Characterization of neurotropic HPAI H5N1 viruses with novel genome constellations and mammalian adaptive mutations in free-living mesocarnivores in Canada

References

• Klenk HD, Rott R, Becht H. On the structure of the influenza virus envelope. Virology. 1972;47:579–591.
   PubMed Web of Science ®Google Scholar
• Shaw ML, Palese P. Orthomyxoviridae. In: Knipe D, Howley P, editor. Fields virology. Philadelphia, PA: Lippincott Williams & Wilkins; 2013. p. 1151–1185.
   Google Scholar
• McGeoch D, Fellner P, Newton C. Influenza virus genome consists of eight distinct RNA species. Proc Natl Acad Sci. 1976;73:3045–3049.
   PubMed Web of Science ®Google Scholar
• Bouvier NM, Palese P. The biology of influenza viruses. Vaccine. 2008;26(Suppl 4):D49–D53.
   PubMed Web of Science ®Google Scholar
• Sharp GB, Kawaoka Y, Jones DJ, et al. Coinfection of wild ducks by influenza A viruses: distribution patterns and biological significance. J Virol. 1997;71:6128–6135.
   PubMed Web of Science ®Google Scholar
• Süss J, Schäfer J, Sinnecker H, et al. Influenza virus subtypes in aquatic birds of eastern Germany. Arch Virol. 1994;135:101–114.
   PubMed Web of Science ®Google Scholar
• Xu X, Subbarao, Cox NJ, et al. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: Similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology. 1999;261:15–19.
   PubMed Web of Science ®Google Scholar
• Chen H, Smith GJ, Li KS, et al. Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci. 2006;103:2845–2850.
   PubMed Web of Science ®Google Scholar
• Cattoli G, Milani A, Temperton N, et al. Antigenic drift in H5N1 avian influenza virus in poultry is driven by mutations in major antigenic sites of the hemagglutinin molecule analogous to those for human influenza virus. J Virol. 2011;85:8718–8724.
   PubMed Web of Science ®Google Scholar
• Lycett SJ, Duchatel F, Digard P. A brief history of bird flu. Philos Trans R Soc Lond B Biol Sci. 2019;374:20180257.
   PubMed Web of Science ®Google Scholar
• Lee DH, Bahl J, Kim M, et al. Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014–2015. Emerg Infect Dis. 2016;22:1283–1285.
   PubMed Web of Science ®Google Scholar
• Poen MJ, Venkatesh D, Bestebroer TM, et al. Co-circulation of genetically distinct highly pathogenic avian influenza A clade 2.3.4.4 (H5N6) viruses in wild waterfowl and poultry in Europe and East Asia, 2017–18. Virus Evol. 2019;5:vez004.
   PubMed Web of Science ®Google Scholar
• Lin R, Lu L, Lycett S, et al. Dealing with highly pathogenic avian influenza: an impending crisis. Innovation. 2021;2:100084.
   Google Scholar
• Lee DH, Torchetti K, Winker K, et al. Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory birds. J Virol. 2015;89:6521–6524.
   PubMed Web of Science ®Google Scholar
• Pasick J, Berhane Y, Joseph T, et al. Reassortant highly pathogenic influenza A H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci Rep. 2015;5:9484.
   PubMed Web of Science ®Google Scholar
• Caliendo V, Lewis NS, Pohlmann A, et al. Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci Rep. 2022;12:11729.
   PubMed Web of Science ®Google Scholar
• Alkie TN, Lopes S, Hisanaga T, et al. A threat from both sides: Multiple introductions of genetically distinct H5 HPAI viruses into Canada via both East Asia-Australasia/Pacific and Atlantic flyways. Virus Evol. 2022;8:veac077.
   PubMed Web of Science ®Google Scholar
• Klopfleisch R, Wolf PU, Uhl W, et al. Distribution of lesions and antigen of highly pathogenic avian influenza virus A/swan/Germany/R65/06 (H5N1) in domestic cats after presumptive infection by wild birds. Vet Pathol. 2007;44:261–268.
   PubMed Web of Science ®Google Scholar
• Songserm T, Amonsin A, Jam-on R, et al. Fatal avian influenza A H5N1 in a dog. Emerg Infect Dis. 2006;12:1744–1747.
   PubMed Web of Science ®Google Scholar
• Keawcharoen J, Oraveerakul K, Kuiken T, et al. Avian influenza H5N1 in tigers and leopards. Emerg Infect Dis. 2004;10:2189–2191.
   PubMed Web of Science ®Google Scholar
• Hu T, Zhao H, Zhang Y, et al. Fatal influenza A (H5N1) virus infection in zoo-housed tigers in Yunnan Province, China. Sci Rep. 2016;6:25845.
   PubMed Web of Science ®Google Scholar
• Rijks JM, Hesselink H, Lollinga P, et al. Highly pathogenic avian influenza A(H5N1) virus in wild red foxes, The Netherlands, 2021. Emerg Infect Dis. 2021;27:2960–2962.
   PubMed Web of Science ®Google Scholar
• Sun H, Pu J, Wei Y, et al. Highly pathogenic avian influenza H5N6 viruses exhibit enhanced affinity for human type sialic acid receptor and in-contact transmission in model ferrets. J Virol. 2016;90:6235–6243.
   PubMed Web of Science ®Google Scholar
• Lee K, Lee EK, Lee H, et al. Highly pathogenic avian influenza A(H5N6) in domestic cats, South Korea. Emerg Infect Dis. 2018;24:2343–2347.
   PubMed Web of Science ®Google Scholar
• Floyd T, Banyard AC, Lean FZX, et al. Encephalitis and death in wild mammals at a rehabilitation center after infection with highly pathogenic avian influenza A(H5N8) virus, United Kingdom. Emerg Infect Dis. 2021;27:2856–2863.
   PubMed Web of Science ®Google Scholar
• Reperant LA, van Amerongen G, van de Bildt MW, et al. Highly pathogenic avian influenza virus (H5N1) infection in red foxes fed infected bird carcasses. Emerg Infect Dis. 2008;14:1835–1841.
   PubMed Web of Science ®Google Scholar
• Spackman E, Senne DA, Myers TJ, et al. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol. 2002;40:3256–3260.
   PubMed Web of Science ®Google Scholar
• Weingartl HM, Berhane Y, Hisanaga T, et al. Genetic and pathobiologic characterization of pandemic H1N1 2009 influenza viruses from a naturally infected swine herd. J Virol. 2010;84:2245–2256.
   PubMed Web of Science ®Google Scholar
• Chrzastek K, Lee DH, Smith D, et al. Use of sequence-independent, single-primer-amplification (SISPA) for rapid detection, identification, and characterization of avian RNA viruses. Virology. 2017;509:159–166.
   PubMed Web of Science ®Google Scholar
• Drummond AJ, Nicholls GK, Rodrigo AG, et al. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics. 2002;161:1307–1320.
   PubMed Web of Science ®Google Scholar
• Bouckaert R, Vaughan TG, Barido-Sottani J, et al. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 2019;15:e1006650.
   PubMed Web of Science ®Google Scholar
• Yang M, Berhane Y, Salo T, et al. Development and application of monoclonal antibodies against avian influenza virus nucleoprotein. J Virol Methods. 2008;147:265–274.
   PubMed Web of Science ®Google Scholar
• Yang M, Clavijo A, Graham J, et al. Production and diagnostic application of monoclonal antibodies against influenza virus H5. J Virol Methods. 2009;162:194–202.
   PubMed Web of Science ®Google Scholar
• Bussey KA, Bousse TL, Desmet EA, et al. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol. 2010;84:4395–4406.
   PubMed Web of Science ®Google Scholar
• Yamayoshi S, Yamada S, Fukuyama S, et al. Virulence-affecting amino acid changes in the PA protein of H7N9 influenza A viruses. J Virol. 2014;88:3127–3134.
   PubMed Web of Science ®Google Scholar
• Yamayoshi S, Kiso M, Yasuhara A, et al. Enhanced replication of highly pathogenic influenza A(H7N9) virus in humans. Emerg Infect Dis. 2018;24:746–750.
   PubMed Web of Science ®Google Scholar
• Gabriel G, Czudai-Matwich V, Klenk HD. Adaptive mutations in the H5N1 polymerase complex. Virus Res. 2013;178:53–62.
   PubMed Web of Science ®Google Scholar
• Taft AS, Ozawa M, Fitch A, et al. Identification of mammalian-adapting mutations in the polymerase complex of an avian H5N1 influenza virus. Nat Commun. 2015;17(6):7491.
   Google Scholar
• Li J, Ishaq M, Prudence M, et al. Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian influenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2. Virus Res. 2009;144:123–129.
   PubMed Web of Science ®Google Scholar
• Elgendy EM, Arai Y, Kawashita N, et al. Identification of polymerase gene mutations that affect viral replication in H5N1 influenza viruses isolated from Pigeons. J Gen Virol. 2017;98:6–17.
   PubMed Web of Science ®Google Scholar
• Feng X, Wang Z, Shi J, et al. Glycine at position 622 in PB1 contributes to the virulence of H5N1 avian influenza virus in mice. J Virol. 2016;90:1872–1879.
   PubMed Web of Science ®Google Scholar
• Gabriel G, Dauber B, Wolff T, et al. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci. 2005;102:18590–18595.
   PubMed Web of Science ®Google Scholar
• Gabriel G, Herwig A, Klenk HD. Interaction of polymerase subunit PB2 and NP with importin α1 Is a determinant of host range of influenza A virus. PLoS Pathog. 2008;4:e11.
   PubMed Web of Science ®Google Scholar
• Ramey AM, Hill NJ, DeLiberto TJ, et al. Highly Pathogenic avian influenza is an emerging disease threat to wild birds in North America. J Wildl Manage. 2022;86:e22171.
   Web of Science ®Google Scholar
• Shriner SA, Root JJ, Lutman MW, et al. Surveillance for highly pathogenic H5 avian influenza virus in synanthropic wildlife associated with poultry farms during an acute outbreak. Sci Rep. 2016;6:36237.
   PubMed Web of Science ®Google Scholar
• Jiang W, Wang S, Zhang C, et al. Characterization of H5N1 highly pathogenic mink influenza viruses in eastern China. Vet Microbiol. 2017;201:225–230.
   PubMed Web of Science ®Google Scholar
• Chutinimitkul S, van Riel D, Munster VJ, et al. In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity. J Virol. 2010;84:6825–6833.
   PubMed Web of Science ®Google Scholar
• Hatta M, Gao P, Halfmann P, et al. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science. 2001;293:1840–1842.
   PubMed Web of Science ®Google Scholar
• Liu WJ, Li J, Zou R, et al. Dynamic PB2-E627K substitution of influenza H7N9 virus indicates the in vivo genetic tuning and rapid host adaptation. Proc Natl Acad Sci. 2020;117:23807–23814.
   PubMed Web of Science ®Google Scholar
• Postel A, King J, Kaiser FK, et al. Infections with highly pathogenic avian influenza A virus (HPAIV) H5N8 in harbor seals at the German North Sea coast, 2021. Emerg Microbes Infect. 2022;11:725–729.
   PubMed Web of Science ®Google Scholar
• Herfst S, Mok CKP, van den Brand JMA, et al. Human clade 2.3.4.4 A/H5N6 influenza virus lacks mammalian adaptation markers and does not transmit via the airborne route between ferrets. mSphere. 2018;3:e00405–17.
   PubMed Web of Science ®Google Scholar
• Aggarwal S, Dewhurst S, Takimoto T, et al. Biochemical impact of the host adaptation-associated PB2 E627K mutation on the temperature-dependent RNA synthesis kinetics of influenza A virus polymerase complex. J Biol Chem. 2011;286:34504–34513.
   PubMed Web of Science ®Google Scholar
• Boivin S, Hart DJ. Interaction of the influenza A virus polymerase PB2 C-terminal region with importin α isoforms provides insights into host adaptation and polymerase assembly. J Biol Chem. 2011;286:10439–10448.
   PubMed Web of Science ®Google Scholar
• Delaforge E, Milles S, Bouvignies G, et al. Large-scale conformational dynamics control H5N1 influenza polymerase PB2 binding to importin α. J Am Chem Soc. 2015;137:15122–15134.
   PubMed Web of Science ®Google Scholar
• Resa-Infante P, Jorba N, Zamarreño N, et al. The host-dependent interaction of α-importins with influenza PB2 polymerase subunit Is required for virus RNA replication. PLoS One. 2008;3:e3904.
   PubMed Web of Science ®Google Scholar
• Weber M, Sediri H, Felgenhauer U, et al. Influenza virus adaptation PB2-627K modulates nucleocapsid inhibition by the pathogen sensor RIG-I. Cell Host Microbe. 2015;17:309–319.
   PubMed Web of Science ®Google Scholar
• Arai Y, Kawashita N, Ibrahim MS, et al. PB2 mutations arising during H9N2 influenza evolution in the Middle East confer enhanced replication and growth in mammals. PLoS Pathog. 2019;15:e1007919.
   PubMed Web of Science ®Google Scholar
• Luk GS, Leung CY, Sia SF, et al. Transmission of H7N9 influenza viruses with a polymorphism at PB2 residue 627 in chickens and ferrets. J Virol. 2015;89:9939–9951.
   PubMed Web of Science ®Google Scholar
• Steel J, Lowen AC, Mubareka S, et al. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 2009;5:e1000252.
   PubMed Web of Science ®Google Scholar
• Mok CK, Lee HH, Lestra M, et al. Amino acid substitutions in polymerase basic protein 2 gene contribute to the pathogenicity of the novel A/H7N9 influenza virus in mammalian hosts. J Virol. 2014;88:3568–3576.
   PubMed Web of Science ®Google Scholar