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Virology1983; 131(2); 394-408; doi: 10.1016/0042-6822(83)90507-x

Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants.

Abstract: Human and animal (avian and equine) influenza A virus isolates of the H3 serotype exhibit marked differences in their ability to bind specific sialyloligosaccharide sequences that serve as cell surface receptor determinants (G. Rogers and J. Paulson, 1983, Virology 127, 361-373). Whereas human isolates of this subtype strongly agglutinate enzymatically modified human erythrocytes containing the terminal SA alpha 2,6Gal sequence, avian and equine isolates preferentially agglutinate erythrocytes bearing the SA alpha 2, 3Gal sequence. As shown in this report, a glycoprotein found in horse serum, alpha 2-macroglobulin, is a potent inhibitor of viral adsorption to the cell surface for human H3 isolates. In contrast, avian and equine isolates are poorly inhibited suggesting a correlation between receptor specificity and inhibitor sensitivity. Growth of a human H3 isolate (A/Memphis/102/72) on MDCK cells in the presence of horse serum resulted in an overall shift in the virus receptor specificity from preferential binding of the SA alpha 2,6Gal linkage to preferential binding of the SA alpha 2,3Gal linkage characteristic of avian and equine isolates. Clonally isolated variants of A/Memphis/102/72 grown in the presence or absence of horse serum exhibited binding properties that account for those observed in the field isolates. Clones which preferentially bound the SA alpha 2,6Gal linkage, like the parent human virus, were very sensitive to inhibition of hemagglutination by horse serum and equine alpha 2-macroglobulin. In contrast, receptor variants which preferentially bound the SA alpha 2,3Gal linkage, like the avian and equine isolate, were insensitive to such inhibitors. None of the variants was very sensitive to inhibition of hemagglutination by human alpha 2-macroglobulin. These results suggest that the presence, in vivo, of a glycoprotein inhibitor such as equine alpha 2-macroglobulin could suppress infection of influenza viruses bearing an H3 hemagglutinin with a SA alpha 2,6Gal specific, inhibitor sensitive phenotype, allowing growth to predominance of a virus which is SA alpha 2,3Gal specific and inhibitor insensitive as found in avian and equine isolates.
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Publication Date: 1983-12-01 PubMed ID: 6197808DOI: 10.1016/0042-6822(83)90507-xGoogle Scholar: Lookup
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  • Comparative Study
  • Journal Article
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  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article investigates the differences in flu virus strains from humans, birds, and horses, and their sensitivity to a glycoprotein inhibitor. Researchers found that a horse serum glycoprotein inhibitor could potentially suppress the human influenza virus while having little effect on avian and equine viruses.

Study Overview

The study largely revolves around understanding different abilities of the H3 serotype influenza A virus, isolated from humans, birds, and horses, to bind with sialyloligosaccharide sequences on cell surfaces. These sequences play a role in the virus’s ability to infect cells. The nature of these sequences varies between different species, leading to the observed differences in the ability of different virus strains to bind them.

Experiment and Observations

  • While human-isolated viruses of H3 serotype strongly bind to cells containing specific sequences, avian and equine isolates prefer other specific sequences.
  • The researchers found that a glycoprotein in horse serum, alpha 2-macroglobulin, is a potent inhibitor of the virus’s ability to bind to the cell surface in instances of human isolates. Conversely, avian and equine isolates were less affected, suggesting a correlation between receptor specificity and sensitivity to the inhibitor.
  • When they grew a human H3 isolate on dog kidney cells (MDCK cells) in the presence of horse serum, they found that the virus’s receptor specificity shifted, showing a preference for the sequence favored by avian and equine isolates. This shift demonstrated the capacity for change under the influence of different environmental components.

Findings and Implications

  • The study also showed that different variants of the human H3 isolate that were grown with or without horse serum exhibited varying binding properties, reflecting the characteristics seen in human, avian, and equine isolates observed in the field. Variants that showed a preference for the sequence favored by the human virus were markedly sensitive to horse serum and the alpha 2-macroglobulin inhibitor. In contrast, variants favoring the sequence found in avian and equine viruses were generally resistant to such inhibitors.
  • These results led the researchers to speculate upon the potential role of a glycoprotein inhibitor such as equine alpha 2-macroglobulin in suppressing human influenza infection in vivo. A virus showing a preference for sequences found in avian and equine isolates and demonstrating resistance to the inhibitor could potentially grow to predominance.

The outcome of this research points to the potential use of glycoprotein inhibitors in controlling the spread of specific strains of the influenza virus in humans, offering possible directions for the development of new treatment strategies.

Cite This Article

APA
Rogers GN, Pritchett TJ, Lane JL, Paulson JC. (1983). Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology, 131(2), 394-408. https://doi.org/10.1016/0042-6822(83)90507-x

Publication

Virology
ISSN: 0042-6822
NlmUniqueID: 0110674
Country: United States
Language: English
Volume: 131
Issue: 2
Pages: 394-408

Researcher Affiliations

Rogers, G N
    Pritchett, T J
      Lane, J L
        Paulson, J C

          MeSH Terms

          • Adsorption
          • Animals
          • Chick Embryo
          • Ducks
          • Erythrocytes / immunology
          • Erythrocytes / microbiology
          • Glycoproteins / antagonists & inhibitors
          • Hemagglutination Inhibition Tests
          • Hemagglutination Tests
          • Hemagglutinins, Viral / analysis
          • Horses
          • Humans
          • Influenza A virus / drug effects
          • Receptors, Virus / drug effects
          • Viral Proteins / antagonists & inhibitors
          • alpha-Macroglobulins / pharmacology

          Grant Funding

          • AI-16165 / NIAID NIH HHS
          • GM07185 / NIGMS NIH HHS

          Citations

          This article has been cited 85 times.
          1. Scheibner D, Salaheldin AH, Bagato O, Zaeck LM, Mostafa A, Blohm U, Müller C, Eweas AF, Franzke K, Karger A, Schäfer A, Gischke M, Hoffmann D, Lerolle S, Li X, Abd El-Hamid HS, Veits J, Breithaupt A, Boons GJ, Matrosovich M, Finke S, Pleschka S, Mettenleiter TC, de Vries RP, Abdelwhab EM. Phenotypic effects of mutations observed in the neuraminidase of human origin H5N1 influenza A viruses. PLoS Pathog 2023 Feb;19(2):e1011135.
            doi: 10.1371/journal.ppat.1011135pubmed: 36745654google scholar: lookup
          2. Liu Y, Chen H, Duan W, Zhang X, He X, Nielsen R, Ma L, Zhai W. Predicting Egg Passage Adaptations to Design Better Vaccines for the H3N2 Influenza Virus. Viruses 2022 Sep 17;14(9).
            doi: 10.3390/v14092065pubmed: 36146872google scholar: lookup
          3. Kiseleva I. Current Opinion in LAIV: A Matter of Parent Virus Choice. Int J Mol Sci 2022 Jun 19;23(12).
            doi: 10.3390/ijms23126815pubmed: 35743258google scholar: lookup
          4. Wang Y, Tang CY, Wan XF. Antigenic characterization of influenza and SARS-CoV-2 viruses. Anal Bioanal Chem 2022 Apr;414(9):2841-2881.
            doi: 10.1007/s00216-021-03806-6pubmed: 34905077google scholar: lookup
          5. Chan L, Alizadeh K, Alizadeh K, Fazel F, Kakish JE, Karimi N, Knapp JP, Mehrani Y, Minott JA, Morovati S, Rghei A, Stegelmeier AA, Vanderkamp S, Karimi K, Bridle BW. Review of Influenza Virus Vaccines: The Qualitative Nature of Immune Responses to Infection and Vaccination Is a Critical Consideration. Vaccines (Basel) 2021 Sep 1;9(9).
            doi: 10.3390/vaccines9090979pubmed: 34579216google scholar: lookup
          6. Oladunni FS, Oseni SO, Martinez-Sobrido L, Chambers TM. Equine Influenza Virus and Vaccines. Viruses 2021 Aug 20;13(8).
            doi: 10.3390/v13081657pubmed: 34452521google scholar: lookup
          7. Li Y, Liu D, Wang Y, Su W, Liu G, Dong W. The Importance of Glycans of Viral and Host Proteins in Enveloped Virus Infection. Front Immunol 2021;12:638573.
            doi: 10.3389/fimmu.2021.638573pubmed: 33995356google scholar: lookup
          8. Thompson AJ, Paulson JC. Adaptation of influenza viruses to human airway receptors. J Biol Chem 2021 Jan-Jun;296:100017.
            doi: 10.1074/jbc.REV120.013309pubmed: 33144323google scholar: lookup
          9. Eggink D, Spronken M, van der Woude R, Buzink J, Broszeit F, McBride R, Pawestri HA, Setiawaty V, Paulson JC, Boons GJ, Fouchier RAM, Russell CA, de Jong MD, de Vries RP. Phenotypic Effects of Substitutions within the Receptor Binding Site of Highly Pathogenic Avian Influenza H5N1 Virus Observed during Human Infection. J Virol 2020 Jun 16;94(13).
            doi: 10.1128/JVI.00195-20pubmed: 32321815google scholar: lookup
          10. Dai X, Zhang X, Ostrikov K, Abrahamyan L. Host receptors: the key to establishing cells with broad viral tropism for vaccine production. Crit Rev Microbiol 2020 Mar;46(2):147-168.
            doi: 10.1080/1040841X.2020.1735992pubmed: 32202955google scholar: lookup
          11. de Vries E, Du W, Guo H, de Haan CAM. Influenza A Virus Hemagglutinin-Neuraminidase-Receptor Balance: Preserving Virus Motility. Trends Microbiol 2020 Jan;28(1):57-67.
            doi: 10.1016/j.tim.2019.08.010pubmed: 31629602google scholar: lookup
          12. Wasik BR, Voorhees IEH, Barnard KN, Alford-Lawrence BK, Weichert WS, Hood G, Nogales A, Martínez-Sobrido L, Holmes EC, Parrish CR. Influenza Viruses in Mice: Deep Sequencing Analysis of Serial Passage and Effects of Sialic Acid Structural Variation. J Virol 2019 Dec 1;93(23).
            doi: 10.1128/JVI.01039-19pubmed: 31511393google scholar: lookup
          13. Zhao P, Sun L, Xiong J, Wang C, Chen L, Yang P, Yu H, Yan Q, Cheng Y, Jiang L, Chen Y, Zhao G, Jiang Q, Xiong C. Semiaquatic mammals might be intermediate hosts to spread avian influenza viruses from avian to human. Sci Rep 2019 Aug 12;9(1):11641.
            doi: 10.1038/s41598-019-48255-5pubmed: 31406229google scholar: lookup
          14. Guan M, Hall JS, Zhang X, Dusek RJ, Olivier AK, Liu L, Li L, Krauss S, Danner A, Li T, Rutvisuttinunt W, Lin X, Hallgrimsson GT, Ragnarsdottir SB, Vignisson SR, TeSlaa J, Nashold SW, Jarman R, Wan XF. Aerosol Transmission of Gull-Origin Iceland Subtype H10N7 Influenza A Virus in Ferrets. J Virol 2019 Jul 1;93(13).
            doi: 10.1128/JVI.00282-19pubmed: 30996092google scholar: lookup
          15. Neumann G, Kawaoka Y. Predicting the Next Influenza Pandemics. J Infect Dis 2019 Apr 8;219(Suppl_1):S14-S20.
            doi: 10.1093/infdis/jiz040pubmed: 30715371google scholar: lookup
          16. Obadan AO, Santos J, Ferreri L, Thompson AJ, Carnaccini S, Geiger G, Gonzalez Reiche AS, Rajão DS, Paulson JC, Perez DR. Flexibility In Vitro of Amino Acid 226 in the Receptor-Binding Site of an H9 Subtype Influenza A Virus and Its Effect In Vivo on Virus Replication, Tropism, and Transmission. J Virol 2019 Mar 15;93(6).
            doi: 10.1128/JVI.02011-18pubmed: 30567980google scholar: lookup
          17. Horman WSJ, Nguyen THO, Kedzierska K, Bean AGD, Layton DS. The Drivers of Pathology in Zoonotic Avian Influenza: The Interplay Between Host and Pathogen. Front Immunol 2018;9:1812.
            doi: 10.3389/fimmu.2018.01812pubmed: 30135686google scholar: lookup
          18. Joseph U, Vijaykrishna D, Smith GJD, Su YCF. Adaptive evolution during the establishment of European avian-like H1N1 influenza A virus in swine. Evol Appl 2018 Apr;11(4):534-546.
            doi: 10.1111/eva.12536pubmed: 29636804google scholar: lookup
          19. Pickens JA, Tripp RA. Verdinexor Targeting of CRM1 is a Promising Therapeutic Approach against RSV and Influenza Viruses. Viruses 2018 Jan 21;10(1).
            doi: 10.3390/v10010048pubmed: 29361733google scholar: lookup
          20. Wasik BR, Barnard KN, Ossiboff RJ, Khedri Z, Feng KH, Yu H, Chen X, Perez DR, Varki A, Parrish CR. Distribution of O-Acetylated Sialic Acids among Target Host Tissues for Influenza Virus. mSphere 2017 Sep-Oct;2(5).
            doi: 10.1128/mSphere.00379-16pubmed: 28904995google scholar: lookup
          21. Tzarum N, McBride R, Nycholat CM, Peng W, Paulson JC, Wilson IA. Unique Structural Features of Influenza Virus H15 Hemagglutinin. J Virol 2017 Jun 15;91(12).
            doi: 10.1128/JVI.00046-17pubmed: 28404848google scholar: lookup
          22. Sun H, Kaplan BS, Guan M, Zhang G, Ye J, Long LP, Blackmon S, Yang CK, Chiang MJ, Xie H, Zhao N, Cooley J, Smith DF, Liao M, Cardona C, Li L, Wang GP, Webby R, Wan XF. Pathogenicity and transmission of a swine influenza A(H6N6) virus. Emerg Microbes Infect 2017 Apr 12;6(4):e17.
            doi: 10.1038/emi.2017.3pubmed: 28400591google scholar: lookup
          23. Mao H, Liu Y, Sia SF, Peiris JSM, Lau YL, Tu W. Avian influenza virus directly infects human natural killer cells and inhibits cell activity. Virol Sin 2017 Apr;32(2):122-129.
            doi: 10.1007/s12250-016-3918-ypubmed: 28255852google scholar: lookup
          24. Kwon SJ, Na DH, Kwak JH, Douaisi M, Zhang F, Park EJ, Park JH, Youn H, Song CS, Kane RS, Dordick JS, Lee KB, Linhardt RJ. Nanostructured glycan architecture is important in the inhibition of influenza A virus infection. Nat Nanotechnol 2017 Jan;12(1):48-54.
            doi: 10.1038/nnano.2016.181pubmed: 27775724google scholar: lookup
          25. Lee DW, Hsu HL, Bacon KB, Daniel S. Image Restoration and Analysis of Influenza Virions Binding to Membrane Receptors Reveal Adhesion-Strengthening Kinetics. PLoS One 2016;11(10):e0163437.
            doi: 10.1371/journal.pone.0163437pubmed: 27695072google scholar: lookup
          26. Ranadheera C, Hagan MW, Leung A, Collignon B, Cutts T, Theriault S, Embury-Hyatt C, Kobasa D. Reduction of Neuraminidase Activity Exacerbates Disease in 2009 Pandemic Influenza Virus-Infected Mice. J Virol 2016 Nov 1;90(21):9931-9941.
            doi: 10.1128/JVI.01188-16pubmed: 27558428google scholar: lookup
          27. Wasik BR, Barnard KN, Parrish CR. Effects of Sialic Acid Modifications on Virus Binding and Infection. Trends Microbiol 2016 Dec;24(12):991-1001.
            doi: 10.1016/j.tim.2016.07.005pubmed: 27491885google scholar: lookup
          28. Di Lella S, Herrmann A, Mair CM. Modulation of the pH Stability of Influenza Virus Hemagglutinin: A Host Cell Adaptation Strategy. Biophys J 2016 Jun 7;110(11):2293-2301.
            doi: 10.1016/j.bpj.2016.04.035pubmed: 27276248google scholar: lookup
          29. Nogales A, Baker SF, Domm W, Martínez-Sobrido L. Development and applications of single-cycle infectious influenza A virus (sciIAV). Virus Res 2016 May 2;216:26-40.
            doi: 10.1016/j.virusres.2015.07.013pubmed: 26220478google scholar: lookup
          30. Neumann G, Kawaoka Y. Transmission of influenza A viruses. Virology 2015 May;479-480:234-46.
            doi: 10.1016/j.virol.2015.03.009pubmed: 25812763google scholar: lookup
          31. Stencel-Baerenwald JE, Reiss K, Reiter DM, Stehle T, Dermody TS. The sweet spot: defining virus-sialic acid interactions. Nat Rev Microbiol 2014 Nov;12(11):739-49.
            doi: 10.1038/nrmicro3346pubmed: 25263223google scholar: lookup
          32. Van Breedam W, Pöhlmann S, Favoreel HW, de Groot RJ, Nauwynck HJ. Bitter-sweet symphony: glycan-lectin interactions in virus biology. FEMS Microbiol Rev 2014 Jul;38(4):598-632.
            doi: 10.1111/1574-6976.12052pubmed: 24188132google scholar: lookup
          33. Matsuoka Y, Matsumae H, Katoh M, Eisfeld AJ, Neumann G, Hase T, Ghosh S, Shoemaker JE, Lopes TJ, Watanabe T, Watanabe S, Fukuyama S, Kitano H, Kawaoka Y. A comprehensive map of the influenza A virus replication cycle. BMC Syst Biol 2013 Oct 2;7:97.
            doi: 10.1186/1752-0509-7-97pubmed: 24088197google scholar: lookup
          34. Yang G, Li S, Blackmon S, Ye J, Bradley KC, Cooley J, Smith D, Hanson L, Cardona C, Steinhauer DA, Webby R, Liao M, Wan XF. Mutation tryptophan to leucine at position 222 of haemagglutinin could facilitate H3N2 influenza A virus infection in dogs. J Gen Virol 2013 Dec;94(Pt 12):2599-2608.
            doi: 10.1099/vir.0.054692-0pubmed: 23994833google scholar: lookup
          35. Lu X, Shi Y, Zhang W, Zhang Y, Qi J, Gao GF. Structure and receptor-binding properties of an airborne transmissible avian influenza A virus hemagglutinin H5 (VN1203mut). Protein Cell 2013 Jul;4(7):502-11.
            doi: 10.1007/s13238-013-3906-zpubmed: 23794001google scholar: lookup
          36. Lu X, Qi J, Shi Y, Wang M, Smith DF, Heimburg-Molinaro J, Zhang Y, Paulson JC, Xiao H, Gao GF. Structure and receptor binding specificity of hemagglutinin H13 from avian influenza A virus H13N6. J Virol 2013 Aug;87(16):9077-85.
            doi: 10.1128/JVI.00235-13pubmed: 23760233google scholar: lookup
          37. Paulson JC, de Vries RP. H5N1 receptor specificity as a factor in pandemic risk. Virus Res 2013 Dec 5;178(1):99-113.
            doi: 10.1016/j.virusres.2013.02.015pubmed: 23619279google scholar: lookup
          38. Nicholls JM, Moss RB, Haslam SM. The use of sialidase therapy for respiratory viral infections. Antiviral Res 2013 Jun;98(3):401-9.
            doi: 10.1016/j.antiviral.2013.04.012pubmed: 23602850google scholar: lookup
          39. Rumschlag-Booms E, Rong L. Influenza a virus entry: implications in virulence and future therapeutics. Adv Virol 2013;2013:121924.
            doi: 10.1155/2013/121924pubmed: 23365574google scholar: lookup
          40. Uraki R, Kiso M, Shinya K, Goto H, Takano R, Iwatsuki-Horimoto K, Takahashi K, Daniels RS, Hungnes O, Watanabe T, Kawaoka Y. Virulence determinants of pandemic A(H1N1)2009 influenza virus in a mouse model. J Virol 2013 Feb;87(4):2226-33.
            doi: 10.1128/JVI.01565-12pubmed: 23221570google scholar: lookup
          41. Shirato H. Norovirus recognition sites on histo-blood group antigens. Front Microbiol 2012;3:177.
            doi: 10.3389/fmicb.2012.00177pubmed: 22783230google scholar: lookup
          42. Sriwilaijaroen N, Suzuki Y. Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad Ser B Phys Biol Sci 2012;88(6):226-49.
            doi: 10.2183/pjab.88.226pubmed: 22728439google scholar: lookup
          43. Watanabe T, Shinya K, Watanabe S, Imai M, Hatta M, Li C, Wolter BF, Neumann G, Hanson A, Ozawa M, Yamada S, Imai H, Sakabe S, Takano R, Iwatsuki-Horimoto K, Kiso M, Ito M, Fukuyama S, Kawakami E, Gorai T, Simmons HA, Schenkman D, Brunner K, Capuano SV 3rd, Weinfurter JT, Nishio W, Maniwa Y, Igarashi T, Makino A, Travanty EA, Wang J, Kilander A, Dudman SG, Suresh M, Mason RJ, Hungnes O, Friedrich TC, Kawaoka Y. Avian-type receptor-binding ability can increase influenza virus pathogenicity in macaques. J Virol 2011 Dec;85(24):13195-203.
            doi: 10.1128/JVI.00859-11pubmed: 21937653google scholar: lookup
          44. Sakabe S, Ozawa M, Takano R, Iwastuki-Horimoto K, Kawaoka Y. Mutations in PA, NP, and HA of a pandemic (H1N1) 2009 influenza virus contribute to its adaptation to mice. Virus Res 2011 Jun;158(1-2):124-9.
            doi: 10.1016/j.virusres.2011.03.022pubmed: 21458512google scholar: lookup
          45. Yamanaka T, Tsujimura K, Kondo T, Matsumura T, Ishida H, Kiso M, Hidari KI, Suzuki T. Infectivity and pathogenicity of canine H3N8 influenza A virus in horses. Influenza Other Respir Viruses 2010 Nov;4(6):345-51.
            doi: 10.1111/j.1750-2659.2010.00157.xpubmed: 20958928google scholar: lookup
          46. Chen CH, Zhang XQ, Lo CW, Liu PF, Liu YT, Gallo RL, Hsieh MF, Schooley RT, Huang CM. The essentiality of alpha-2-macroglobulin in human salivary innate immunity against new H1N1 swine origin influenza A virus. Proteomics 2010 Jun;10(12):2396-401.
            doi: 10.1002/pmic.200900775pubmed: 20391540google scholar: lookup
          47. Kato T, Kawaguchi A, Nagata K, Hatanaka K. Development of tetraphenylethylene-based fluorescent oligosaccharide probes for detection of influenza virus. Biochem Biophys Res Commun 2010 Mar 26;394(1):200-4.
            doi: 10.1016/j.bbrc.2010.02.155pubmed: 20188703google scholar: lookup
          48. Zhang Y, Lin X, Wang G, Zhou J, Lu J, Zhao H, Zhang F, Wu J, Xu C, Du N, Li Z, Zhang Y, Wang X, Bi S, Shu Y, Zhou H, Tan W, Wu X, Chen Z, Wang Y. Neuraminidase and hemagglutinin matching patterns of a highly pathogenic avian and two pandemic H1N1 influenza A viruses. PLoS One 2010 Feb 11;5(2):e9167.
            doi: 10.1371/journal.pone.0009167pubmed: 20161801google scholar: lookup
          49. Li C, Hatta M, Watanabe S, Neumann G, Kawaoka Y. Compatibility among polymerase subunit proteins is a restricting factor in reassortment between equine H7N7 and human H3N2 influenza viruses. J Virol 2008 Dec;82(23):11880-8.
            doi: 10.1128/JVI.01445-08pubmed: 18815312google scholar: lookup
          50. Shirato H, Ogawa S, Ito H, Sato T, Kameyama A, Narimatsu H, Xiaofan Z, Miyamura T, Wakita T, Ishii K, Takeda N. Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding. J Virol 2008 Nov;82(21):10756-67.
            doi: 10.1128/JVI.00802-08pubmed: 18701592google scholar: lookup
          51. Fujisawa H. Neutrophils play an essential role in cooperation with antibody in both protection against and recovery from pulmonary infection with influenza virus in mice. J Virol 2008 Mar;82(6):2772-83.
            doi: 10.1128/JVI.01210-07pubmed: 18184718google scholar: lookup
          52. Hatta M, Hatta Y, Kim JH, Watanabe S, Shinya K, Nguyen T, Lien PS, Le QM, Kawaoka Y. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog 2007 Oct 5;3(10):1374-9.
            doi: 10.1371/journal.ppat.0030133pubmed: 17922570google scholar: lookup
          53. Perk S, Banet-Noach C, Golender N, Simanov L, Rozenblut E, Nagar S, Pokamunski S, Pirak M, Tendler Y, García M, Panshin A. Molecular characterization of the glycoprotein genes of H5N1 influenza A viruses isolated in Israel and the Gaza Strip during 2006 outbreaks. Virus Genes 2007 Dec;35(3):497-502.
            doi: 10.1007/s11262-007-0120-1pubmed: 17616798google scholar: lookup
          54. Lekcharoensuk P, Lager KM, Vemulapalli R, Woodruff M, Vincent AL, Richt JA. Novel swine influenza virus subtype H3N1, United States. Emerg Infect Dis 2006 May;12(5):787-94.
            doi: 10.3201/eid1205.051060pubmed: 16704839google scholar: lookup
          55. Kogure T, Suzuki T, Takahashi T, Miyamoto D, Hidari KI, Guo CT, Ito T, Kawaoka Y, Suzuki Y. Human trachea primary epithelial cells express both sialyl(alpha2-3)Gal receptor for human parainfluenza virus type 1 and avian influenza viruses, and sialyl(alpha2-6)Gal receptor for human influenza viruses. Glycoconj J 2006 Feb;23(1-2):101-6.
            doi: 10.1007/s10719-006-5442-zpubmed: 16575527google scholar: lookup
          56. Shinya K, Hatta M, Yamada S, Takada A, Watanabe S, Halfmann P, Horimoto T, Neumann G, Kim JH, Lim W, Guan Y, Peiris M, Kiso M, Suzuki T, Suzuki Y, Kawaoka Y. Characterization of a human H5N1 influenza A virus isolated in 2003. J Virol 2005 Aug;79(15):9926-32.
            doi: 10.1128/JVI.79.15.9926-9932.2005pubmed: 16014953google scholar: lookup
          57. Baranowski E, Ruiz-Jarabo CM, Pariente N, Verdaguer N, Domingo E. Evolution of cell recognition by viruses: a source of biological novelty with medical implications. Adv Virus Res 2003;62:19-111.
            doi: 10.1016/s0065-3527(03)62002-6pubmed: 14719364google scholar: lookup
          58. Slepushkin VA, Staber PD, Wang G, McCray PB Jr, Davidson BL. Infection of human airway epithelia with H1N1, H2N2, and H3N2 influenza A virus strains. Mol Ther 2001 Mar;3(3):395-402.
            doi: 10.1006/mthe.2001.0277pubmed: 11273782google scholar: lookup
          59. Hughes MT, McGregor M, Suzuki T, Suzuki Y, Kawaoka Y. Adaptation of influenza A viruses to cells expressing low levels of sialic acid leads to loss of neuraminidase activity. J Virol 2001 Apr;75(8):3766-70.
            doi: 10.1128/JVI.75.8.3766-3770.2001pubmed: 11264365google scholar: lookup
          60. Horimoto T, Kawaoka Y. Pandemic threat posed by avian influenza A viruses. Clin Microbiol Rev 2001 Jan;14(1):129-49.
            doi: 10.1128/CMR.14.1.129-149.2001pubmed: 11148006google scholar: lookup
          61. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 2000 Sep;74(18):8502-12.
            doi: 10.1128/jvi.74.18.8502-8512.2000pubmed: 10954551google scholar: lookup
          62. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 1998 Sep;72(9):7367-73.
            doi: 10.1128/JVI.72.9.7367-7373.1998pubmed: 9696833google scholar: lookup
          63. Matrosovich M, Gao P, Kawaoka Y. Molecular mechanisms of serum resistance of human influenza H3N2 virus and their involvement in virus adaptation in a new host. J Virol 1998 Aug;72(8):6373-80.
            doi: 10.1128/JVI.72.8.6373-6380.1998pubmed: 9658077google scholar: lookup
          64. Liang R, Loebach J, Horan N, Ge M, Thompson C, Yan L, Kahne D. Polyvalent binding to carbohydrates immobilized on an insoluble resin. Proc Natl Acad Sci U S A 1997 Sep 30;94(20):10554-9.
            doi: 10.1073/pnas.94.20.10554pubmed: 9380673google scholar: lookup
          65. Kelm S, Schauer R. Sialic acids in molecular and cellular interactions. Int Rev Cytol 1997;175:137-240.
            doi: 10.1016/s0074-7696(08)62127-0pubmed: 9203358google scholar: lookup
          66. Günther I, Glatthaar B, Döller G, Garten W. A H1 hemagglutinin of a human influenza A virus with a carbohydrate-modulated receptor binding site and an unusual cleavage site. Virus Res 1993 Feb;27(2):147-60.
            doi: 10.1016/0168-1702(93)90078-2pubmed: 8460527google scholar: lookup
          67. Moscona A, Peluso RW. Relative affinity of the human parainfluenza virus type 3 hemagglutinin-neuraminidase for sialic acid correlates with virus-induced fusion activity. J Virol 1993 Nov;67(11):6463-8.
            doi: 10.1128/JVI.67.11.6463-6468.1993pubmed: 8411349google scholar: lookup
          68. Gentsch JR, Pacitti AF. Effect of neuraminidase treatment of cells and effect of soluble glycoproteins on type 3 reovirus attachment to murine L cells. J Virol 1985 Nov;56(2):356-64.
            doi: 10.1128/JVI.56.2.356-364.1985pubmed: 4057353google scholar: lookup
          69. Anders EM, Scalzo AA, Rogers GN, White DO. Relationship between mitogenic activity of influenza viruses and the receptor-binding specificity of their hemagglutinin molecules. J Virol 1986 Nov;60(2):476-82.
            doi: 10.1128/JVI.60.2.476-482.1986pubmed: 3490581google scholar: lookup
          70. Pyhälä R, Pyhälä L, Valle M, Aho K. Egg-grown and tissue-culture-grown variants of influenza A (H3N2) virus with special attention to their use as antigens in seroepidemiology. Epidemiol Infect 1987 Dec;99(3):745-53.
            doi: 10.1017/s0950268800066607pubmed: 3428377google scholar: lookup
          71. Klenk HD, Rott R. The molecular biology of influenza virus pathogenicity. Adv Virus Res 1988;34:247-81.
            doi: 10.1016/s0065-3527(08)60520-5pubmed: 3046255google scholar: lookup
          72. Patterson S, Oxford JS. Analysis of antigenic determinants on internal and external proteins of influenza virus and identification of antigenic subpopulations of virions in recent field isolates using monoclonal antibodies and immunogold labelling. Arch Virol 1986;88(3-4):189-202.
            doi: 10.1007/BF01310874pubmed: 2423056google scholar: lookup
          73. Yewdell JW, Caton AJ, Gerhard W. Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. J Virol 1986 Feb;57(2):623-8.
            doi: 10.1128/JVI.57.2.623-628.1986pubmed: 2418215google scholar: lookup
          74. Kilpatrick DR, Lipton HL. Predominant binding of Theiler's viruses to a 34-kilodalton receptor protein on susceptible cell lines. J Virol 1991 Oct;65(10):5244-9.
            doi: 10.1128/JVI.65.10.5244-5249.1991pubmed: 1895381google scholar: lookup
          75. Freund R, Garcea RL, Sahli R, Benjamin TL. A single-amino-acid substitution in polyomavirus VP1 correlates with plaque size and hemagglutination behavior. J Virol 1991 Jan;65(1):350-5.
            doi: 10.1128/JVI.65.1.350-355.1991pubmed: 1845896google scholar: lookup
          76. Ryan-Poirier KA, Kawaoka Y. Distinct glycoprotein inhibitors of influenza A virus in different animal sera. J Virol 1991 Jan;65(1):389-95.
            doi: 10.1128/JVI.65.1.389-395.1991pubmed: 1702161google scholar: lookup
          77. Wu R, Plopper CG, Cheng PW. Mucin-like glycoprotein secreted by cultured hamster tracheal epithelial cells. Biochemical and immunological characterization. Biochem J 1991 Aug 1;277 ( Pt 3)(Pt 3):713-8.
            doi: 10.1042/bj2770713pubmed: 1651700google scholar: lookup
          78. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992 Mar;56(1):152-79.
            doi: 10.1128/mr.56.1.152-179.1992pubmed: 1579108google scholar: lookup
          79. Ito T. Pathogenicity and host range of avian influenza viruses: molecular determinants and virological perspectives. J Vet Med Sci 2025 Nov 1;87(11):1259-1265.
            doi: 10.1292/jvms.25-0313pubmed: 40958564google scholar: lookup
          80. Chen Y, Dean KJ, Fenske GJ, Murphy SI, Gavelek A, Pouillot R, Van Doren JM, Dennis S. Rapid risk assessment to address emerging concerns of HPAI in raw and pasteurized milk. PLoS One 2025;20(6):e0322948.
            doi: 10.1371/journal.pone.0322948pubmed: 40465792google scholar: lookup
          81. Chang Y, Shan Z, Shi W, Li Q, Wang Y, Wang B, Wang G, Chen H, Jiang L, Li C. KRT6A Restricts Influenza A Virus Replication by Inhibiting the Nuclear Import and Assembly of Viral Ribonucleoprotein Complex. Viruses 2025 May 4;17(5).
            doi: 10.3390/v17050671pubmed: 40431683google scholar: lookup
          82. Anderson M, Lopez J, Wyr M, Ramirez PW. Defining diverse spike-receptor interactions involved in SARS-CoV-2 entry: Mechanisms and therapeutic opportunities. Virology 2025 Jun;607:110507.
            doi: 10.1016/j.virol.2025.110507pubmed: 40157321google scholar: lookup
          83. Wang G, Jiang L, Yan Y, Kong F, Li Q, Zhang J, Hou S, Wang B, Wang X, Kong H, Deng G, Shi J, Tian G, Zeng X, Chen H, Li C. Cellular SLC35B4 promotes internalization during influenza A virus entry. mBio 2025 May 14;16(5):e0019425.
            doi: 10.1128/mbio.00194-25pubmed: 40130891google scholar: lookup
          84. Azeem S, Yoon KJ. Diagnostic Assays for Avian Influenza Virus Surveillance and Monitoring in Poultry. Viruses 2025 Feb 6;17(2).
            doi: 10.3390/v17020228pubmed: 40006983google scholar: lookup
          85. Lotke R, Petersen M, Sauter D. Restriction of Viral Glycoprotein Maturation by Cellular Protease Inhibitors. Viruses 2024 Feb 22;16(3).
            doi: 10.3390/v16030332pubmed: 38543698google scholar: lookup
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