Recent H3N2 Influenza Virus Clinical Isolates Rapidly Acquire Hemagglutinin or Neuraminidase Mutations when Propagated for Antigenic Analyses

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2014 Jul 4

PMID 24991002

Citations 32

Authors

Benjamin S Chambers

Yang Li

Richard L Hodinka

Scott E Hensley

Affiliations

Soon will be listed here.

Abstract

Prior to serological testing, influenza viruses are typically propagated in eggs or cell culture. Recent human H3N2 strains bind to cells with low avidity. Here, we isolated nine primary H3N2 viral isolates from respiratory secretions of children. Upon propagation in vitro, five of these isolates acquired hemagglutinin or neuraminidase mutations that increased virus binding to cell surfaces. These mutations can potentially confound serological assays commonly used to identify antigenically novel influenza viruses.

Citing Articles

Phylogenomic Analyses of the Hemagglutinin-Neuraminidase () Gene in Human Parainfluenza Virus Type 4 Isolates in Japan.

Otani K, Kimura R, Nagasawa N, Hayashi Y, Ohmiya S, Watanabe O Microorganisms. 2025; 13(2).

PMID: 40005750 PMC: 11857914. DOI: 10.3390/microorganisms13020384.

Characteristics and evolution of hemagglutinin and neuraminidase genes of Influenza A(H3N2) viruses in Thailand during 2015 to 2018.

Anoma S, Bhattarakosol P, Kowitdamrong E PeerJ. 2024; 12:e17523.

PMID: 38846750 PMC: 11155671. DOI: 10.7717/peerj.17523.

Glyco-engineered MDCK cells display preferred receptors of H3N2 influenza absent in eggs used for vaccines.

Kikuchi C, Antonopoulos A, Wang S, Maemura T, Karamanska R, Lee C Nat Commun. 2023; 14(1):6178.

PMID: 37794004 PMC: 10551000. DOI: 10.1038/s41467-023-41908-0.

Contemporary human H3N2 influenza A viruses require a low threshold of suitable glycan receptors for efficient infection.

Spruit C, Sweet I, Maliepaard J, Bestebroer T, Lexmond P, Qiu B Glycobiology. 2023; 33(10):784-800.

PMID: 37471650 PMC: 10629718. DOI: 10.1093/glycob/cwad060.

On the Evolutionary Trajectory of SARS-CoV-2: Host Immunity as a Driver of Adaptation in RNA Viruses.

Warger J, Gaudieri S Viruses. 2023; 15(1).

PMID: 36680110 PMC: 9866609. DOI: 10.3390/v15010070.

References

Klimov A, Balish A, Veguilla V, Sun H, Schiffer J, Lu X . Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol Biol. 2012; 865:25-51. DOI: 10.1007/978-1-61779-621-0_3. View

Smith D, Lapedes A, de Jong J, Bestebroer T, Rimmelzwaan G, Osterhaus A . Mapping the antigenic and genetic evolution of influenza virus. Science. 2004; 305(5682):371-6. DOI: 10.1126/science.1097211. View

Underwood P, Skehel J, Wiley D . Receptor-binding characteristics of monoclonal antibody-selected antigenic variants of influenza virus. J Virol. 1987; 61(1):206-8. PMC: 255240. DOI: 10.1128/JVI.61.1.206-208.1987. View

Nicholls J, Chan R, Russell R, Air G, Peiris J . Evolving complexities of influenza virus and its receptors. Trends Microbiol. 2008; 16(4):149-57. DOI: 10.1016/j.tim.2008.01.008. View

Hensley S, Das S, Bailey A, Schmidt L, Hickman H, Jayaraman A . Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science. 2009; 326(5953):734-6. PMC: 2784927. DOI: 10.1126/science.1178258. View

Lee H, Tang J, Kong D, Loh T, Chiang D, Lam T . Comparison of mutation patterns in full-genome A/H3N2 influenza sequences obtained directly from clinical samples and the same samples after a single MDCK passage. PLoS One. 2013; 8(11):e79252. PMC: 3815150. DOI: 10.1371/journal.pone.0079252. View

Barr I, McCauley J, Cox N, Daniels R, Engelhardt O, Fukuda K . Epidemiological, antigenic and genetic characteristics of seasonal influenza A(H1N1), A(H3N2) and B influenza viruses: basis for the WHO recommendation on the composition of influenza vaccines for use in the 2009-2010 northern hemisphere season. Vaccine. 2009; 28(5):1156-67. DOI: 10.1016/j.vaccine.2009.11.043. View

Zhu X, McBride R, Nycholat C, Yu W, Paulson J, Wilson I . Influenza virus neuraminidases with reduced enzymatic activity that avidly bind sialic Acid receptors. J Virol. 2012; 86(24):13371-83. PMC: 3503043. DOI: 10.1128/JVI.01426-12. View

Oh D, Barr I, Mosse J, Laurie K . MDCK-SIAT1 cells show improved isolation rates for recent human influenza viruses compared to conventional MDCK cells. J Clin Microbiol. 2008; 46(7):2189-94. PMC: 2446904. DOI: 10.1128/JCM.00398-08. View

10.

Yewdell J, Caton A, GERHARD W . Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. J Virol. 1986; 57(2):623-8. PMC: 252777. DOI: 10.1128/JVI.57.2.623-628.1986. View

11.

HIRST G . THE QUANTITATIVE DETERMINATION OF INFLUENZA VIRUS AND ANTIBODIES BY MEANS OF RED CELL AGGLUTINATION. J Exp Med. 2009; 75(1):49-64. PMC: 2135212. DOI: 10.1084/jem.75.1.49. View

12.

Hoffmann E, Neumann G, Kawaoka Y, HOBOM G, Webster R . A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A. 2000; 97(11):6108-13. PMC: 18566. DOI: 10.1073/pnas.100133697. View

13.

Yewdell J . Viva la revolución: rethinking influenza a virus antigenic drift. Curr Opin Virol. 2011; 1(3):177-83. PMC: 3199585. DOI: 10.1016/j.coviro.2011.05.005. View

14.

Lin Y, Xiong X, Wharton S, Martin S, Coombs P, Vachieri S . Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc Natl Acad Sci U S A. 2012; 109(52):21474-9. PMC: 3535595. DOI: 10.1073/pnas.1218841110. View

15.

Krauss S, Walker D, Webster R . Influenza virus isolation. Methods Mol Biol. 2012; 865:11-24. DOI: 10.1007/978-1-61779-621-0_2. View

16.

Li Y, Bostick D, Sullivan C, Myers J, Griesemer S, StGeorge K . Single hemagglutinin mutations that alter both antigenicity and receptor binding avidity influence influenza virus antigenic clustering. J Virol. 2013; 87(17):9904-10. PMC: 3754131. DOI: 10.1128/JVI.01023-13. View

17.

Bedford T, Suchard M, Lemey P, Dudas G, Gregory V, Hay A . Integrating influenza antigenic dynamics with molecular evolution. Elife. 2014; 3:e01914. PMC: 3909918. DOI: 10.7554/eLife.01914. View

18.

Stohr K, Bucher D, Colgate T, Wood J . Influenza virus surveillance, vaccine strain selection, and manufacture. Methods Mol Biol. 2012; 865:147-62. DOI: 10.1007/978-1-61779-621-0_9. View

19.

Hooper K, Bloom J . A mutant influenza virus that uses an N1 neuraminidase as the receptor-binding protein. J Virol. 2013; 87(23):12531-40. PMC: 3838107. DOI: 10.1128/JVI.01889-13. View

20.

Skowronski D, Janjua N, De Serres G, Sabaiduc S, Eshaghi A, Dickinson J . Low 2012-13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLoS One. 2014; 9(3):e92153. PMC: 3965421. DOI: 10.1371/journal.pone.0092153. View