Virulence and transmission characteristics of clade 2.3.4.4b H5N6 subtype avian influenza viruses possessing different internal gene constellations

References

• Nunez IA, Ross TM. A review of H5Nx avian influenza viruses. Ther Adv Vaccines Immunother. 2019;7:2515135518821625. doi: 10.1177/2515135518821625
   Google Scholar
• Revised and updated nomenclature for highly pathogenic avian influenza a (H5N1) viruses . Influenza and other respiratory viruses. Influenza Other Respir Viruses. 2014;8(3):384–14. doi: 10.1111/irv.12230
   PubMed Web of Science ®Google Scholar
• Zhang R, Chen T, Ou X, et al. Clinical, epidemiological and virological characteristics of the first detected human case of avian influenza A(H5N6) virus. Infect Genet Evol. 2016;40:236–242. doi: 10.1016/j.meegid.2016.03.010
   PubMed Web of Science ®Google Scholar
• Bi Y, Chen Q, Wang Q, et al. Genesis, evolution and prevalence of H5N6 avian influenza viruses in China. Cell Host Microbe. 2016;20(6):810–821. doi: 10.1016/j.chom.2016.10.022
   PubMed Web of Science ®Google Scholar
• Zhang Q, Mei X, Zhang C, et al. Novel reassortant 2.3.4.4B H5N6 highly pathogenic avian influenza viruses circulating among wild, domestic birds in Xinjiang, Northwest China. J Vet Sci. 2021;22(4):e43. doi: 10.4142/jvs.2021.22.e43
   PubMed Web of Science ®Google Scholar
• Li Y, Li M, Li Y, et al. Outbreaks of highly pathogenic avian influenza (H5N6) virus Subclade 2.3.4.4h in Swans, Xinjiang, Western China, 2020. Emerg Infect Dis. 2020;26(12):2956–2960. doi: 10.3201/eid2612.201201
   PubMed Web of Science ®Google Scholar
• Turner JCM, Barman S, Feeroz MM, et al. Highly pathogenic avian influenza A(H5N6) virus clade 2.3.4.4h in wild birds and live poultry markets, Bangladesh. Emerg Infect Dis. 2021;27(9):2492–2494. doi: 10.3201/eid2709.210819
   PubMed Web of Science ®Google Scholar
• Jeong S, Otgontogtokh N, Lee DH, et al. Highly pathogenic avian influenza clade 2.3.4.4 subtype H5N6 viruses isolated from wild Whooper Swans, Mongolia, 2020. Emerg Infect Dis. 2021;27(4):1181–1183. doi: 10.3201/eid2704.203859
   PubMed Web of Science ®Google Scholar
• Gu W, Shi J, Cui P, et al. Novel H5N6 reassortants bearing the clade 2.3.4.4b HA gene of H5N8 virus have been detected in poultry and caused multiple human infections in China. Emerg Microbes Infect. 2022;11(1):1174–1185. doi: 10.1080/22221751.2022.2063076
   PubMed Web of Science ®Google Scholar
• Shi W, Gao GF. Emerging H5N8 avian influenza viruses. Science. 2021;372(6544):784–786. doi: 10.1126/science.abg6302
   PubMed Web of Science ®Google Scholar
• Zhao K, Gu M, Zhong L, et al. Characterization of three H5N5 and one H5N8 highly pathogenic avian influenza viruses in China. Vet Microbiol. 2013;163(3–4):351–357. doi: 10.1016/j.vetmic.2012.12.025
   PubMed Web of Science ®Google Scholar
• Verhagen JH, Fouchier RAM, Lewis N. Highly pathogenic avian influenza viruses at the wild–domestic bird interface in Europe: future directions for Research and surveillance. Viruses. 2021;13(2):212. doi: 10.3390/v13020212
   PubMed Web of Science ®Google Scholar
• Li X, Lv X, Li Y, et al. Emergence, prevalence, and evolution of H5N8 avian influenza viruses in central China, 2020. Emerg Microbes Infect. 2022;11(1):73–82. doi: 10.1080/22221751.2021.2011622
   PubMed Web of Science ®Google Scholar
• Cui Y, Li Y, Li M, et al. Evolution and extensive reassortment of H5 influenza viruses isolated from wild birds in China over the past decade. Emerg Microbes Infect. 2020;9(1):1793–1803. doi: 10.1080/22221751.2020.1797542
   PubMed Web of Science ®Google Scholar
• Seekings AH, Warren CJ, Thomas SS, et al. Highly pathogenic avian influenza virus H5N6 (clade 2.3.4.4b) has a preferable host tropism for waterfowl reflected in its inefficient transmission to terrestrial poultry. Virology. 2021;559:74–85. doi: 10.1016/j.virol.2021.03.010
   PubMed Web of Science ®Google Scholar
• WHO. Human infection with avian influenza A(H5) viruses [M/OL]. 2020. https://apps.who.int/iris/bitstream/handle/10665/365675/AI-20230310.pdf?sequence=76&isAllowed=y.
   Google Scholar
• Hoffmann E, Stech J, Guan Y, et al. Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol. 2001;146(12):2275–2289. doi: 10.1007/s007050170002
   PubMed Web of Science ®Google Scholar
• Reed LJ, Muench H. A Simple method of estimating fifty per cent endpoints12. Am J Epidemiol. 1938;27(3):493–497. doi: 10.1093/oxfordjournals.aje.a118408
   Google Scholar
• Wang Z, Yang H, CHEN Y, et al. A single-amino-acid substitution at position 225 in hemagglutinin alters the transmissibility of Eurasian avian-like H1N1 swine influenza virus in guinea pigs. J Virol. 2017;91(21): doi: 10.1128/JVI.00800-17
   Web of Science ®Google Scholar
• Gao R, Gu M, Shi L, et al. N-linked glycosylation at site 158 of the HA protein of H5N6 highly pathogenic avian influenza virus is important for viral biological properties and host immune responses. Vet Res. 2021;52(1):8. doi: 10.1186/s13567-020-00879-6
   PubMed Web of Science ®Google Scholar
• Huang J, Wu S, Wu W, et al. The biological characteristics of novel H5N6 highly pathogenic avian influenza virus and its pathogenesis in ducks. Front Microbiol. 2021;12:628545. doi: 10.3389/fmicb.2021.628545
   PubMed Web of Science ®Google Scholar
• Munier S, Larcher T, Cormier-aline F, et al. A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J Virol. 2010;84(2):940–952. doi: 10.1128/JVI.01581-09
   PubMed Web of Science ®Google Scholar
• Guo F, Li Y, Yu S, et al. Adaptive evolution of human-isolated H5Nx avian influenza a viruses. Front Microbiol. 2019;10:1328. doi: 10.3389/fmicb.2019.01328
   PubMed Web of Science ®Google Scholar
• Herfst S, Schrauwen EJ, Linster M, et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science. 2012;336(6088):1534–1541. doi: 10.1126/science.1213362
   PubMed Web of Science ®Google Scholar
• Conenello GM, Zamarin D, Perrone LA, et al. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza a viruses contributes to increased virulence. PLoS Pathog. 2007;3(10):1414–1421. doi: 10.1371/journal.ppat.0030141
   PubMed Web of Science ®Google Scholar
• Lewis NS, Banyard AC, Whittard E, et al. Emergence and spread of novel H5N8, H5N5 and H5N1 clade 2.3.4.4 highly pathogenic avian influenza in 2020. Emerg Microbes Infect. 2021;10(1):148–151. doi: 10.1080/22221751.2021.1872355
   PubMed Web of Science ®Google Scholar
• Cui P, Shi J, Wang C, et al. Global dissemination of H5N1 influenza viruses bearing the clade 2.3.4.4b HA gene and biologic analysis of the ones detected in China. Emerg Microbes Infect. 2022;11(1):1693–1704. doi: 10.1080/22221751.2022.2088407
   PubMed Web of Science ®Google Scholar
• Hao X, Wang J, Hu J, et al. Internal gene Cassette from a genotype S H9N2 avian influenza virus Attenuates the pathogenicity of H5 viruses in chickens and mice. Front Microbiol. 2017;8:1978. doi: 10.3389/fmicb.2017.01978
   PubMed Web of Science ®Google Scholar
• Liu K, Gu M, Hu S, et al. Genetic and biological characterization of three poultry-origin H5N6 avian influenza viruses with all internal genes from genotype S H9N2 viruses. Arch Virol. 2018;163(4):947–960. doi: 10.1007/s00705-017-3695-4
   PubMed Web of Science ®Google Scholar
• Yang R, Sun H, Gao F, et al. Human infection of avian influenza a H3N8 virus and the viral origins: a descriptive study. The Lancet Microbe. 2022;3(11):e824–e834. doi: 10.1016/S2666-5247(22)00192-6
   PubMedGoogle Scholar
• Ge Z, Gu M, Cai T, et al. Phylogenetic tracing and biological characterization of a novel clade 2.3.2.1 reassortant of H5N6 subtype avian influenza virus in China. Transbound Emerg Dis. 2021;68(2):730–741. doi: 10.1111/tbed.13736
   PubMed Web of Science ®Google Scholar
• Bo H, Zhang Y, Dong J, et al. Distribution and gene characteristics of H3, H4 and H6 subtypes of low pathogenic avian influenza viruses in environment related avian influenza viruses during 2014-2021 in China. Zhonghua Yu Fang Yi Xue Za Zhi. 2022;56(11):1549–1553. doi: 10.3760/cma.j.cn112150-20220810-00803
   PubMedGoogle Scholar
• De Vries E, Du W, Guo H, et al. Influenza a virus hemagglutinin-neuraminidase-receptor balance: Preserving virus Motility. Trends Microbiol. 2020;28(1):57–67. doi: 10.1016/j.tim.2019.08.010
   PubMed Web of Science ®Google Scholar
• Gu M, Xu L, Wang X, et al. Current situation of H9N2 subtype avian influenza in China. Vet Res. 2017;48(1):49. doi: 10.1186/s13567-017-0453-2
   PubMed Web of Science ®Google Scholar
• Liu K, Ding P, Pei Y, et al. Emergence of a novel reassortant avian influenza virus (H10N3) in Eastern China with high pathogenicity and respiratory droplet transmissibility to mammals. Sci China Life Sci. 2022;65(5):1024–1035. doi: 10.1007/s11427-020-1981-5
   PubMed Web of Science ®Google Scholar
• Tan X, Yan X, Liu Y, et al. A case of human infection by H3N8 influenza virus. Emerg Microbes Infect. 2022;11(1):2214–2217. doi: 10.1080/22221751.2022.2117097
   PubMed Web of Science ®Google Scholar
• Scheibner D, Breithaupt A, Luttermann C, et al. Genetic determinants for virulence and transmission of the panzootic avian influenza virus H5N8 clade 2.3.4.4 in Pekin ducks. J Virol. 2022;96(13):e0014922. doi: 10.1128/jvi.00149-22
   PubMed Web of Science ®Google Scholar
• Leyson CM, Youk S, Ferreira HL, et al. Multiple gene segments are associated with enhanced virulence of clade 2.3.4.4 H5N8 highly pathogenic avian influenza virus in Mallards. J Virol. 2021;95(18):e0095521. doi: 10.1128/JVI.00955-21
   PubMed Web of Science ®Google Scholar
• Wille M, Barr IG. Resurgence of avian influenza virus. Science. 2022;376(6592):459–460. doi: 10.1126/science.abo1232
   PubMed Web of Science ®Google Scholar
• Zeng X-Y, He X-W, Meng F, et al. Protective efficacy of an H5/H7 trivalent inactivated vaccine (H5-Re13, H5-Re14, and H7-Re4 strains) in chickens, ducks, and geese against newly detected H5N1, H5N6, H5N8, and H7N9 viruses. J Integr Agr. 2022;21(7):2086–2094. doi: 10.1016/S2095-3119(22)63904-2
   Web of Science ®Google Scholar
• Ling YH, Wang H, Han MQ, et al. Nucleoporin 85 interacts with influenza a virus PB1 and PB2 to promote its replication by facilitating nuclear import of ribonucleoprotein. Front Microbiol. 2022;13:895779. doi: 10.3389/fmicb.2022.895779
   PubMed Web of Science ®Google Scholar
• Pflug A, Guilligay D, Reich S, et al. Structure of influenza a polymerase bound to the viral RNA promoter. Nature. 2014;516(7531):355–360. doi: 10.1038/nature14008
   PubMed Web of Science ®Google Scholar
• Dawson AR, Wilson GM, Freiberger EC, et al. Phosphorylation controls RNA binding and transcription by the influenza virus polymerase. PLoS Pathog. 2020;16(9):e1008841. doi: 10.1371/journal.ppat.1008841
   PubMed Web of Science ®Google Scholar
• Li J, Liang L, Jiang L, et al. Viral RNA-binding ability conferred by SUMOylation at PB1 K612 of influenza a virus is essential for viral pathogenesis and transmission. PLoS Pathog. 2021;17(2):e1009336. doi: 10.1371/journal.ppat.1009336
   PubMed Web of Science ®Google Scholar
• Wang G, Zhao Y, Zhou Y, et al. PIAS1-mediated SUMOylation of influenza a virus PB2 restricts viral replication and virulence. PLoS Pathog. 2022;18(4):e1010446. doi: 10.1371/journal.ppat.1010446
   PubMed Web of Science ®Google Scholar
• Boravleva E, Treshchalina A, Postnikova Y, et al. Molecular characteristics, receptor specificity, and pathogenicity of avian influenza viruses isolated from wild ducks in Russia. Int J Mol Sci. 2022;23(18):10829. doi: 10.3390/ijms231810829
   PubMed Web of Science ®Google Scholar
• Xiao Y, Evseev D, Stevens CA, et al. Influenza PB1-F2 inhibits avian MAVS signaling. Viruses. 2020;12(4):409. doi: 10.3390/v12040409
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang J. PB1F2 from influenza a virus regulates the interaction between cytochrome C and cardiolipin. Membranes (Basel). 2022;12(8):795. doi: 10.3390/membranes12080795
   PubMed Web of Science ®Google Scholar
• Vasin AV, Temkina OA, Egorov VV, et al. Molecular mechanisms enhancing the proteome of influenza a viruses: an overview of recently discovered proteins. Virus Res. 2014;185:53–63. doi: 10.1016/j.virusres.2014.03.015
   PubMed Web of Science ®Google Scholar
• Hara K, Kashiwagi T, Hamada N, et al. Basic amino acids in the N-terminal half of the PB2 subunit of influenza virus RNA polymerase are involved in both transcription and replication. J Gen Virol. 2017;98(5):900–905. doi: 10.1099/jgv.0.000750
   PubMed Web of Science ®Google Scholar
• Whelan M, Pelchat M. Role of RNA polymerase II promoter-proximal pausing in viral transcription. Viruses. 2022;14(9):2029. doi: 10.3390/v14092029
   PubMed Web of Science ®Google Scholar
• Li B, Su G, Xiao C, et al. The PB2 co-adaptation of H10N8 avian influenza virus increases the pathogenicity to chickens and mice. Transbound Emerg Dis. 2022;69(4):1794–1803. doi: 10.1111/tbed.14157
   PubMed Web of Science ®Google Scholar