Receptor binding specificity of recent human H3N2 influenza viruses

Virology Journal - Tập 4 Số 1 - 2007
Kshama Kumari1, Shelly Gulati1, David F. Smith2, Upma Gulati1, Richard D. Cummings2, Gillian M. Air1
1Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, USA
2Department of Biochemistry and Consortium for Functional Glycomics Core H, Emory University School of Medicine, Atlanta, USA

Tóm tắt

AbstractBackgroundHuman influenza viruses are known to bind to sialic acid linked α2-6 to galactose, but the binding specificity beyond that linkage has not been systematically examined. H3N2 human influenza isolates lost binding to chicken red cells in the 1990s but viruses isolated since 2003 have re-acquired the ability to agglutinate chicken erythrocytes. We have investigated specificity of binding, changes in hemagglutinin sequence of the recent viruses and the role of sialic acid in productive infection.ResultsViruses that agglutinate, or do not agglutinate, chicken red cells show identical binding to a Glycan Array of 264 oligosaccharides, binding exclusively to a subset of α2-6-sialylsaccharides. We identified an amino acid change in hemagglutinin that seemed to correlate with chicken red cell binding but when tested by mutagenesis there was no effect. Recombinant hemagglutinins expressed on Sf-9 cells bound chicken red cells but the released recombinant baculoviruses agglutinated only human red cells. Similarly, an isolate that does not agglutinate chicken red cells show hemadsorption of chicken red cells to infected MDCK cells. We suggest that binding of chicken red cells to cell surface hemagglutinin but not to virions is due to a more favorable hemagglutinin density on the cell surface. We investigated whether a virus specific for α2-6 sialyloligosaccharides shows differential entry into cells that have varying proportions of α2-6 and α2-3 sialic acids, including human A549 and HeLa cells with high levels of α2-6 sialic acid, and CHO cells that have only α2-3 sialic acid. We found that the virus enters all cell types tested and synthesizes viral nucleoprotein, localized in the nucleus, and hemagglutinin, transported to the cell surface, but infectious progeny viruses were released only from MDCK cells.ConclusionAgglutination of chicken red cells does not correlate with altered binding to any oligosaccharide on the Glycan Array, and may result from increased avidity due to density of hemagglutinin and not increased affinity. Absence of α2-6 sialic acid does not protect a cell from influenza infection and the presence of high levels of α2-6-sialic acids on a cell surface does not guarantee productive replication of a virus with α2-6 receptor specificity.

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Tài liệu tham khảo

Gottschalk A: The chemistry of virus receptors. In The Viruses. Volume 3. Edited by: Burnet FM, Stanley WM. New York , Academic Press; 1959:51-61.

Carroll SM, Higa HH, Paulson JC: Different cell-surface receptor determinants of antigenically similar influenza virus hemagglutinins. J Biol Chem 1981,256(16):8357-8363.

Rogers GN, Paulson JC: Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983,127(2):361-373. 10.1016/0042-6822(83)90150-2

Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, Wiley DC: Single amino acid substitutions in influenza hæmagglutinin change receptor binding specificity. Nature 1983, 304: 76-78. 10.1038/304076a0

Rogers GN, Daniels RS, Skehel JJ, Wiley DC, Wang X, Higa HH, Paulson JC: Host-mediated selection of influenza receptor variants. Sialic acid alpha 2,6Gal specific clones of A/duck/Ukraine/1/63 revert to sialic acid alpha 2,3Gal-specific wild type in ovo. J Biol Chem, 1985, 260: 7362-7367.

Baum LG, Paulson JC: Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl 1990, 40: 35-38.

Couceiro JN, Paulson JC, Baum LG: Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 1993, 29: 155-165. 10.1016/0168-1702(93)90056-S

Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA: Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997,233(1):224-234. 10.1006/viro.1997.8580

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 1998,72(9):7367-7373.

Rogers GN, D'Souza BL: Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989,173(1):317-322. 10.1016/0042-6822(89)90249-3

Wu W, Air GM: Binding of influenza viruses to sialic acids: reassortant viruses with A/NWS/33 hemagglutinin bind to alpha2,8-linked sialic acid. Virology 2004,325(2):340-350. 10.1016/j.virol.2004.05.013

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 2000,74(18):8502-8512. 10.1128/JVI.74.18.8502-8512.2000

Choppin PW, Tamm I: Two kinds of particles with contrasting properties in influenza A virus strains from the 1957 pandemic. Virology 1959,8():539-542. 10.1016/0042-6822(59)90059-5

Matrosovich M, Zhou N, Kawaoka Y, Webster R: The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 1999,73(2):1146-1155.

Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA: Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 2006,312(5772):404-410. 10.1126/science.1124513

Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, Sakai-Tagawa Y, Muramoto Y, Ito M, Kiso M, Horimoto T, Shinya K, Sawada T, Kiso M, Usui T, Murata T, Lin Y, Hay A, Haire LF, Stevens DJ, Russell RJ, Gamblin SJ, Skehel JJ, Kawaoka Y: Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 2006,444(7117):378-382. 10.1038/nature05264

Abe Y, Smith CW, Katkin JP, Thurmon LM, Xu X, Mendoza LH, Ballantyne CM: Endothelial alpha 2,6-linked sialic acid inhibits VCAM-1-dependent adhesion under flow conditions. J Immunol 1999,163(5):2867-2876.

Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S: Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 2001,289(1):74-85. 10.1006/viro.2001.1121

Nobusawa E, Ishihara H, Morishita T, Sato K, Nakajima K: Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Virology 2000,278(2):587-596. 10.1006/viro.2000.0679

Grassauer A, Egorov AY, Ferko B, Romanova I, Katinger H, Muster T: A host restriction-based selection system for influenza haemagglutinin transfectant viruses. J Gen Virol 1998,79(Pt 6):1405-1409.

Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, Kawaoka Y: Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 1997, 227: 493-499. 10.1006/viro.1996.8323

Gambaryan AS, Matrosovich MN: A solid-phase enzyme-linked assay for influenza virus receptor-binding activity. J Virol Methods 1992, 39: 111-123. 10.1016/0166-0934(92)90130-6

Matrosovich MN, Gambaryan AS, Tuzikov AB, Byramova NE, Mochalova LV, Golbraikh AA, Shenderovich MD, Finne J, Bovin NV: Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology 1993,196(1):111-121. 10.1006/viro.1993.1459

Masuda H, Suzuki T, Sugiyama Y, Horiike G, Murakami K, Miyamoto D, Jwa Hidari KI, Ito T, Kida H, Kiso M, Fukunaga K, Ohuchi M, Toyoda T, Ishihama A, Kawaoka Y, Suzuki Y: Substitution of amino acid residue in influenza A virus hemagglutinin affects recognition of sialyl-oligosaccharides containing N-glycolylneuraminic acid. FEBS Lett 1999,464(1-2):71-74. 10.1016/S0014-5793(99)01575-6

Suzuki Y, Nakao T, Ito T, Watanabe N, Toda Y, Xu G, Suzuki T, Kobayashi T, Kimura Y, Yamada A, et : Structural determination of gangliosides that bind to influenza A, B, and C viruses by an improved binding assay: strain-specific receptor epitopes in sialo-sugar chains. Virology 1992,189(1):121-131. 10.1016/0042-6822(92)90687-K

Glaser L, Stevens J, Zamarin D, Wilson IA, Garcia-Sastre A, Tumpey TM, Basler CF, Taubenberger JK, Palese P: A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J Virol 2005,79(17):11533-11536. 10.1128/JVI.79.17.11533-11536.2005

Parrish CR, Kawaoka Y: The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 2005, 59: 553-586. 10.1146/annurev.micro.59.030804.121059

Gambaryan AS, Tuzikov AB, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Bovin NV, Matrosovich MN: Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6'-sialyl(N-acetyllactosamine). Virology 1997,232(2):345-350. 10.1006/viro.1997.8572

Totani K, Kubota T, Kuroda T, Murata T, Hidari KI, Suzuki T, Suzuki Y, Kobayashi K, Ashida H, Yamamoto K, Usui T: Chemoenzymatic synthesis and application of glycopolymers containing multivalent sialyloligosaccharides with a poly(L-glutamic acid) backbone for inhibition of infection by influenza viruses. Glycobiology 2003,13(5):315-26. Epub 2002 Dec 17.. 10.1093/glycob/cwg032

Gambaryan A, Yamnikova S, Lvov D, Tuzikov A, Chinarev A, Pazynina G, Webster R, Matrosovich M, Bovin N: Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology 2005,334(2):276-283. 10.1016/j.virol.2005.02.003

Blixt O, Head S, Mondala T, Scanlan C, Huflejt ME, Alvarez R, Bryan MC, Fazio F, Calarese D, Stevens J, Razi N, Stevens DJ, Skehel JJ, van Die I, Burton DR, Wilson IA, Cummings R, Bovin N, Wong CH, Paulson JC: Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci U S A 2004,101(49):17033-17038. 10.1073/pnas.0407902101

Dyukova VI, Shilova NV, Galanina OE, Rubina AY, Bovin NV: Design of carbohydrate multiarrays. Biochim Biophys Acta 2006,1760(4):603-609.

Ratner DM, Adams EW, Disney MD, Seeberger PH: Tools for glycomics: mapping interactions of carbohydrates in biological systems. Chembiochem 2004,5(10):1375-1383. 10.1002/cbic.200400106

Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA: Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 2006,355(5):1143-1155. 10.1016/j.jmb.2005.11.002

Consortium for Functional Glycomics[http://www.functionalglycomics.org]

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 1986,60(2):476-482.

Zhang H, Air GM: Expression of functional influenza virus A polymerase proteins and template from cloned cDNAs in recombinant vaccinia virus infected cells. Biochem Biophys Res Commun 1994, 200: 95-101. 10.1006/bbrc.1994.1419

Lee EU, Roth J, Paulson JC: Alteration of terminal glycosylation sequences on N-linked oligosaccharides of Chinese hamster ovary cells by expression of beta-galactoside alpha 2,6-sialyltransferase. J Biol Chem 1989,264(23):13848-13855.

Connor RJ, Kawaoka Y, Webster RG, Paulson JC: Receptor Specificity in Human, Avian and Equine H2 and H3 Influenza Virus Isolates. Virology 1994, 205: 17-23. 10.1006/viro.1994.1615

Ito T, Suzuki Y, Suzuki T, Takada A, Horimoto T, Wells K, Kida H, Otsuki K, Kiso M, Ishida H, Kawaoka Y: Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J Virol 2000,74(19):9300-9305. 10.1128/JVI.74.19.9300-9305.2000

Suzuki Y, Ito T, Suzuki T, Holland RE Jr., Chambers TM, Kiso M, Ishida H, Kawaoka Y: Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 2000,74(24):11825-11831. 10.1128/JVI.74.24.11825-11831.2000

Mochalova L, Gambaryan A, Romanova J, Tuzikov A, Chinarev A, Katinger D, Katinger H, Egorov A, Bovin N: Receptor-binding properties of modern human influenza viruses primarily isolated in Vero and MDCK cells and chicken embryonated eggs. Virology 2003,313(2):473-480. 10.1016/S0042-6822(03)00377-5

Johnston SL, Wellens K, Siegel C: Comparison of hemagglutination and hemadsorption tests for influenza detection. Diagn Microbiol Infect Dis 1992,15(4):363-365. 10.1016/0732-8893(92)90025-O

Sauter NK, Hanson JE, Glick GD, Brown JH, Crowther RL, Park SJ, Skehel JJ, Wiley DC: Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: analysis by proton nuclear magnetic resonance spectroscopy and X-ray crystallography. Biochemistry 1992,31(40):9609-9621. 10.1021/bi00155a013

Lees WJ, Spaltenstein A, Kingery-Wood JE, Whitesides GM: Polyacrylamides bearing pendant alpha-sialoside groups strongly inhibit agglutination of erythrocytes by influenza A virus: multivalency and steric stabilization of particulate biological systems. J Med Chem 1994,37(20):3419-3433. 10.1021/jm00046a027

Deom CM, Caton AJ, Schulze IT: Host cell-mediated selection of a mutant influenza A virus that has lost a complex oligosaccharide from the tip of the hemagglutinin. Proc Natl Acad Sci U S A 1986,83(11):3771-3775. 10.1073/pnas.83.11.3771

Gambaryan AS, Marinina VP, Tuzikov AB, Bovin NV, Rudneva IA, Sinitsyn BV, Shilov AA, Matrosovich MN: 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):170-177. 10.1006/viro.1998.9224

Ohuchi M, Ohuchi R, Feldmann A, Klenk HD: Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 1997,71(11):8377-8384.

Gujuluva CN, Kundu A, Murti KG, Nayak DP: Abortive replication of influenza virus A/WSN/33 in HeLa229 cells: defective viral entry and budding processes. Virology 1994, 204: 491-505. 10.1006/viro.1994.1563

Stray SJ, Cummings RD, Air GM: Influenza virus infection of desialylated cells. Glycobiology 2000, 10: 649-658. 10.1093/glycob/10.7.649

Gulati U, Kumari K, Wu W, Keitel WA, Air GM: Amount and avidity of serum antibodies against native glycoproteins and denatured virus after repeated influenza whole-virus vaccination. Vaccine 2005, 23: 1414-1425. 10.1016/j.vaccine.2004.08.053

Gulati U, Hwang CC, Venkatramani L, Gulati S, Stray SJ, Lee JT, Laver WG, Bochkarev A, Zlotnick A, Air GM: Antibody epitopes on the neuraminidase of a recent H3N2 influenza virus (A/Memphis/31/98). J Virol 2002,76(23):12274-12280. 10.1128/JVI.76.23.12274-12280.2002

Liu C, Air GM: Selection and characterization of a neuraminidase-minus mutant of influenza virus and its rescue by cloned neuraminidase genes. Virology 1993, 194: 403-407. 10.1006/viro.1993.1276

Laver WG: Purification of influenza virus. In Fundamental Techniques in Virology. Edited by: Habel K, Salzman NP. New York , Academic Press; 1969:82-86.

Gulati U, Wu W, Gulati S, Kumari K, Waner JL, Air GM: Mismatched hemagglutinin and neuraminidase specificities in recent human H3N2 influenza viruses. Virology 2005,339(1):12-20. 10.1016/j.virol.2005.05.009

Macken C, Lu H, Goodman J, Boykin L: The value of a database in surveillance and vaccine selection. In Options for the Control of Influenza IV. Edited by: Osterhaus ADME, Cox N, Hampson AW. Amsterdam , Elsevier Science; 2001:103-106.