The role of glycosylation in the N-terminus of the hemagglutinin of a unique H4N2 with a natural polybasic cleavage site in virus fitness in vitro and in vivo

References

• Webster RG, Bean WJ, Gorman OT, et al. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56(1):152–179.
   PubMedGoogle Scholar
• Tong S, Zhu X, Li Y, et al. New world bats harbor diverse influenza A viruses. PLoS Pathog. 2013;9(10):e1003657.
   PubMed Web of Science ®Google Scholar
• Fouchier RA, Munster V, Wallensten A, et al. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol. 2005;79(5):2814–2822.
   PubMed Web of Science ®Google Scholar
• Alexander DJ. An overview of the epidemiology of avian influenza. Vaccine. 2007;25(30):5637–5644.
   PubMed Web of Science ®Google Scholar
• Abdelwhab El SM, Veits J, Mettenleiter TC. Genetic changes that accompanied shifts of low pathogenic avian influenza viruses toward higher pathogenicity in poultry. Virulence. 2013;4(6):441–452.
   PubMed Web of Science ®Google Scholar
• Klenk HD, Garten W. Host cell proteases controlling virus pathogenicity. Trends Microbiol. 1994;2(2):39–43.
   PubMedGoogle Scholar
• Steinhauer DA. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology. 1999;258(1):1–20.
   PubMed Web of Science ®Google Scholar
• Bosch FX, Garten W, Klenk HD, et al. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of Avian influenza viruses. Virology. 1981;113(2):725–735.
   PubMed Web of Science ®Google Scholar
• Londt BZ, Banks J, Alexander DJ. Highly pathogenic avian influenza viruses with low virulence for chickens in in vivo tests. Avian Pathol. 2007;36(5):347–350.
   PubMed Web of Science ®Google Scholar
• Ohuchi M, Orlich M, Ohuchi R, et al. Mutations at the cleavage site of the hemagglutinin after the pathogenicity of influenza virus A/chick/Penn/83 (H5N2). Virology. 1989;168(2):274–280.
   PubMed Web of Science ®Google Scholar
• Lee CW, Swayne DE, Linares JA, et al. H5N2 avian influenza outbreak in Texas in 2004: the first highly pathogenic strain in the United States in 20 years? J Virol. 2005;79(17):11412–11421.
   PubMed Web of Science ®Google Scholar
• Horimoto T, Kawaoka Y. Molecular changes in virulent mutants arising from avirulent avian influenza viruses during replication in 14-day-old embryonated eggs. Virology. 1995;206(1):755–759.
   PubMed Web of Science ®Google Scholar
• Stech O, Veits J, Abdelwhab EM, et al. The neuraminidase stalk deletion serves as major virulence determinant of H5N1 highly pathogenic avian influenza viruses in chicken. Sci Rep-Uk. 2015;5:13493.
   PubMed Web of Science ®Google Scholar
• Wasilenko JL, Lee CW, Sarmento L, et al. NP, PB1, and PB2 viral genes contribute to altered replication of H5N1 avian influenza viruses in chickens. J Virol. 2008;82(9):4544–4553.
   PubMed Web of Science ®Google Scholar
• Ohuchi R, Ohuchi M, Garten W, et al. Oligosaccharides in the stem region maintain the influenza virus hemagglutinin in the metastable form required for fusion activity. J Virol. 1997;71(5):3719–3725.
   PubMed Web of Science ®Google Scholar
• Chen W, Zhong Y, Qin Y, et al. The evolutionary pattern of glycosylation sites in influenza virus (H5N1) hemagglutinin and neuraminidase. PLoS One. 2012;7(11):e49224.
   PubMed Web of Science ®Google Scholar
• Kawaoka Y, Naeve CW, Webster RG. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology. 1984;139(2):303–316.
   PubMed Web of Science ®Google Scholar
• Yin Y, Zhang X, Qiao Y, et al. Glycosylation at 11Asn on hemagglutinin of H5N1 influenza virus contributes to its biological characteristics. Vet Res. 2017;48(1):81.
   PubMedGoogle Scholar
• Gohrbandt S, Veits J, Breithaupt A, et al. H9 avian influenza reassortant with engineered polybasic cleavage site displays a highly pathogenic phenotype in chicken. J Gen Virol. 2011;92(Pt 8):1843–1853.
   PubMedGoogle Scholar
• Munster VJ, Schrauwen EJ, de Wit E, et al. Insertion of a multibasic cleavage motif into the hemagglutinin of a low-pathogenic avian influenza H6N1 virus induces a highly pathogenic phenotype. J Virol. 2010;84(16):7953–7960.
   PubMed Web of Science ®Google Scholar
• Veits J, Weber S, Stech O, et al. Avian influenza virus hemagglutinins H2, H4, H8, and H14 support a highly pathogenic phenotype. Proc Natl Acad Sci U S A. 2012;109(7):2579–2584.
   PubMed Web of Science ®Google Scholar
• Wong SS, Yoon SW, Zanin M, et al. Characterization of an H4N2 influenza virus from Quails with a multibasic motif in the hemagglutinin cleavage site. Virology. 2014;468-470:72–80.
   PubMed Web of Science ®Google Scholar
• Garten W, Bosch FX, Linder D, et al. Proteolytic activation of the influenza virus hemagglutinin: the structure of the cleavage site and the enzymes involved in cleavage. Virology. 1981;115(2):361–374.
   PubMed Web of Science ®Google Scholar
• Katoh K, Standley DM. MAFFT: iterative refinement and additional methods. Methods Mol Biol. 2014;1079:131–146.
   PubMedGoogle Scholar
• Gischke M, Ulrich R, O IF, et al. Insertion of basic amino acids in the hemagglutinin cleavage site of H4N2 avian influenza virus (AIV)-Reduced virus fitness in chickens is restored by reassortment with highly pathogenic H5N1 AIV. Int J Mol Sci. 2020;21(7):2353.
   PubMed Web of Science ®Google Scholar
• Bottcher E, Matrosovich T, Beyerle M, et al. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J Virol. 2006;80(19):9896–9898.
   PubMed Web of Science ®Google Scholar
• Choi JW, Shin EK, Ha SH, et al. Optimal conditions for cryopreservation of primary chicken embryo kidney cells with dimethyl sulfoxide. Mol Biotechnol. 2007;35(3):237–241.
   PubMed Web of Science ®Google Scholar
• Stech J, Stech O, Herwig A, et al. Rapid and reliable universal cloning of influenza A virus genes by target-primed plasmid amplification. Nucleic Acids Res. 2008;36(21):e139.
   PubMed Web of Science ®Google Scholar
• Alexander DJ Avian Influenza: OIE; 2015 [23]. [cited 2017 Oct 22]. Available from: https://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.03.04_AI.pdf
   Google Scholar
• Mahmood T, Yang PC. Western blot: technique, theory, and trouble shooting. N Am J Med Sci. 2012;4(9):429–434.
   PubMedGoogle Scholar
• Matrosovich MN, Gambaryan AS. Solid-phase assays of receptor-binding specificity. Methods Mol Biol. 2012;865:71–94.
   PubMedGoogle Scholar
• Zaraket H, Bridges OA, Duan S, et al. Increased acid stability of the hemagglutinin protein enhances H5N1 influenza virus growth in the upper respiratory tract but is insufficient for transmission in ferrets. J Virol. 2013;87(17):9911–9922.
   PubMed Web of Science ®Google Scholar
• Abdelwhab El SM, Veits J, Tauscher K, et al. A unique multibasic proteolytic cleavage site and three mutations in the HA2 domain confer high virulence of H7N1 avian influenza virus in chickens. J Virol. 2016;90(1):400–411.
   PubMed Web of Science ®Google Scholar
• Vallbracht M, Schröter C, Klupp B, et al. Transient transfection-based fusion assay for viral proteins. Bio-Protocol. 2017;7(5):e2162.
   PubMed Web of Science ®Google Scholar
• Graaf A, Ulrich R, Maksimov P, et al. A viral race for primacy: co-infection of a natural pair of low and highly pathogenic H7N7 avian influenza viruses in chickens and embryonated chicken eggs. Emerg Microbes Infect. 2018;7(1):204.
   PubMedGoogle Scholar
• Hoffmann B, Hoffmann D, Henritzi D, et al. Riems influenza a typing array (RITA): an RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses. Sci Rep-Uk. 2016;6:27211.
   PubMed Web of Science ®Google Scholar
• Tan L-G, Chen Z-K, Ma X-X, et al. Glycosylation of the hemagglutinin protein of H9N2 subtype avian influenza virus influences its replication and virulence in mice. J Integr Agri. 2019;18(7):1443–1450.
   Web of Science ®Google Scholar
• Baron J, Tarnow C, Mayoli-Nussle D, et al. Matriptase, HAT, and TMPRSS2 activate the hemagglutinin of H9N2 influenza A viruses. J Virol. 2013;87(3):1811–1820.
   PubMed Web of Science ®Google Scholar
• Kandeil A, Bagato O, Zaraket H, et al. Proteolytic enzymes in embryonated chicken eggs sustain the replication of egg-grown low-pathogenicity avian influenza viruses in cells in the absence of exogenous proteases. J Virol Methods. 2014;202:28–33. .
   PubMed Web of Science ®Google Scholar
• Abdelwhab EM, Veits J, Ulrich R, et al. Composition of the hemagglutinin polybasic proteolytic cleavage motif mediates variable virulence of H7N7 avian influenza viruses. Sci Rep. 2016;6:39505.
   PubMed Web of Science ®Google Scholar
• Wagner R, Heuer D, Wolff T, et al. N-Glycans attached to the stem domain of haemagglutinin efficiently regulate influenza A virus replication. J Gen Virol. 2002;83(Pt 3):601–609.
   PubMedGoogle Scholar
• Russell CJ, Hu M, Okda FA. Influenza hemagglutinin protein stability, activation, and pandemic risk. Trends Microbiol. 2018;26(10):841–853.
   PubMed Web of Science ®Google Scholar
• Scholtissek C. Stability of infectious influenza A viruses to treatment at low pH and heating. Arch Virol. 1985;85(1):1–11.
   PubMed Web of Science ®Google Scholar
• Scholtissek C. Stability of infectious influenza A viruses at low pH and at elevated temperature. Vaccine. 1985;3(3 Suppl):215–218.
   PubMed Web of Science ®Google Scholar
• Liao HY, Hsu CH, Wang SC, et al. Differential receptor binding affinities of influenza hemagglutinins on glycan arrays. J Am Chem Soc. 2010;132(42):14849–14856.
   PubMed Web of Science ®Google Scholar
• Keiner B, Maenz B, Wagner R, et al. Intracellular distribution of NS1 correlates with the infectivity and interferon antagonism of an avian influenza virus (H7N1). J Virol. 2010;84(22):11858–11865.
   PubMed Web of Science ®Google Scholar
• Hussain S, Turnbull ML, Wise HM, et al. Mutation of influenza a virus PA-X decreases pathogenicity in chicken embryos and can increase the yield of reassortant candidate vaccine viruses. J Virol. 2019;93(2):e01551–18.
   PubMed Web of Science ®Google Scholar
• Seekings AH, Howard WA, Nunez A, et al. The emergence of H7N7 highly pathogenic avian influenza virus from low pathogenicity avian influenza virus using an in ovo embryo culture model. Viruses. 2020;12(9). DOI:10.3390/v12090920.
   Web of Science ®Google Scholar