Amino acid substitutions in antigenic region B of hemagglutinin play a critical role in the antigenic drift of subclade 2.3.4.4 highly pathogenic H5NX influenza viruses.
Amino Acid Substitution
Animals
Antigenic Variation
/ genetics
Antigens, Viral
/ genetics
China
Epitopes
/ immunology
Hemagglutination Inhibition Tests
Hemagglutinin Glycoproteins, Influenza Virus
/ genetics
Influenza A Virus, H5N1 Subtype
/ genetics
Influenza A Virus, H5N8 Subtype
/ genetics
Influenza A virus
/ genetics
Influenza in Birds
/ immunology
Mutation
Poultry
Poultry Diseases
/ immunology
Reverse Genetics
Highly pathogenic avian influenza
antigenic drift
clade 2.3.4.4
hemagglutinin (HA) gene
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Jan 2020
Jan 2020
Historique:
received:
06
01
2019
revised:
06
08
2019
accepted:
26
08
2019
pubmed:
5
9
2019
medline:
27
5
2020
entrez:
5
9
2019
Statut:
ppublish
Résumé
As one of the important control strategies for highly pathogenic avian influenza (HPAI) in China, vaccination has been implemented compulsively in poultry flocks since 2004. However, the emergence and dominance of the circulating antigenic variants require the update of vaccines periodically. In order to investigate the key molecular sites responsible for the antigenic drift, a total of 13 amino acid positions divergent between clade 2.3.4 H5 viruses and their descendent subclade 2.3.4.4 variants in or around the recognized antigenic epitopes A-E were initially identified through inspecting a comprehensive HA sequence alignment of the H5 subtype HPAI viruses. Subsequently, a panel of single-site or multi-site HA mutants was constructed by reverse genetics with two H5N1 viruses of S (clade 2.3.4) and QD1 (subclade 2.3.4.4) as the HA backbone to study their antigenic variations, respectively. The hemagglutination-inhibition assay revealed an evident impact of mutations at sites 88, 156, 205, 208, 239 and 289 to the HA antigenicity and highlighted that the amino acid substitutions located in the antigenic region B, especially the combined mutations at sites 205 and 208, were the major antigenic determinant which was also consistent with results from flow cytometry and antigenic mapping. Our findings provided more insights into the molecular mechanism of antigenic drift of the H5 subtype HPAI virus, which would be helpful for the selection of vaccine candidates and accordingly for the prevention and control of this devastating viral agent.
Substances chimiques
Antigens, Viral
0
Epitopes
0
Hemagglutinin Glycoproteins, Influenza Virus
0
Banques de données
GENBANK
['EU195389', 'EU195396', 'KY437804', 'KY437811', 'KY437772', 'KY437779', 'KY437780', 'KY437787', 'KT221063', 'KT221086']
Types de publication
Comparative Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
263-275Subventions
Organisme : Jiangsu Provincial Natural Science Fund
ID : BK20170068
Organisme : Jiangsu Provincial Natural Science Foundation
ID : BK20130442
Organisme : National Natural Science Foundation of China
ID : 31702245
Organisme : China Postdoctoral Science Foundation 2017T100410
Organisme : Earmarked Fund For China Agriculture Research System CARS-40
Organisme : Taishan Scholars program of Shandong Province
ID : ts201511056
Organisme : Priority Academic Program Development of Jiangsu Higher Education Institutions
Organisme : Jiangsu Qinglan Project and the High-end talent support programme of Yangzhou University
Informations de copyright
© 2019 Blackwell Verlag GmbH.
Références
Abe, Y., Takashita, E., Sugawara, K., Matsuzaki, Y., Muraki, Y., & Hongo, S. (2004). Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. Journal of Virology, 78, 9605-9611. https://doi.org/10.1128/JVI.78.18.9605-9611.2004
Bush, R. M., Fitch, W. M., Bender, C. A., & Cox, N. J. (1999). Positive selection on the H3 hemagglutinin gene of human influenza virus A. Molecular Biology and Evolution, 16, 1457-1465. https://doi.org/10.1093/oxfordjournals.molbev.a026057
Cai, Z., Zhang, T., & Wan, X. F. (2010). A computational framework for influenza antigenic cartography. PLoS Computational Biology, 6, e1000949. https://doi.org/10.1371/journal.pcbi.1000949
Cai, Z., Zhang, T., & Wan, X. F. (2011). Concepts and applications for influenza antigenic cartography. Influenza and Other Respiratory Viruses, 5(Suppl 1), 204-207.
Caton, A. J., Brownlee, G. G., Yewdell, J. W., & Gerhard, W. (1982). The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell, 31, 417-427. https://doi.org/10.1016/0092-8674(82)90135-0
Claes, F., Morzaria, S. P., & Donis, R. O. (2016). Emergence and dissemination of clade 2.3.4.4 H5Nx influenza viruses-how is the Asian HPAI H5 lineage maintained. Current Opinion in Virology, 16, 158-163. https://doi.org/10.1016/j.coviro.2016.02.005
de Jong, J. C., Claas, E. C., Osterhaus, A. D., Webster, R. G., & Lim, W. L. (1997). A pandemic warning? Nature, 389, 554. https://doi.org/10.1038/39218
Ding, X., Jiang, L., Ke, C., Yang, Z., Lei, C., Cao, K., … Li, M. (2010). Amino acid sequence analysis and identification of mutations under positive selection in hemagglutinin of 2009 influenza A (H1N1) isolates. Virus Genes, 41, 329-340. https://doi.org/10.1007/s11262-010-0526-z
Ducatez, M. F., Bahl, J., Griffin, Y., Stigger-Rosser, E., Franks, J., Barman, S., … Webby, R. J. (2011). Feasibility of reconstructed ancestral H5N1 influenza viruses for cross-clade protective vaccine development. Proceedings of the National Academy of Sciences, USA, 108, 349-354. https://doi.org/10.1073/pnas.1012457108
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797. https://doi.org/10.1093/nar/gkh340
Fouchier, R. A., Munster, V., Wallensten, A., Bestebroer, T. M., Herfst, S., Smith, D., … Osterhaus, A. D. (2005). Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. Journal of Virology, 79, 2814-2822. https://doi.org/10.1128/JVI.79.5.2814-2822.2005
Gu, M., Zhao, G., Zhao, K., Zhong, L., Huang, J., Wan, H., … Liu, X. (2013). Novel variants of clade 2.3.4 highly pathogenic avian influenza A(H5N1) viruses, China. Emerging Infectious Diseases, 19, 2021-2024. https://doi.org/10.3201/eid1912.130340
Ha, Y., Stevens, D. J., Skehel, J. J., & Wiley, D. C. (2002). H5 avian and H9 swine influenza virus haemagglutinin structures: Possible origin of influenza subtypes. EMBO Journal, 21, 865-875. https://doi.org/10.1093/emboj/21.5.865
Hoffmann, E., Stech, J., Guan, Y., Webster, R. G., & Perez, D. R. (2001). Universal primer set for the full-length amplification of all influenza A viruses. Archives of Virology, 146, 2275-2289. https://doi.org/10.1007/s007050170002
Hoper, D., Kalthoff, D., Hoffmann, B., & Beer, M. (2012). Highly pathogenic avian influenza virus subtype H5N1 escaping neutralization: More than HA variation. Journal of Virology, 86, 1394-1404. https://doi.org/10.1128/JVI.00797-11
Hu, J., Hu, Z., Mo, Y., Wu, Q., Cui, Z., Duan, Z., … Liu, X. (2013). The PA and HA gene-mediated high viral load and intense innate immune response in the brain contribute to the high pathogenicity of H5N1 avian influenza virus in mallard ducks. Journal of Virology, 87, 11063-11075. https://doi.org/10.1128/JVI.00760-13
Jagger, B. W., Wise, H. M., Kash, J. C., Walters, K. A., Wills, N. M., Xiao, Y. L., … Digard, P. (2012). An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science, 337, 199-204. https://doi.org/10.1126/science.1222213
Kaverin, N. V., Rudneva, I. A., Govorkova, E. A., Timofeeva, T. A., Shilov, A. A., Kochergin-Nikitsky, K. S., … Webster, R. G. (2007). Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. Journal of Virology, 81, 12911-12917. https://doi.org/10.1128/JVI.01522-07
Kaverin, N. V., Rudneva, I. A., Ilyushina, N. A., Varich, N. L., Lipatov, A. S., Smirnov, Y. A., … Webster, R. G. (2002). Structure of antigenic sites on the haemagglutinin molecule of H5 avian influenza virus and phenotypic variation of escape mutants. Journal of General Virology, 83, 2497-2505. https://doi.org/10.1099/0022-1317-83-10-2497
Laver, W. G., Downie, J. C., & Webster, R. G. (1974). Studies on antigenic variation in influenza virus. Evidence for multiple antigenic determinants on the hemagglutinin subunits of A-Hong Kong-68 (H3 N2) virus and the A-England-72 strains. Virology, 59, 230-244. https://doi.org/10.1016/0042-6822(74)90218-9
Li, J., Gu, M., Liu, D., Liu, B., Jiang, K., Zhong, L., … Liu, X. (2016). Phylogenetic and biological characterization of three K1203 (H5N8)-like avian influenza A virus reassortants in China in 2014. Archives of Virology, 161, 289-302. https://doi.org/10.1007/s00705-015-2661-2
Li, Q., Wang, X., Gu, M., Zhu, J., Hao, X., Gao, Z., … Liu, X. (2014). Novel H5 clade 2.3.4.6 viruses with both alpha-2,3 and alpha-2,6 receptor binding properties may pose a pandemic threat. Veterinary Research, 45, 127.
Li, Y., Zhang, X., Xu, Q., Fu, Q., Zhu, Y., Chen, S., … Liu, X. (2013). Characterisation and haemagglutinin gene epitope mapping of a variant strain of H5N1 subtype avian influenza virus. Veterinary Microbiology, 162, 614-622. https://doi.org/10.1016/j.vetmic.2012.11.033
Ministry, C. s. A., 2015c. Reassortant Avian Influenza Virus, Inactivated (H5N1 Subtype, Strain Re-8) Vaccine. Available at: http://www.guojixumu.com/newsall.aspx?xml:id=3880.
Ministry, C. s. A., 2015a. Reassortant Avian Influenza virus, (Strain Re-6/Re-7+Re-8, and Re-6+Re-8) Vaccine.
Ministry, C. s. A., 2015b. Reassortant Avian Influenza Virus, Inactivated (H5N1 Subtype, Strain Re-6/Re-7) Vaccine. Available at: http://www.guojixumu.com/newsall.aspx?xml:id=5640.
Munoz, E. T., & Deem, M. W. (2005). Epitope analysis for influenza vaccine design. Vaccine, 23, 1144-1148. https://doi.org/10.1016/j.vaccine.2004.08.028
OIE (2013). Available at. http://www.oie.int/en/international-standard-setting/terrestrial-manual/.
Prabakaran, M., He, F., Meng, T., Madhan, S., Yunrui, T., Jia, Q., & Kwang, J. (2010). Neutralizing epitopes of influenza virus hemagglutinin: Target for the development of a universal vaccine against H5N1 lineages. Journal of Virology, 84, 11822-11830. https://doi.org/10.1128/JVI.00891-10
Reed, L. J., & Muench, H. (1938). A simple method of estimating fifty percent endpoints. American Journal of Epidemiology, 27, 5.
Rockman, S., Camuglia, S., Vandenberg, K., Ong, C., Baker, M. A., Nation, R. L., … Velkov, T. (2013). Reverse engineering the antigenic architecture of the haemagglutinin from influenza H5N1 clade 1 and 2.2 viruses with fine epitope mapping using monoclonal antibodies. Molecular Immunology, 53, 435-442. https://doi.org/10.1016/j.molimm.2012.10.001
Shi, S., Chen, S., Han, W., Wu, B., Zhang, X., Tang, Y., … Liu, X. (2016). Cross-clade protective immune responses of NS1-truncated live attenuated H5N1 avian influenza vaccines. Vaccine, 34, 350-357. https://doi.org/10.1016/j.vaccine.2015.11.045
Skehel, J. J., Stevens, D. J., Daniels, R. S., Douglas, A. R., Knossow, M., Wilson, I. A., & Wiley, D. C. (1984). A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proceedings of the National Academy of Sciences, USA, 81, 1779-1783. https://doi.org/10.1073/pnas.81.6.1779
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688-2690. https://doi.org/10.1093/bioinformatics/btl446
Subbarao, K., Klimov, A., Katz, J., Regnery, H., Lim, W., Hall, H., … Cox, N. (1998). Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science, 279, 393-396. https://doi.org/10.1126/science.279.5349.393
Sun, H., Pu, J., Hu, J., Liu, L., Xu, G., Gao, G. F., … Liu, J. (2016). Characterization of clade 2.3.4.4 highly pathogenic H5 avian influenza viruses in ducks and chickens. Veterinary Microbiology, 182, 116-122. https://doi.org/10.1016/j.vetmic.2015.11.001
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739. https://doi.org/10.1093/molbev/msr121
Tong, S., Li, Y., Rivailler, P., Conrardy, C., Castillo, D. A., Chen, L. M., … Donis, R. O. (2012). A distinct lineage of influenza A virus from bats. Proceedings of the National Academy of Sciences, USA, 109, 4269-4274. https://doi.org/10.1073/pnas.1116200109
Wang, H. (2002). Avian Respiratory Diseases. China Agricultural Press.
Wang, T. T., & Palese, P. (2009). Universal epitopes of influenza virus hemagglutinins? Nature Structural & Molecular Biology, 16, 233-234. https://doi.org/10.1038/nsmb.1574
WHO (2017). Zoonotic influenza viruses: Antigenic and genetic characteristics and development of candidate vaccine viruses for pandemic preparedness. Weekly Epidemiological Record, 92, 633-647.
WHO/OIE/FAO (2012). Continued evolution of highly pathogenic avian influenza A (H5N1): Updated nomenclature. Influenza and Other Respiratory Viruses, 6, 1-5.
WHO/OIE/FAO (2015). Evolution of the influenza A (H5) haemagglutinin.
Wiley, D. C., Wilson, I. A., & Skehel, J. J. (1981). Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature, 289, 373-378. https://doi.org/10.1038/289373a0
Wu, Y., Wu, Y., Tefsen, B., Shi, Y., & Gao, G. F. (2014). Bat-derived influenza-like viruses H17N10 and H18N11. Trends in Microbiology, 22, 183-191. https://doi.org/10.1016/j.tim.2014.01.010
Zhong, L., Zhao, Q., Zhao, K., Wang, X., Zhao, G., Li, Q., … Liu, X. (2014). The antigenic drift molecular basis of the H5N1 influenza viruses in a novel branch of clade 2.3.4. Veterinary Microbiology, 171, 23-30. https://doi.org/10.1016/j.vetmic.2014.02.033