A human antibody against Zika virus crosslinks the E protein to prevent infection

Nature Communications

Volumn 8, Issue , 2017, Pages

  Hasan, S Saif ^a   Miller, Andrew ^a   Sapparapu, Gopal ^b   Fernandez, Estefania ^c   Klose, Thomas ^a   Long, Feng ^a   Fokine, Andrei ^a   Porta, Jason C ^a   Jiang, Wen ^a   Diamond, Michael S ^c   Crowe, James E ^b,d   Kuhn, Richard J ^a   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; GLYCOPROTEIN E; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; ZIKA VIRUS E PROTEIN; ZIKV 117; NEUTRALIZING ANTIBODY; PROTEIN BINDING; VIRAL PROTEIN; VIRUS ANTIBODY;

ANTIBODY; EPIDEMIC; PREGNANCY; PROTEIN; RODENT; VIRUS;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; COMPARATIVE STUDY; CROSS REACTION; CRYOELECTRON MICROSCOPY; ENDOSOME; INFECTION PREVENTION; MOUSE; NONHUMAN; PROTEIN CROSS LINKING; SEQUENCE ALIGNMENT; STEREOSPECIFICITY; VERO CELL LINE; VIRUS NEUTRALIZATION; VIRUS STRAIN; ZIKA FEVER; ZIKA VIRUS; CHEMISTRY; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; MOLECULAR MODEL; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE; VIROLOGY;

FRENCH POLYNESIA;

ZIKA VIRUS;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BINDING SITES; CRYOELECTRON MICROSCOPY; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN MULTIMERIZATION; VIRAL STRUCTURAL PROTEINS; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85015383878     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14722     Document Type: Article

References (55)

1. Kuno, G., Chang, G. J., Tsuchiya, K. R., Karabatsos, N., & Cropp, C. B. Phylogeny of the genus Flavivirus. J. Virol. 72, 73-83 (1998
2. Dick, G. W., Kitchen, S. F., & Haddow, A. J. Zika virus. I. Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46, 509-520 1952
3. MacNamara, F. N. Zika virus: a report on three cases of human infection during an epidemic of jaundice in Nigeria. Trans. R. Soc. Trop. Med. Hyg. 48, 139-145 (1954
4. Duffy, M. R., et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 360, 2536-2543 (2009
5. Cao-Lormeau, V. M., et al. Zika virus, French polynesia, South pacific, 2013. Emerg. Infect. Dis. 20, 1085-1086 (2014
6. Zanluca, C., et al. First report of autochthonous transmission of Zika virus in Brazil. Mem. Inst. Oswaldo Cruz 110, 569-572 (2015
7. CDC. All countries, & territories with active Zika virus transmission https://www.cdc.gov/zika/geo/active-countries.html (2016
8. Sirohi, D., et al. The 3.8 Å resolution cryo-EM structure of Zika virus. Science 352, 467-470 (2016
9. Kostyuchenko, V. A., et al. Structure of the thermally stable Zika virus. Nature 533, 425-428 (2016
10. Kuhn, R. J., et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108, 717-725 (2002
11. Perera, R., & Kuhn, R. J. Structural proteomics of dengue virus. Curr. Opin. Microbiol. 11, 369-377 (2008
12. Zhang, Y., et al. Structures of immature flavivirus particles. EMBO J. 22, 2604-2613 (2003
13. Yu, I. M., et al. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319, 1834-1837 (2008
14. Cao-Lormeau, V. M., et al. Guillain-Barre Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387, 1531-1539 (2016
15. Mlakar, J., et al. Zika virus associated with microcephaly. N. Engl. J. Med. 374, 951-958 (2016
16. Martines, R. B., et al. Notes from the field: evidence of Zika virus infection in brain and placental tissues from two congenitally infected newborns and two fetal losses-Brazil, 2015. MMWR Morb. Mortal. Wkly. Rep. 65, 159-160 (2016
17. NYC Health. Health department reports four more babies born with congenital Zika virus syndrome in NYC http://www1.nyc.gov/site/doh/about/press/pr2016/pr101-16.page (2016
18. Foy, B. D., et al. Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg. Infect. Dis. 17, 880-882 (2011
19. Musso, D., et al. Potential sexual transmission of Zika virus. Emerg. Infect. Dis. 21, 359-361 (2015
20. Sapparapu, G., et al. Neutralizing human monoclonal antibodies prevent Zika virus replication and fetal disease in pregnancy. Nature 540, 443-447 (2016
21. Stettler, K., et al. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353, 823-826 (2016
22. Scheres, S. H., & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853-854 (2012
23. Guo, F., & Jiang, W. Single particle cryo-electron microscopy and 3-D reconstruction of viruses. Methods Mol. Biol. 1117, 401-443 (2014
24. Henderson, R., et al. Tilt-pair analysis of images from a range of different specimens in single-particle electron cryomicroscopy. J. Mol. Biol. 413, 1028-1046 (2011
25. Pettersen, E. F., et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 2004
26. Emsley, P., & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004
27. Rossmann, M. G., Bernal, R., & Pletnev, S. V. Combining electron microscopic with x-ray crystallographic structures. J. Struct. Biol. 136, 190-200 (2001
28. Rey, F. A., Heinz, F. X., Mandl, C., Kunz, C., & Harrison, S. C. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375, 291-298 (1995
29. Zhao, H., et al. Structural basis of Zika virus-specific antibody protection. Cell 166, 1016-1027 (2016
30. Wang, et al. Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci. Transl. Med. 369, 369ra179 (2016
31. Rouvinski, A., et al. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 520, 109-113 (2015
32. Dejnirattisai, W., et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 16, 170-177 (2015
33. Fibriansah, G., et al. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat. Commun. 6, 6341 (2015
34. Fibriansah, G., et al. Cryo-EM structure of an antibody that neutralizes dengue virus type 2 by locking E protein dimers. Science 349, 88-91 2015
35. Teoh, E. P., et al. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med. 4, 139ra83 (2012
36. Kaufmann, B., et al. 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, 18950-18955 (2010
37. Zhang, S., et al. Neutralization mechanism of a highly potent antibody against Zika virus. Nat. Commun. 7, 13679 (2016
38. Bressanelli, S., et al. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 23, 728-738 2004
39. Modis, Y., Ogata, S., Clements, D., & Harrison, S. C. Structure of the dengue virus envelope protein after membrane fusion. Nature 427, 313-319 (2004
40. Zhang, Y., et al. Conformational changes of the flavivirus E glycoprotein. Structure 12, 1607-1618 (2004
41. Lindenbach, B. D., & Rice, C. M. Molecular biology of flaviviruses. Adv. Virus Res. 59, 23-61 (2003
42. Zhang, X., et al. Structure of acidic pH dengue virus showing the fusogenic glycoprotein trimers. J. Virol. 89, 743-750 (2015
43. Swanstrom, J. A., et al. Dengue virus envelope dimer epitope monoclonal antibodies isolated from dengue patients are protective against Zika virus. MBio 7, e01123-16 (2016
44. Dejnirattisai, W., et al. Dengue virus sero-cross-reactivity drives antibodydependent enhancement of infection with Zika virus. Nat. Immunol. 17, 1102-1108 (2016
45. Barba-Spaeth, G., et al. Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nature 536, 48-53 (2016
46. Priyamvada, L., et al. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc. Natl Acad. Sci. USA 113, 7852-7857 (2016
47. Thornburg, N. J., et al. H7N9 influenza virus neutralizing antibodies that possess few somatic mutations. J. Clin. Invest. 126, 1482-1494 (2016
48. Sapparapu, G., et al. Frequent use of the IgA isotype in human B cells encoding potent norovirus-specific monoclonal antibodies that block HBGA binding. PLoS Pathog. 12, e1005719 (2016
49. Carragher, B., et al. Leginon: an automated system for acquisition of images from vitreous ice specimens. J. Struct. Biol. 132, 33-45 (2000
50. Lander, G. C., et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95-102 (2009
51. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012
52. Yu, G., et al. An algorithm for estimation and correction of anisotropic magnification distortion of cryo-EM images without need of pre-calibration. J. Struct. Biol. 195, 207-215 (2016
53. Liu, Z., Guo, F., Wang, F., Li, T. C., & Jiang, W. 2.9 Å resolution cryo-EM 3D reconstruction of close-packed virus particles. Structure 24, 319-328 2016
54. Sievers, F., et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011
55. Robert, X., & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320-W324 (2014