A chicken influenza virus recognizes fucosylated α2,3 sialoglycan receptors on the epithelial cells lining upper respiratory tracts of chickens

Virology

Volumn 456-457, Issue 1, 2014, Pages 131-138

  Hiono, Takahiro ^a,c   Okamatsu, Masatoshi ^a,c   Nishihara, Shoko ^b,c   Takase Yoden, Sayaka ^b,c   Sakoda, Yoshihiro ^a,c   Kida, Hiroshi ^a,b,c  

^a HOKKAIDO UNIVERSITY   (Japan)

^b SOKA UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Avian influenza virus; Fucosylation; Hemagglutinin; Interspecies transmission; Receptor

Indexed keywords

POLYSACCHARIDE; SIALIC ACID ALPHA 2,3 GALACTOSE GLYCAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CARBOHYDRATE ANALYSIS; CELL GROWTH; CONTROLLED STUDY; DUCK; EPITHELIUM CELL; FUCOSYLATION; GENE SEQUENCE; INFLUENZA VIRUS A; MDCK CELL; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR BINDING; TROPISM; UPPER RESPIRATORY TRACT; UPREGULATION; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS TRANSMISSION;

AVIAN INFLUENZA VIRUS; FUCOSYLATION; HEMAGGLUTININ; INTERSPECIES TRANSMISSION; RECEPTOR;

ANIMALS; CHICKENS; EPITHELIAL CELLS; GALACTOSE; ORTHOMYXOVIRIDAE; RECEPTORS, VIRUS; RESPIRATORY SYSTEM; VIRUS ATTACHMENT;

EID: 84897482457     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.03.004     Document Type: Article

References (37)

1. Aich U., Beckley N., Shriver Z., Raman R., Viswanathan K., Hobbie S., Sasisekharan R. Glycomics-based analysis of chicken red blood cells provides insight into the selectivity of the viral agglutination assay. FEBS J. 2011, 278:1699-1712.
2. Belser J.A., Blixt O., Chen L.M., Pappas C., Maines T.R., Van Hoeven N., Donis R., Busch J., McBride R., Paulson J.C., Katz J.M., Tumpey T.M. Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc. Natl. Acad. Sci. USA 2008, 105:7558-7563.
3. Chandrasekaran A., Srinivasan A., Raman R., Viswanathan K., Raguram S., Tumpey T.M., Sasisekharan V., Sasisekharan R. Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat. Biotechnol. 2008, 26:107-113.
4. Costa T., Chaves A.J., Valle R., Darji A., van Riel D., Kuiken T., Majó N., Ramis A. Distribution patterns of influenza virus receptors and viral attachment patterns in the respiratory and intestinal tracts of seven avian species. Vet. Res. 2012, 43:28.
5. Fouchier R.A., Munster V., Wallensten A., Bestebroer T.M., Herfst S., Smith D., Rimmelzwaan G.F., Olsen B., Osterhaus A.D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005, 79:2814-2822.
6. 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, 334:276-283.
7. Gambaryan A.S., Tuzikov A.B., Pazynina G.V., Desheva J.A., Bovin N.V., Matrosovich M.N., Klimov A.I. 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol. J. 2008, 5:85.
8. Hoffmann E., Neumann G., Kawaoka Y., Hobom G., Webster R.G. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. USA 2000, 97:6108-6113.
9. Hoffmann E., Stech J., Guan Y., Webster R.G., Perez D.R. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 2001, 146:2275-2289.
10. Ikeda N., Eguchi H., Nishihara S., Narimatsu H., Kannagi R., Irimura T., Ohta M., Matsuda H., Taniguchi N., Honke K. A remodeling system of the 3[U+05F3]-sulfo-Lewis a and 3[U+05F3]-sulfo-Lewis x epitopes. J. Biol. Chem. 2001, 276:38588-38594.
11. Ito T., Couceiro J.N., Kelm S., Baum L.G., Krauss S., Castrucci M.R., Donatelli I., Kida H., Paulson J.C., Webster R.G., Kawaoka Y. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 1998, 72:7367-7373.
12. 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, 74:9300-9305.
13. Johansson L., Johansson P., Miller-Podraza H. Detection by the lectins from Maackia amurensis and Sambucus nigra of 3- and 6-linked sialic acid in gangliosides with neolacto chains separated on thin-layer chromatograms and blotted to PVDF membranes. Anal. Biochem. 1999, 267:239-241.
14. Kawaguchi T., Matsumoto I., Osawa T. Studies on hemagglutinins from Maackia amurensis seeds. J. Biol. Chem. 1974, 249:2786-2792.
15. Kida H., Yanagawa R. Isolation and characterization of influenza a viruses from wild free-flying ducks in Hokkaido, Japan. Zentralbl. Bakteriol. Orig. A 1979, 244:135-143.
16. Kida H., Yanagawa R., Matsuoka Y. Duck influenza lacking evidence of disease signs and immune response. Infect. Immun. 1980, 30:547-553.
17. Kishida N., Sakoda Y., Eto M., Sunaga Y., Kida H. Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens. Arch. Virol. 2004, 149:2095-2104.
18. Konami Y., Yamamoto K., Osawa T., Irimura T. Strong affinity of Maackia amurensis hemagglutinin (MAH) for sialic acid-containing Ser/Thr-linked carbohydrate chains of N-terminal octapeptides from human glycophorin A. FEBS Lett. 1994, 342:334-338.
19. Kuchipudi S.V., Nelli R., White G.A., Bain M., Chang K.C., Dunham S. Differences in influenza virus receptors in chickens and ducks: implications for interspecies transmission. J. Mol. Genet. Med. 2009, 3:143-151.
20. Matrosovich M.N., Gambaryan A.S., Teneberg S., Piskarev V.E., Yamnikova S.S., Lvov D.K., Robertson J.S., Karlsson K.A. 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, 233:224-234.
21. Niwa H., Yamamura K., Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991, 108:193-199.
22. Okamatsu M., Saito T., Yamamoto Y., Mase M., Tsuduku S., Nakamura K., Tsukamoto K., Yamaguchi S. Low pathogenicity H5N2 avian influenza outbreak in Japan during the 2005-2006. Vet. Microbiol. 2007, 124:35-46.
23. Pillai S.P., Lee C.W. Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys. Virol. J. 2010, 7:5.
24. Read L., Muench H. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. (Lond.) 1938, 27:493-497.
25. Rogers G.N., D'Souza B.L. Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989, 173:317-322.
26. Rogers G.N., Paulson J.C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127:361-373.
27. Sakoda Y., Sugar S., Batchluun D., Erdene-Ochir T.O., Okamatsu M., Isoda N., Soda K., Takakuwa H., Tsuda Y., Yamamoto N., Kishida N., Matsuno K., Nakayama E., Kajihara M., Yokoyama A., Takada A., Sodnomdarjaa R., Kida H. Characterization of H5N1 highly pathogenic avian influenza virus strains isolated from migratory waterfowl in Mongolia on the way back from the southern Asia to their northern territory. Virology 2010, 406:88-94.
28. Shibuya N., Goldstein I.J., Broekaert W.F., Nsimba-Lubaki M., Peeters B., Peumans W.J. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2-6)Gal/GalNAc sequence. J. Biol. Chem. 1987, 262:1596-1601.
29. Shichinohe S., Okamatsu M., Sakoda Y., Kida H. Selection of H3 avian influenza viruses with SAα2,6Gal receptor specificity in pigs. Virology 2013, 444:404-408.
30. Shinya K., Ebina M., Yamada S., Ono M., Kasai N., Kawaoka Y. Avian flu: influenza virus receptors in the human airway. Nature 2006, 440:435-436.
31. Soda K., Asakura S., Okamatsu M., Sakoda Y., Kida H. H9N2 influenza virus acquires intravenous pathogenicity on the introduction of a pair of di-basic amino acid residues at the cleavage site of the hemagglutinin and consecutive passages in chickens. Virol. J. 2011, 8:64.
32. Stevens J., Blixt O., Chen L.M., Donis R.O., Paulson J.C., Wilson I.A. Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J. Mol. Biol. 2008, 381:1382-1394.
33. Stevens J., Blixt O., Paulson J.C., Wilson I.A. Glycan microarray technologies: tools to survey host specificity of influenza viruses. Nat. Rev. Microbiol. 2006, 4:857-864.
34. Suda T., Kamiyama S., Suzuki M., Kikuchi N., Nakayama K., Narimatsu H., Jigami Y., Aoki T., Nishihara S. Molecular cloning and characterization of a human multisubstrate specific nucleotide-sugar transporter homologous to Drosophila fringe connection. J. Biol. Chem. 2004, 279:26469-26474.
35. Suzuki Y., Ito T., Suzuki T., Holland R.E., Chambers T.M., Kiso M., Ishida H., Kawaoka Y. Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol. 2000, 74:11825-11831.
36. Tong S., Li Y., Rivailler P., Conrardy C., Castillo D.A., Chen L.M., Recuenco S., Ellison J.A., Davis C.T., York I.A., Turmelle A.S., Moran D., Rogers S., Shi M., Tao Y., Weil M.R., Tang K., Rowe L.A., Sammons S., Xu X., Frace M., Lindblade K.A., Cox N.J., Anderson L.J., Rupprecht C.E., Donis R.O. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 2012, 109:4269-4274.
37. Tong S., Zhu X., Li Y., Shi M., Zhang J., Bourgeois M., Yang H., Chen X., Recuenco S., Gomez J., Chen L.M., Johnson A., Tao Y., Dreyfus C., Yu W., McBride R., Carney P.J., Gilbert A.T., Chang J., Guo Z., Davis C.T., Paulson J.C., Stevens J., Rupprecht C.E., Holmes E.C., Wilson I.A., Donis R.O. New world bats harbor diverse influenza A viruses. PLoS Pathog. 2013, 9(e1003657).