Characterization of Influenza Virus Binding to Receptors on Isolated Cell Membranes

Overview

Journal Methods Mol Biol

Specialty Molecular Biology

Date 2022 Sep 29

PMID 36175633

Authors

Mikhail N Matrosovich

Alexandra S Gambaryan

Affiliations

Soon will be listed here.

Abstract

An interplay between receptor-binding properties of influenza viruses (IVs) and spectrum of sialic acid-containing receptors on target cells in birds and mammals determine viral host range, tissue tropism, and pathogenicity. Here, we describe method that allows to characterize binding of IVs to biologically relevant cellular receptors using a conventional solid-phase enzyme-linked assay. In this method, we isolate plasma membranes from respiratory and intestinal epithelial cells of animal origin (Subheading 3.2). We adsorb the membranes in the wells of 96-well ELISA plates, incubate the membrane-coated wells with serially diluted IVs, and determine amounts of IVs attached to the membranes using viral ability to bind peroxidase-labeled sialoglycoprotein fetuin. Based on the concentration dependence of IV binding to the membrane, we estimate binding avidity and number of binding sites. We describe two variants of the assay in Subheadings 3.6 and 3.7 and provide examples.

References

Overeem N, van der Vries E, Huskens J . A Dynamic, Supramolecular View on the Multivalent Interaction between Influenza Virus and Host Cell. Small. 2021; 17(13):e2007214. DOI: 10.1002/smll.202007214. View

Ji Y, White Y, Hadden J, Grant O, Woods R . New insights into influenza A specificity: an evolution of paradigms. Curr Opin Struct Biol. 2017; 44:219-231. PMC: 5715462. DOI: 10.1016/j.sbi.2017.06.001. View

Kuchipudi S, Nelli R, Gontu A, Satyakumar R, Surendran Nair M, Subbiah M . Sialic Acid Receptors: The Key to Solving the Enigma of Zoonotic Virus Spillover. Viruses. 2021; 13(2). PMC: 7915228. DOI: 10.3390/v13020262. View

van Riel D, Munster V, de Wit E, Rimmelzwaan G, Fouchier R, Osterhaus A . Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol. 2007; 171(4):1215-23. PMC: 1988871. DOI: 10.2353/ajpath.2007.070248. View

Verhagen J, Eriksson P, Leijten L, Blixt O, Olsen B, Waldenstrom J . Host Range of Influenza A Virus H1 to H16 in Eurasian Ducks Based on Tissue and Receptor Binding Studies. J Virol. 2020; 95(6). PMC: 8094940. DOI: 10.1128/JVI.01873-20. View

Eriksson P, Lindskog C, Lorente-Leal V, Waldenstrom J, Gonzalez-Acuna D, Jarhult J . Attachment Patterns of Human and Avian Influenza Viruses to Trachea and Colon of 26 Bird Species - Support for the Community Concept. Front Microbiol. 2019; 10:815. PMC: 6482220. DOI: 10.3389/fmicb.2019.00815. View

Detmer S, Gramer M, Goyal S, Torremorell M . In vitro characterization of influenza A virus attachment in the upper and lower respiratory tracts of pigs. Vet Pathol. 2012; 50(4):648-58. DOI: 10.1177/0300985812467469. View

Wang B, Liu B, Chen L, Zhang J, He H, Zhang H . Qualitative and quantitative analyses of influenza virus receptors in trachea and lung tissues of humans, mice, chickens and ducks. Sci China Life Sci. 2012; 55(7):612-7. DOI: 10.1007/s11427-012-4341-8. View

Ambepitiya Wickramasinghe I, de Vries R, Eggert A, Wandee N, de Haan C, Grone A . Host tissue and glycan binding specificities of avian viral attachment proteins using novel avian tissue microarrays. PLoS One. 2015; 10(6):e0128893. PMC: 4452732. DOI: 10.1371/journal.pone.0128893. View

10.

Matrosovich M, Matrosovich T, Carr J, Roberts N, Klenk H . Overexpression of the alpha-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J Virol. 2003; 77(15):8418-25. PMC: 165236. DOI: 10.1128/jvi.77.15.8418-8425.2003. View

11.

Govorkova E, Matrosovich M, Tuzikov A, Bovin N, Gerdil C, Fanget B . Selection of receptor-binding variants of human influenza A and B viruses in baby hamster kidney cells. Virology. 1999; 262(1):31-8. DOI: 10.1006/viro.1999.9892. View

12.

Gubareva L, Matrosovich M, Brenner M, Bethell R, Webster R . Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus. J Infect Dis. 1998; 178(5):1257-62. DOI: 10.1086/314440. View

13.

Gambaryan A, Matrosovich M, BENDER C, KILBOURNE E . Differences in the biological phenotype of low-yielding (L) and high-yielding (H) variants of swine influenza virus A/NJ/11/76 are associated with their different receptor-binding activity. Virology. 1998; 247(2):223-31. DOI: 10.1006/viro.1998.9274. View

14.

Gambaryan A, Marinina V, Tuzikov A, Bovin N, Rudneva I, Sinitsyn B . Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs. Virology. 1998; 247(2):170-7. DOI: 10.1006/viro.1998.9224. View

15.

Gambaryan A, Webster R, Matrosovich M . Differences between influenza virus receptors on target cells of duck and chicken. Arch Virol. 2002; 147(6):1197-208. DOI: 10.1007/s00705-002-0796-4. View

16.

Gambaryan A, Tuzikov A, Pazynina G, Webster R, Matrosovich M, Bovin N . H5N1 chicken influenza viruses display a high binding affinity for Neu5Acalpha2-3Galbeta1-4(6-HSO3)GlcNAc-containing receptors. Virology. 2004; 326(2):310-6. DOI: 10.1016/j.virol.2004.06.002. View

17.

Gambarian A, Marinina V, Solodar T, Bovin N, Tuzikov A, Pazynina G . [Different receptor specificity of influence viruses from ducks and chickens and its reflection in the composition of sialosides on host cells and mucins]. Vopr Virusol. 2006; 51(4):24-32. View

18.

Eisfeld A, Neumann G, Kawaoka Y . Influenza A virus isolation, culture and identification. Nat Protoc. 2014; 9(11):2663-81. PMC: 5619698. DOI: 10.1038/nprot.2014.180. View

19.

Gambaryan A, Matrosovich M . A solid-phase enzyme-linked assay for influenza virus receptor-binding activity. J Virol Methods. 1992; 39(1-2):111-23. DOI: 10.1016/0166-0934(92)90130-6. View