A multimechanistic antibody targeting the receptor binding site potently cross-protects against influenza B viruses

Science Translational Medicine

Volumn 9, Issue 412, 2017, Pages

  Shen, Chenguang ^a   Chen, Junyu ^a   Li, Rui ^a   Zhang, Mengya ^a   Wang, Guosong ^a   Stegalkina, Svetlana ^b   Zhang, Limin ^a   Chen, Jing ^a   Cao, Jianli ^a   Bi, Xingjian ^a   Anderson, Stephen F ^b   Alefantis, Timothy ^b   Zhang, Minwei ^c   Cai, Xiaoyang ^c   Yang, Kunyu ^d   Zheng, Qingbing ^a   Fang, Mujing ^a   Yu, Hai ^a   Luo, Wenxin ^a   Zheng, Zizheng ^a   Yuan, Quan ^a   Zhang, Jun ^a   Shih, James Wai Kuo ^a   Kleanthous, Harry ^b   Chen, Honglin ^a,e   Chen, Yixin ^a   Xia, Ningshao ^a   more..

^a XIAMEN UNIVERSITY   (China)

^b SANOFI PASTEUR   (France)

^c THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

^d Department of Clinical Laboratory Xiamen International Travel Healthcare Center   (China)

^e THE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; INFLUENZA VIRUS HEMAGGLUTININ; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY C12G6; NEUTRALIZING ANTIBODY; OSELTAMIVIR; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; CELL MEDIATED CYTOTOXICITY; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; EPITOPE MAPPING; FEMALE; HEMAGGLUTINATION INHIBITION; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; INFLUENZA B; INFLUENZA B VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; VIRUS ENTRY; VIRUS NEUTRALIZATION; VIRUS RELEASE; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; COMBINATION DRUG THERAPY; CROSS PROTECTION; DOG; IMMUNIZATION; IMMUNOLOGY; ISOLATION AND PURIFICATION; MDCK CELL LINE; METABOLISM; MOLECULAR MODEL; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRUS INFECTION; PROTEIN DOMAIN; TREATMENT OUTCOME; VIROLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BINDING SITES; CROSS PROTECTION; DOGS; DRUG THERAPY, COMBINATION; EPITOPE MAPPING; EPITOPES; FEMALE; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNIZATION; INFLUENZA B VIRUS; MADIN DARBY CANINE KIDNEY CELLS; MICE, INBRED BALB C; MODELS, MOLECULAR; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; PROTEIN DOMAINS; RECEPTORS, VIRUS; TREATMENT OUTCOME;

EID: 85031817628     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aam5752     Document Type: Article

References (33)

1. World Health Organization, Influenza (seasonal) fact sheet (2014); www.who.int/mediacentre/factsheets/fs211/en.
2. S. Su, S. S. Chaves, A. Perez, T. D'Mello, P. D. Kirley, K. Yousey-Hindes, M. M. Farley, M. Harris, R. Sharangpani, R. Lynfield, C. Morin, E. B. Hancock, S. Zansky, G. E. Hollick, B. Fowler, C. McDonald-Hamm, A. Thomas, V. Horan, M. L. Lindegren, W. Schaffner, A. Price, A. Bandyopadhyay, A. M. Fry, Comparing clinical characteristics between hospitalized adults with laboratory-confirmed influenza A and B virus infection. Clin. Infect. Dis. 59, 252-255 (2014).
3. Y. Pan, Y. Zhang, P. Yang, H. Qian, W. Shi, S. Wu, S. Cui, D. Zhang, Q. Wang, Epidemiological and phylogenetic characteristics of influenza B infection in severe acute respiratory infection cases in Beijing, 2014 to 2015. Medicine 94, e2399 (2015).
4. W. W. Thompson, D. K. Shay, E. Weintraub, L. Brammer, C. B. Bridges, N. J. Cox, K. Fukuda, Influenza-associated hospitalizations in the United States. JAMA 292, 1333-1340 (2004).
5. M. W. Shaw, X. Xu, Y. Li, S. Normand, R. T. Ueki, G. Y. Kunimoto, H. Hall, A. Klimov, N. J. Cox, K. Subbarao, Reappearance and global spread of variants of influenza B/Victoria/2/87 lineage viruses in the 2000-2001 and 2001-2002 seasons. Virology 303, 1-8 (2002).
6. R. B. Belshe, The need for quadrivalent vaccine against seasonal influenza. Vaccine 28, D45-D53 (2010).
7. K. Subbarao, Y. Matsuoka, The prospects and challenges of universal vaccines for influenza. Trends Microbiol. 21, 350-358 (2013).
8. T. Heikkinen, N. Ikonen, T. Ziegler, Impact of influenza B lineage-level mismatch between trivalent seasonal influenza vaccines and circulating viruses, 1999-2012. Clin. Infect. Dis. 59, 1519-1524 (2014).
9. X. Li, H. Liao, Y. Liu, L. Liu, F. Wang, H. Song, J. Cheng, X. Liu, D. Xu, Drug-resistant and genetic evolutionary analysis of influenza virus from patients during the 2013 and 2014 influenza season in Beijing. Microb. Drug Resist. 23, 253-260 (2017).
10. D. R. Burton, P. Poignard, R. L. Stanfield, I. A. Wilson, Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337, 183-186 (2012).
11. F. Krammer, P. Palese, Advances in the development of influenza virus vaccines. Nat. Rev. Drug Discov. 14, 167-182 (2015).
12. D. Corti, J. Voss, S. J. Gamblin, G. Codoni, A. Macagno, D. Jarrossay, S. G. Vachieri, D. Pinna, A. Minola, F. Vanzetta, C. Silacci, B. M. Fernandez-Rodriguez, G. Agatic, S. Bianchi, I. Giacchetto-Sasselli, L. Calder, F. Sallusto, P. Collins, L. F. Haire, N. Temperton, J. P. M. Langedijk, J. J. Skehel, A. Lanzavecchia, A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856 (2011).
13. C.-J. Wei, H. M. Yassine, P. M. McTamney, J. G. D. Gall, J. R. R. Whittle, J. C. Boyington, G. J. Nabel, Elicitation of broadly neutralizing influenza antibodies in animals with previous influenza exposure. Sci. Transl. Med. 4, 147ra114 (2012).
14. N. L. Kallewaard, D. Corti, P. J. Collins, U. Neu, J. M. McAuliffe, E. Benjamin, L. Wachter-Rosati, F. J. Palmer-Hill, A. Q. Yuan, P. A. Walker, M. K. Vorlaender, S. Bianchi, B. Guarino, A. De Marco, F. Vanzetta, G. Agatic, M. Foglierini, D. Pinna, B. Fernandez-Rodriguez, A. Fruehwirth, C. Silacci, R. W. Ogrodowicz, S. R. Martin, F. Sallusto, J. A. Suzich, A. Lanzavecchia, Q. Zhu, S. J. Gamblin, J. J. Skehel, Structure and function analysis of an antibody recognizing all influenza A subtypes. Cell 166, 596-608 (2016).
15. G. M. Air, Influenza virus antigenicity and broadly neutralizing epitopes. Curr. Opin. Virol. 11, 113-121 (2015).
16. M. Yasugi, R. Kubota-Koketsu, A. Yamashita, N. Kawashita, A. Du, T. Sasaki, M. Nishimura, R. Misaki, M. Kuhara, N. Boonsathorn, K. Fujiyama, Y. Okuno, T. Nakaya, K. Ikuta, Human monoclonal antibodies broadly neutralizing against influenza B virus. PLOS Pathog. 9, e1003150 (2013).
17. C. Dreyfus, N. S. Laursen, T. Kwaks, D. Zuijdgeest, R. Khayat, D. C. Ekiert, J. H. Lee, Z. Metlagel, M. V. Bujny, M. Jongeneelen, R. van der Vlugt, M. Lamrani, H. J. W. M. Korse, E. Geelen, Ö. Sahin, M. Sieuwerts, J. P. J. Brakenhoff, R. Vogels, O. T. W. Li, L. L. M. Poon, M. Peiris, W. Koudstaal, A. B. Ward, I. A. Wilson, J. Goudsmit, R. H. E. Friesen, Highly conserved protective epitopes on influenza B viruses. Science 337, 1343-1348 (2012).
18. N. Chai, L. R. Swem, S. Park, G. Nakamura, N. Chiang, A. Estevez, R. Fong, L. Kamen, E. Kho, M. Reichelt, Z. Lin, H. Chiu, E. Skippington, Z. Modrusan, J. Stinson, M. Xu, P. Lupardus, C. Ciferri, M.-W. Tan, A broadly protective therapeutic antibody against influenza B virus with two mechanisms of action. Nat. Commun. 8, 14234 (2017).
19. T. Velkov, The specificity of the influenza B virus hemagglutinin receptor binding pocket: What does it bind to? J. Mol. Recognit. 26, 439-449 (2013).
20. C. D. O'Donnell, L. Vogel, A. Wright, S. R. Das, J. Wrammert, G.-M. Li, M. McCausland, N.-Y. Zheng, J. W. Yewdell, R. Ahmed, P. C. Wilson, K. Subbarao, Antibody pressure by a human monoclonal antibody targeting the 2009 pandemic H1N1 virus hemagglutinin drives the emergence of a virus with increased virulence in mice. mBio 3, e00120-e12 (2012).
21. D. M. Skowronski, M.-E. Hamelin, N. Z. Janjua, G. De Serres, J. L. Gardy, C. Rhéaume, X. Bouhy, G. Boivin, Cross-lineage influenza B and heterologous influenza A antibody responses in vaccinated mice: Immunologic interactions and B/Yamagata dominance. PLOS ONE 7, e38929 (2012).
22. A. Maroof, Y. M. Yorgensen, Y. Li, J. T. Evans, Intranasal vaccination promotes detrimental Th17-mediated immunity against influenza infection. PLOS Pathog. 10, e1003875 (2014).
23. M. A. Rose, S. Zielen, U. Baumann, Mucosal immunity and nasal influenza vaccination. Expert Rev. Vaccines 11, 595-607 (2012).
24. F. Cox, T. Kwaks, B. Brandenburg, M. H. Koldijk, V. Klaren, B. Smal, H. J. W. M. Korse, E. Geelen, L. Tettero, D. Zuijdgeest, E. J. M. Stoop, E. Saeland, R. Vogels, R. H. E. Friesen, W. Koudstaal, J. Goudsmit, HA antibody-mediated FcgRIIIa activity is both dependent on FcR engagement and interactions between HA and sialic acids. Front. Immunol. 7, 399 (2016).
25. P. E. Leon, W. He, C. E. Mullarkey, M. J. Bailey, M. S. Miller, F. Krammer, P. Palese, G. S. Tan, Optimal activation of Fc-mediated effector functions by influenza virus hemagglutinin antibodies requires two points of contact. Proc. Natl. Acad. Sci. U.S.A. 113, E5944-E5951 (2016).
26. P. D. Reuman, S. Keely, G. M. Schiff, Assessment of signs of influenza illness in the ferret model. J. Virol. Methods 24, 27-34 (1989).
27. N. Tewawong, K. Suwannakarn, S. Prachayangprecha, S. Korkong, P. Vichiwattana, S. Vongpunsawad, Y. Poovorawan, Molecular epidemiology and phylogenetic analyses of influenza B virus in Thailand during 2010 to 2014. PLOS ONE 10, e0116302 (2015).
28. G.-M. Li, C. Chiu, J. Wrammert, M. McCausland, S. F. Andrews, N.-Y. Zheng, J.-H. Lee, M. Huang, X. Qu, S. Edupuganti, M. Mulligan, S. R. Das, J. W. Yewdell, A. K. Mehta, P. C. Wilson, R. Ahmed, Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc. Natl. Acad. Sci. U.S.A. 109, 9047-9052 (2012).
29. S. F. Andrews, Y. Huang, K. Kaur, L. I. Popova, I. Y. Ho, N. T. Pauli, C. J. H. Dunand, W. M. Taylor, S. Lim, M. Huang, X. Qu, J.-H. Lee, M. Salgado-Ferrer, F. Krammer, P. Palese, J. Wrammert, R. Ahmed, P. C. Wilson, Immune history profoundly affects broadly protective B cell responses to influenza. Sci. Transl. Med. 7, 316ra192 (2015).
30. R. Chen, Z. Weng, A novel shape complementarity scoring function for protein-protein docking. Proteins 51, 397-408 (2003).
31. L. Li, R. Chen, Z. Weng, RDOCK: Refinement of rigid-body protein docking predictions. Proteins 53, 693-707 (2003).
32. E. F. Pettersen, T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, T. E. Ferrin, UCSF Chimera - A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
33. V. Srivastava, Z. Yang, I. F. N. Hung, J. Xu, B. Zheng, M.-Y. Zhang, Identification of dominant antibody-dependent cell-mediated cytotoxicity epitopes on the hemagglutinin antigen of pandemic H1N1 influenza virus. J. Virol. 87, 5831-5840 (2013).