brasil, P., Pereira, J.P. Jr., Raja Gabaglia, C., Damasceno, L., Wakimoto, M., Ribeiro Nogueira, R.M., Carvalho de Sequeira, P., Machado Siqueira, A., Abreu de Carvalho, L.M., Cotrim da Cunha, D., et al. Zika Virus Infection in Pregnant Women in Rio de Janeiro - Preliminary Report. N. Engl. J. Med., 2016 Published online March 4, 2016.
7. Brien, J.D., Lazear, H.M., Diamond, M.S., Propagation, quantification, detection, and storage of West Nile virus. Curr Protoc Microbiol, 31, 2013 15D.3.1–15D.3.18.
8. Carteaux, G., Maquart, M., Bedet, A., Contou, D., Brugières, P., Fourati, S., Cleret de Langavant, L., de Broucker, T., Brun-Buisson, C., Leparc-Goffart, I., Mekontso Dessap, A., Zika Virus Associated with Meningoencephalitis. N. Engl. J. Med. 374 (2016), 1595–1596.
9. Cherrier, M.V., Kaufmann, B., Nybakken, G.E., Lok, S.M., Warren, J.T., Chen, B.R., Nelson, C.A., Kostyuchenko, V.A., Holdaway, H.A., Chipman, P.R., et al. Structural basis for the preferential recognition of immature flaviviruses by a fusion-loop antibody. EMBO 28 (2009), 3269–3276.
10. Cockburn, J.J., Navarro Sanchez, M.E., Fretes, N., Urvoas, A., Staropoli, I., Kikuti, C.M., Coffey, L.L., Arenzana Seisdedos, F., Bedouelle, H., Rey, F.A., Mechanism of dengue virus broad cross-neutralization by a monoclonal antibody. Structure 20 (2012), 303–314.
11. Correia, B.E., Bates, J.T., Loomis, R.J., Baneyx, G., Carrico, C., Jardine, J.G., Rupert, P., Correnti, C., Kalyuzhniy, O., Vittal, V., et al. Proof of principle for epitope-focused vaccine design. Nature 507 (2014), 201–206.
12. 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.
13. Dai, L., Song, J., Lu, X., Deng, Y.Q., Musyoki, A.M., Cheng, H., Zhang, Y., Yuan, Y., Song, H., Haywood, J., et al. Structures of the Zika Virus Envelope Protein and Its Complex with a Flavivirus Broadly Protective Antibody. Cell Host Microbe 19 (2016), 696–704.
14. 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. USA 109 (2012), 7439–7444.
15. Dick, G.W., Zika virus. II. Pathogenicity and physical properties. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 521–534.
16. Dick, G.W., Kitchen, S.F., Haddow, A.J., Zika virus. I. Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 509–520.
17. Dowd, K.A., Jost, C.A., Durbin, A.P., Whitehead, S.S., Pierson, T.C., A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLoS Pathog., 7, 2011, e1002111.
18. Dowd, K.A., DeMaso, C.R., Pierson, T.C., Genotypic Differences in Dengue Virus Neutralization Are Explained by a Single Amino Acid Mutation That Modulates Virus Breathing. MBio, 6, 2015 e01559–e15.
19. Edeling, M.A., Austin, S.K., Shrestha, B., Dowd, K.A., Mukherjee, S., Nelson, C.A., Johnson, S., Mabila, M.N., Christian, E.A., Rucker, J., et al. Potent dengue virus neutralization by a therapeutic antibody with low monovalent affinity requires bivalent engagement. PLoS Pathog., 10, 2014, e1004072.
20. Hanna, S.L., Pierson, T.C., Sanchez, M.D., Ahmed, A.A., Murtadha, M.M., Doms, R.W., N-linked glycosylation of west nile virus envelope proteins influences particle assembly and infectivity. J. Virol. 79 (2005), 13262–13274.
21. Heinz, F.X., Holzmann, H., Essl, A., Kundi, M., Field effectiveness of vaccination against tick-borne encephalitis. Vaccine 25 (2007), 7559–7567.
22. 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.
23. Kaufmann, B., Nybakken, G.E., Chipman, P.R., Zhang, W., Diamond, M.S., Fremont, D.H., Kuhn, R.J., Rossmann, M.G., West Nile virus in complex with the Fab fragment of a neutralizing monoclonal antibody. Proc. Natl. Acad. Sci. USA 103 (2006), 12400–12404.
24. Kaufmann, B., Vogt, M.R., Goudsmit, J., Holdaway, H.A., Aksyuk, A.A., Chipman, P.R., Kuhn, R.J., Diamond, M.S., Rossmann, M.G., Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. Proc. Natl. Acad. Sci. USA 107 (2010), 18950–18955.
25. Kim, J., Mohanty, S., Ganesan, L.P., Hua, K., Jarjoura, D., Hayton, W.L., Robinson, J.M., Anderson, C.L., FcRn in the yolk sac endoderm of mouse is required for IgG transport to fetus. J. Immunol. 182 (2009), 2583–2589.
26. Kostyuchenko, V.A., Lim, E.X., Zhang, S., Fibriansah, G., Ng, T.S., Ooi, J.S., Shi, J., Lok, S.M., Structure of the thermally stable Zika virus. Nature 533 (2016), 425–428.
27. Kuhn, R.J., Zhang, W., Rossmann, M.G., Pletnev, S.V., Corver, J., Lenches, E., Jones, C.T., Mukhopadhyay, S., Chipman, P.R., Strauss, E.G., et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108 (2002), 717–725.
28. Lanciotti, R.S., 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 (2008), 1232–1239.
29. 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, 2016 Published online June 28, 2016.
30. Lazear, H.M., Diamond, M.S., Zika Virus: New Clinical Syndromes and Its Emergence in the Western Hemisphere. J. Virol. 90 (2016), 4864–4875.
31. 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.
32. 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.
33. Lok, S.M., Kostyuchenko, V., Nybakken, G.E., Holdaway, H.A., Battisti, A.J., Sukupolvi-Petty, S., Sedlak, D., Fremont, D.H., Chipman, P.R., Roehrig, J.T., et al. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 15 (2008), 312–317.
34. Martina, B.E., Koraka, P., van den Doel, P., van Amerongen, G., Rimmelzwaan, G.F., Osterhaus, A.D., Immunization with West Nile virus envelope domain III protects mice against lethal infection with homologous and heterologous virus. Vaccine 26 (2008), 153–157.
35. Midgley, C.M., Flanagan, A., Tran, H.B., Dejnirattisai, W., Chawansuntati, K., Jumnainsong, A., Wongwiwat, W., Duangchinda, T., Mongkolsapaya, J., Grimes, J.M., Screaton, G.R., Structural analysis of a dengue cross-reactive antibody complexed with envelope domain III reveals the molecular basis of cross-reactivity. J. Immunol. 188 (2012), 4971–4979.
36. 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.
37. Nybakken, G., Oliphant, T., Johnson, S., Burke, S., Diamond, M.S., Fremont, D.H., Structural basis for neutralization of a therapeutic antibody against West Nile virus. Nature 437 (2005), 764–769.
38. 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, 2014, 19.
39. Oliphant, T., Engle, M., Nybakken, G.E., Doane, C., Johnson, S., Huang, L., Gorlatov, S., Mehlhop, E., Marri, A., Chung, K.M., et al. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 11 (2005), 522–530.
40. Oliphant, T., Nybakken, G.E., Engle, M., Xu, Q., Nelson, C.A., Sukupolvi-Petty, S., Marri, A., Lachmi, B.E., Olshevsky, U., Fremont, D.H., et al. Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J. Virol. 80 (2006), 12149–12159.
41. Pal, P., Dowd, K.A., Brien, J.D., Edeling, M.A., Gorlatov, S., Johnson, S., Lee, I., Akahata, W., Nabel, G.J., Richter, M.K.S., et al. Development of a highly protective combination monoclonal antibody therapy against Chikungunya virus. PLoS Pathog., 9, 2013, e1003312.
42. Pentsuk, N., van der Laan, J.W., An interspecies comparison of placental antibody transfer: new insights into developmental toxicity testing of monoclonal antibodies. Birth Defects Res. B Dev. Reprod. Toxicol. 86 (2009), 328–344.
43. Pierson, T.C., Diamond, M.S., Flaviviruses. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 2013, Lippincott Williams & Wilkins, 747–794.
44. Pierson, T.C., Xu, Q., Nelson, S., Oliphant, T., Nybakken, G.E., Fremont, D.H., Diamond, M.S., The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1 (2007), 135–145.
45. Rossi, S.L., Tesh, R.B., Azar, S.R., Muruato, A.E., Hanley, K.A., Auguste, A.J., Langsjoen, R.M., Paessler, S., Vasilakis, N., Weaver, S.C., Characterization of a Novel Murine Model to Study Zika Virus. Am. J. Trop. Med. Hyg. 94 (2016), 1362–1369.
46. 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., et al. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 520 (2015), 109–113.
47. Schneeweiss, A., Chabierski, S., Salomo, M., Delaroque, N., Al-Robaiy, S., Grunwald, T., Bürki, K., Liebert, U.G., Ulbert, S., A DNA vaccine encoding the E protein of West Nile virus is protective and can be boosted by recombinant domain DIII. Vaccine 29 (2011), 6352–6357.
48. Shi, B., Ma, L., He, X., Wang, X., Wang, P., Zhou, L., Yao, X., Comparative analysis of human and mouse immunoglobulin variable heavy regions from IMGT/LIGM-DB with IMGT/HighV-QUEST. Theor. Biol. Med. Model., 11, 2014, 30.
49. Shrestha, B., Brien, J.D., Sukupolvi-Petty, S., Austin, S.K., Edeling, M.A., Kim, T., O'Brien, K.M., Nelson, C.A., Johnson, S., Fremont, D.H., Diamond, M.S., The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog., 6, 2010, e1000823.
50. 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 (2016), 467–470.
51. Smith, S.A., de Alwis, A.R., Kose, N., Harris, E., Ibarra, K.D., Kahle, K.M., Pfaff, J.M., Xiang, X., Doranz, B.J., de Silva, A.M., et al. The potent and broadly neutralizing human dengue virus-specific monoclonal antibody 1C19 reveals a unique cross-reactive epitope on the bc loop of domain II of the envelope protein. MBio, 4, 2013 e00873–e13.
52. Sukupolvi-Petty, S., Austin, S.K., Engle, M., Brien, J.D., Dowd, K.A., Williams, K.L., Johnson, S., Rico-Hesse, R., Harris, E., Pierson, T.C., et al. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 84 (2010), 9227–9239.
53. Thompson, B.S., Moesker, B., Smit, J.M., Wilschut, J., Diamond, M.S., Fremont, D.H., A therapeutic antibody against west nile virus neutralizes infection by blocking fusion within endosomes. PLoS Pathog., 5, 2009, e1000453.
54. Vogt, M.R., Dowd, K.A., Engle, M., Tesh, R.B., Johnson, S., Pierson, T.C., Diamond, M.S., Poorly neutralizing cross-reactive antibodies against the fusion loop of West Nile virus envelope protein protect in vivo via Fcgamma receptor and complement-dependent effector mechanisms. J. Virol. 85 (2011), 11567–11580.