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Emerging seasonal and pandemic influenza infections

Hemagglutinin glycosylation pattern-specific effects: implications for the fitness of H9.4.2.5-branched H9N2 avian influenza viruses

, , , , & ORCID Icon
Article: 2364736 | Received 27 Mar 2024, Accepted 02 Jun 2024, Published online: 14 Jun 2024

References

  • Hutchinson EC. Influenza virus. Trends Microbiol. 2018;26:809–810. doi:10.1016/j.tim.2018.05.013
  • Hale BG, Albrecht RA, Garcia-Sastre A. Innate immune evasion strategies of influenza viruses. Future Microbiol. 2010;5:23–41. doi:10.2217/fmb.09.108
  • Wu NC, Wilson IA. Influenza hemagglutinin structures and antibody recognition. Cold Spring Harb Perspect Med. 2020;10:a038778. doi:10.1101/cshperspect.a038778
  • Russell CJ, Hu M, Okda FA. Influenza hemagglutinin protein stability, activation, and pandemic risk. Trends Microbiol. 2018;26:841–853. doi:10.1016/j.tim.2018.03.005
  • Bhatt S, Holmes EC, Pybus OG. The genomic rate of molecular adaptation of the human influenza A virus. Mol Biol Evol. 2011;28:2443–2451. doi:10.1093/molbev/msr044
  • Khatri K, Klein JA, White MR, et al. Integrated omics and computational glycobiology reveal structural basis for influenza A virus glycan microheterogeneity and host interactions. Mol Cell Proteomics. 2016;15:1895–1912. doi:10.1074/mcp.M116.058016
  • Zost SJ, Parkhouse K, Gumina ME, et al. Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. Proc Natl Acad Sci U S A. 2017;114:12578–12583. doi:10.1073/pnas.1712377114
  • Chang D, Zaia J. Why glycosylation matters in building a better flu vaccine. Mol Cell Proteomics. 2019;18:2348–2358. doi:10.1074/mcp.R119.001491
  • An Y, McCullers JA, Alymova I, et al. Glycosylation analysis of engineered H3N2 influenza a virus hemagglutinins with sequentially added historically relevant glycosylation sites. J Proteome Res. 2015;14:3957–3969. doi:10.1021/acs.jproteome.5b00416
  • Kim JI, Lee I, Park S, et al. Genetic requirement for hemagglutinin glycosylation and its implications for influenza A H1N1 virus evolution. J Virol. 2013;87:7539–7549. doi:10.1128/JVI.00373-13
  • Zhang M, Gaschen B, Blay W, et al. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology. 2004;14:1229–1246. doi:10.1093/glycob/cwh106
  • Das SR, Hensley SE, David A, et al. Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. P Natl Acad Sci USA. 2011;108:E1417–E1422. doi:10.1073/pnas.1108754108
  • Altman MO, Angel M, Kosik I, et al. Human influenza A virus hemagglutinin glycan evolution follows a temporal pattern to a glycan limit. mBio. 2019;10:e00204–e00219. doi:10.1128/mBio.00204-19
  • Peacock TP, Harvey WT, Sadeyen JR, et al. The molecular basis of antigenic variation among A(H9N2) avian influenza viruses. Emerg Microbes Infect. 2018;7:176. doi:10.1038/s41426-018-0178-y
  • Guo J, Wang Y, Zhao C, et al. Molecular characterization, receptor binding property, and replication in chickens and mice of H9N2 avian influenza viruses isolated from chickens, peafowls, and wild birds in eastern China. Emerg Microbes Infect. 2021;10:2098–2112. doi:10.1080/22221751.2021.1999778
  • Sun Y, Liu J. H9N2 influenza virus in China: a cause of concern. Protein Cell. 2015;6:18–25. doi:10.1007/s13238-014-0111-7
  • Carnaccini S, Perez DR. H9 influenza viruses: an emerging challenge. Cold Spring Harb Perspect Med. 2020;10:a038588. doi:10.1101/cshperspect.a038588
  • Peacock THP, James J, Sealy JE, et al. A global perspective on H9N2 avian influenza virus. Viruses. 2019;11:640. doi:10.3390/v11070640
  • Song W, Qin K. Human-infecting influenza A (H9N2) virus: a forgotten potential pandemic strain? Zoonoses Public Health. 2020;67:203–212. doi:10.1111/zph.12685
  • Liu Q, Zhao L, Guo Y, et al. Antigenic evolution characteristics and immunological evaluation of H9N2 avian influenza viruses from 1994–2019 in China. Viruses; 2022:14:726. doi:10.3390/v14040726
  • Xia J, Li YX, Dong MY, et al. Evolution of prevalent H9N2 subtype of avian influenza virus during 2019 to 2022 for the development of a control strategy in China. Poult Sci. 2023;102:102957. doi:10.1016/j.psj.2023.102957
  • Hernandez R, Brown DT. Growth and maintenance of chick embryo fibroblasts (CEF). Curr Protoc Microbiol. 2010;Appendix 4:4I. doi:10.1002/9780471729259.mca04is17
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–425. doi:10.1093/oxfordjournals.molbev.a040454
  • Ye S, Evans JG, Stambas J. Influenza reverse genetics: dissecting immunity and pathogenesis. Expert Rev Mol Med. 2014;16:e2. doi:10.1017/erm.2014.4
  • Arai Y, Elgendy EM, Daidoji T, et al. H9N2 influenza virus infections in human cells require a balance between neuraminidase sialidase activity and hemagglutinin receptor affinity. J Virol. 2020;94:e01210–e01220. doi:10.1128/JVI.01210-20
  • Cong YL, Sun YX, Wang WL, et al. Comparative analysis of receptor-binding specificity and pathogenicity in natural reassortant and non-reassortant H3N2 swine influenza virus. Vet Microbiol. 2014;168:105–115. doi:10.1016/j.vetmic.2013.11.007
  • Sun Y, Cong Y, Yu H, et al. Assessing the effects of a two-amino acid flexibility in the Hemagglutinin 220-loop receptor-binding domain on the fitness of Influenza A(H9N2) viruses. Emerg Microbes Infect. 2021;10:822–832. doi:10.1080/22221751.2021.1919566
  • Smith DJ, Lapedes AS, de Jong JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science. 2004;305:371–376. doi:10.1126/science.1097211
  • Milder FJ, Jongeneelen M, Ritschel T, et al. Universal stabilization of the influenza hemagglutinin by structure- based redesign of the pH switch regions. Proc Natl Acad Sci U S A. 2022;119:e2115379119. doi:10.1073/pnas.2115379119
  • Lin YP, Xiong X, Wharton SA, et al. Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc Natl Acad Sci USA. 2012;109:21474–21479. doi:10.1073/pnas.1218841110
  • Wen F, Li L, Zhao N, et al. A Y161F hemagglutinin substitution increases thermostability and improves yields of 2009 H1N1 influenza A virus in cells. J Virol. 2018;92:e01621–17. doi:10.1128/JVI.01621-17
  • Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol. 1938;27: 493–497. doi:10.1093/oxfordjournals.aje.a118408
  • Kornfeld R, Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi:10.1146/annurev.bi.54.070185.003215
  • Wu NC, Thompson AJ, Xie J, et al. A complex epistatic network limits the mutational reversibility in the influenza hemagglutinin receptor-binding site. Nat Commun. 2018;9:1264. doi:10.1038/s41467-018-03663-5
  • Sun H, Deng G, Sun H, et al. N-linked glycosylation enhances hemagglutinin stability in avian H5N6 influenza virus to promote adaptation in mammals. PNAS Nexus. 2022;1:pgac085. doi:10.1093/pnasnexus/pgac085
  • 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;48:81. doi:10.1186/s13567-017-0484-8
  • Sun X, Belser JA, Pappas C, et al. Risk assessment of fifth-wave H7N9 influenza A viruses in mammalian models. J Virol. 2019;93:e01740–e01718. doi:10.1128/JVI.01740-18
  • Scull MA, Gillim-Ross L, Santos C, et al. Avian influenza virus glycoproteins restrict virus replication and spread through human airway epithelium at temperatures of the proximal airways. PLoS Pathog. 2009;5:e1000424. doi:10.1371/journal.ppat.1000424
  • Kaverin NV, Rudneva IA, Smirnov YA, et al. Human-avian influenza virus reassortants: effect of reassortment pattern on multi-cycle reproduction in MDCK cells. Arch Virol. 1988;103:117–126. doi:10.1007/BF01319813
  • Zhang N, Quan K, Chen Z, et al. The emergence of new antigen branches of H9N2 avian influenza virus in China due to antigenic drift on hemagglutinin through antibody escape at immunodominant sites. Emerg Microbes Infect. 2023;12:2246582. doi:10.1080/22221751.2023.2246582
  • Yang H, Carney PJ, Donis RO, et al. Structure and receptor complexes of the hemagglutinin from a highly pathogenic H7N7 influenza virus. J Virol. 2012;86:8645–8652. doi:10.1128/JVI.00281-12
  • Ohuchi M, Ohuchi R, Feldmann A, et al. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol. 1997;71:8377–8384. doi:10.1128/jvi.71.11.8377-8384.1997
  • Gaymard A, Le Briand N, Frobert E, et al. Functional balance between neuraminidase and haemagglutinin in influenza viruses. Clin Microbiol Infect. 2016;22:975–983. doi:10.1016/j.cmi.2016.07.007
  • de Vries E, Du W, Guo H, et al. Influenza A virus hemagglutinin-neuraminidase-receptor balance: preserving virus motility. Trends Microbiol. 2020;28:57–67. doi:10.1016/j.tim.2019.08.010
  • Sakai T, Nishimura SI, Naito T, et al. Influenza A virus hemagglutinin and neuraminidase act as novel motile machinery. Sci Rep. 2017;7:45043. doi:10.1038/srep45043
  • Pu J, Wang SG, Yin YB, et al. Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus. Proc Natl Acad Sci USA. 2015;112:548–553. doi:10.1073/pnas.1422456112
  • Zhang P, Tang Y, Liu X, et al. Characterization of H9N2 influenza viruses isolated from vaccinated flocks in an integrated broiler chicken operation in eastern China during a 5 year period (1998-2002). J Gen Virol. 2008;89:3102–3112. doi:10.1099/vir.0.2008/005652-0
  • Medina RA, Stertz S, Manicassamy B, et al. Glycosylations in the globular head of the hemagglutinin protein modulate the virulence and antigenic properties of the H1N1 influenza viruses. Sci Transl Med. 2013;5:187ra170. doi:10.1126/scitranslmed.3005996
  • Wei CJ, Boyington JC, Dai K, et al. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci Transl Med. 2010;2:24ra21. doi:10.1126/scitranslmed.3000799
  • Eggink D, Goff PH, Palese P. Guiding the immune response against influenza virus hemagglutinin toward the conserved stalk domain by hyperglycosylation of the globular head domain. J Virol. 2014;88:699–704. doi:10.1128/JVI.02608-13
  • Bajic G, Maron MJ, Adachi Y, et al. Influenza antigen engineering focuses immune responses to a subdominant but broadly protective viral epitope. Cell Host Microbe. 2019;25:827–835. doi:10.1016/j.chom.2019.04.003
  • Thornlow DN, Macintyre AN, Oguin TH, et al. Altering the immunogenicity of hemagglutinin immunogens by hyperglycosylation and disulfide stabilization. Front Immunol. 2021;12:737973. doi:10.3389/fimmu.2021.737973
  • Boyoglu-Barnum S, Hutchinson GB, Boyington JC, et al. Glycan repositioning of influenza hemagglutinin stem facilitates the elicitation of protective crossgroup antibody responses. Nat Commun. 2020;11:791. doi:10.1038/s41467-020-14579-4
  • Fan M, Liang B, Zhao Y, et al. Mutations of 127, 183 and 212 residues on the HA globular head affect the antigenicity, replication and pathogenicity of H9N2 avian influenza virus. Transbound Emerg Dis. 2022;69:e659–e670. doi:10.1111/tbed.14363
  • Watanabe Y, Bowden TA, Wilson IA, et al. Exploitation of glycosylation in enveloped virus pathobiology. Biochim Biophys Acta Gen Subj. 2019;1863:1480–1497. doi:10.1016/j.bbagen.2019.05.012
  • Carr CM, Chaudhry C, Kim PS. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci USA. 1997;94:14306–14313. doi:10.1073/pnas.94.26.14306
  • Russier M, Yang G, Briard B, et al. Hemagglutinin stability regulates H1N1 influenza virus replication and pathogenicity in mice by modulating type I interferon responses in dendritic cells. J Virol. 2020;94(3):e01423-19. doi:10.1128/JVI.01423-19
  • Poulson RL, Tompkins SM, Berghaus RD, et al. Environmental stability of swine and human pandemic influenza viruses in water under variable conditions of temperature, salinity, and pH. Appl Environ Microbiol. 2016;82:3721–3726. doi:10.1128/AEM.00133-16
  • Labadie T, Batejat C, Manuguerra JC, et al. Influenza virus segment composition influences viral stability in the environment. Front Microbiol. 2018;9:1496. doi:10.3389/fmicb.2018.01496
  • Jiang W, Liu S, Hou G, et al. Chinese and global distribution of H9 subtype avian influenza viruses. PLoS One. 2012;7:e52671. doi:10.1371/journal.pone.0052671
  • Deng G, Tan D, Shi J, et al. Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the Dongting Lake Region of China. J Virol. 2013;87:9452–9462. doi:10.1128/JVI.00776-13