Changes of the receptor-binding properties of influenza B virus B/Victoria/504/2000 during adaptation in chicken eggs

Virology

Volumn 394, Issue 2, 2009, Pages 218-226

  Lugovtsev, Vladimir Y ^a   Smith, David F ^b   Weir, Jerry P ^a  

^a Office of Biologics Research and Review   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Egg adaptation, Glycan array; Influenza B virus; Receptor binding

Indexed keywords

ARGININE; ASPARTIC ACID; GLUTAMIC ACID; GLYCAN; GLYCINE; METHIONINE; OLIGOSACCHARIDE; PENTASACCHARIDE; TYROSINE; VIRUS HEMAGGLUTININ;

ADAPTATION; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EGG; GENETIC VARIABILITY; INFLUENZA VIRUS B; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; RECEPTOR BINDING; SIALYLATION; VIRUS ATTACHMENT; VIRUS STRAIN;

ADAPTATION, BIOLOGICAL; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CARBOHYDRATE SEQUENCE; CHICK EMBRYO; GENETIC VARIATION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA B VIRUS; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; RECEPTORS, VIRUS;

INFLUENZA B VIRUS;

EID: 70449527362     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.08.014     Document Type: Article

References (47)

1. Baum L.G., and Paulson J.C. Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem. Suppl. 40 (1990) 35-38
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., and Tumpey T.M. Contemporary North American influenza H7 viruses possess human receptor specificity: implications for virus transmissibility. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 7558-7563
3. Blixt O., Head S., Mondala T., Scanlan C., Huflejt M.E., Alvarez R., Bryan M.C., Fazio F., Calarese D., Stevens J., Razi N., Stevens D.J., Skehel J.J., van Die I., Burton D.R., Wilson I.A., Cummings R., Bovin N., Couceiro J.N., Paulson J.C., and Baum L.G. Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res. 29 (1993) 155-165
4. Blixt O., Head S., Mondala T., Scanlan C., Huflejt M.E., Alvarez R., Bryan M.C., Fazio F., Calarese D., Stevens J., Razi N., Stevens D.J., Skehel J.J., van Die I., Burton D.R., Wilson I.A., Cummings R., Bovin N., Wong C.H., and Paulson J.C. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 17033-17038
5. Burnet F.M., and Bull D.R. Changes in influenza virus associated with adaptation to passage in chick embryos. Aust. J. Exp. Biol. Med. Sci. 21 (1943) 55-69
6. Chen R., and Holmes E.C. The evolutionary dynamics of human influenza B virus. J. Mol. Evol. 66 (2008) 655-663
7. Connor R.J., Kawaoka Y., Webster R.G., and Paulson J.C. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205 (1994) 17-23
8. Couceiro J.N., Paulson J.C., and Baum L.G. Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res. 29 (1993) 155-165
9. Gambaryan A.S., and Matrosovich M.N. A solid-phase enzyme-linked assay for influenza virus receptor-binding activity. J. Virol. Methods 39 (1992) 111-123
10. Gambaryan A.S., Matrosovich M.N., Bender C.A., and Kilbourne E.D. 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 247 (1998) 223-231
11. Gambaryan A.S., Piskarev V.E., Yamskov I.A., Sakharov A.M., Tuzikov A.B., Bovin N.V., Nifant'ev N.E., and Matrosovich M.N. Human influenza virus recognition of sialyloligosaccharides. FEBS Lett. 366 (1995) 57-60
12. Gambaryan A.S., Robertson J.S., and Matrosovich M.N. Effects of egg-adaptation on the receptor-binding properties of human influenza A and B viruses. Virology 258 (1999) 232-239
13. Gambaryan A.S., Tuzikov A.B., Piskarev V.E., Yamnikova S.S., Lvov D.K., Robertson J.S., Bovin N.V., and Matrosovich M.N. 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 232 (1997) 345-350
14. Govorkova E.A., Matrosovich M.N., Tuzikov A.B., Bovin N.V., Gerdil C., Fanget B., and Webster R.G. Selection of receptor-binding variants of human influenza A and B viruses in baby hamster kidney cells. Virology 262 (1999) 31-38
15. Ito T., Suzuki Y., Takada A., Kawamoto A., Otsuki K., Masuda H., Yamada M., Suzuki T., Kida H., and Kawaoka Y. Differences in sialic acid-galactose linkages in the chicken egg amnion and allantois influence human influenza virus receptor specificity and variant selection. J. Virol. 71 (1997) 3357-3362
16. Kaverin N.V., Matrosovich M.N., Gambaryan A.S., Rudneva I.A., Shilov A.A., Varich N.L., Makarova N.V., Kropotkina E.A., and Sinitsin B.V. Intergenic HA-NA interactions in influenza A virus: postreassortment substitutions of charged amino acid in the hemagglutinin of different subtypes. Virus Res. 66 (2000) 123-129
17. Kumari K., Gulati S., Smith D.F., Gulati U., Cummings R.D., and Air G.M. Receptor binding specificity of recent human H3N2 influenza viruses. Virol. J. 4 (2007) 42
18. Lamb R.A., and Krug R.M. Orthomyxoviridae: the viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology. 4th ed. (2001), Lippincott, Williams and Wilkins, Philadelphia 1487-1531
19. Lugovtsev V.Y., Vodeiko G.M., and Levandowski R.A. Mutational pattern of influenza B viruses adapted to high growth replication in embryonated eggs. Virus Res. 109 (2005) 149-157
20. Lugovtsev V.Y., Vodeiko G.M., Strupczewski C.M., Ye Z., and Levandowski R.A. Generation of the influenza B viruses with improved growth phenotype by substitution of specific amino acids of hemagglutinin. Virology 365 (2007) 315-323
21. Matrosovich M.N., Gambaryan A.S., Teneberg S., Piskarev V.E., Yamnikova S.S., Lvov D.K., Robertson J.S., and 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 233 (1997) 224-234
22. Matrosovich M.N., Gambaryan A.S., Tuzikov A.B., Byramova N.E., Mochalova L.V., Golbraikh A.A., Shenderovich M.D., Finne J., and Bovin N.V. Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology 196 (1993) 111-121
23. Matrosovich M.N., Klenk H.-D., and Kawaoka Y. Receptor specificity, host-range, and pathogenicity of influenza viruses. In: Kawaoka Y. (Ed). Influenza Virology. Current Topics (2006), Caister Academic Press 95-137
24. Oxford J.S., Schild G.C., Corcoran T., Newman R., Major D., Robertson J., Bootman J., Higgins P., al-Nakib W., and Tyrrell D.A. A host-cell-selected variant of influenza B virus with a single nucleotide substitution in HA affecting a potential glycosylation site was attenuated in virulence for volunteers. Arch. Virol. 110 (1990) 37-46
25. Palmer D.F., Coleman M.T., Dowdle W.R., and Schild G.C. Advanced laboratory techniques for influenza diagnosis. Immunology series no. 6. U.S. Department of Health, Education and Welfare, Washington, D.C. (1975)
26. Paulson J.C., Blixt O., and Collins B.E. Sweet spots in functional glycomics. Nat. Chem. Biol. 2 (2006) 238-248
27. Robertson J.S. Clinical influenza virus and the embryonated hen's egg. Rev. Med. Virol. 3 (1993) 97-106
28. Robertson J.S., Bootman J.S., Nicolson C., Major D., Robertson E.W., and Wood J.M. The hemagglutinin of influenza B virus present in clinical material is a single species identical to that of mammalian cell-grown virus. Virology 179 (1990) 35-40
29. Robertson J.S., Naeve C.W., Webster R.G., Bootman J.S., Newman R., and Schild G.C. Alterations in the hemagglutinin associated with adaptation of influenza B virus to growth in eggs. Virology 143 (1985) 166-174
30. Robertson J.S., Nicolson C., Major D., Robertson E.W., and Wood J.M. The role of amniotic passage in the egg-adaptation of human influenza virus is revealed by haemagglutinin sequence analyses. J. Gen. Virol. 74 (1993) 2047-2051
31. Rogers G.N., and 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 127 (1983) 361-373
32. Rogers G.N., and D'Souza B.L. Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173 (1989) 317-322
33. Saito T., Nakaya Y., Suzuki T., Ito R., Saito T., Saito H., Takao S., Sahara K., Odagiri T., Murata T., Usui T., Suzuki Y., and Tashiro M. Antigenic alteration of influenza B virus associated with loss of a glycosylation site due to host-cell adaptation. J. Med. Virol. 74 (2004) 336-343
34. Sriwilaijaroen N., Kondo S., Yagi H., Wilairat P., Hiramatsu H., Ito M., Ito Y., Kato K., and Suzuki Y. Analysis of N-glycans in embryonated chicken egg chorioallantoic and amniotic cells responsible for binding and adaptation of human and avian influenza viruses. Glycoconj. J. 26 (2008) 433-443
35. Stevens J., Blixt O., Chen L.M., Donis R.O., Paulson J.C., and Wilson I.A. Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J. Mol. Biol. 381 (2008) 1382-1394
36. Stevens J., Blixt O., Glaser L., Taubenberger J.K., Palese P., Paulson J.C., and Wilson I.A. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355 (2006) 1143-1155
37. Stevens J., Blixt O., Paulson J.C., and Wilson I.A. Glycan microarray technologies: tools to survey host specificity of influenza viruses. Nat. Rev. Microbiol. 4 (2006) 857-864
38. Stevens J., Blixt O., Tumpey T.M., Taubenberger J.K., Paulson J.C., and Wilson I.A. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312 (2006) 404-410
39. Suzuki Y. Gangliosides as influenza virus receptors. Variation of influenza viruses and their recognition of the receptor sialo-sugar chains. Prog. Lipid Res. 33 (1994) 429-457
40. Suzuki Y. Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull. 28 (2005) 399-408
41. Suzuki Y., Nagao Y., Kato H., Suzuki T., Matsumoto M., and Murayama J. The hemagglutinins of the human influenza viruses A and B recognize different receptor microdomains. Biochim. Biophys. Acta 903 (1987) 417-424
42. Suzuki Y., Kato H., Naeve C.W., and Webster R.G. Single-amino-acid substitution in an antigenic site of influenza virus hemagglutinin can alter the specificity of binding to cell membrane-associated gangliosides. J. Virol. 63 (1989) 4298-4302
43. Suzuki Y., Nakao T., Ito T., Watanabe N., Toda Y., Xu G., Suzuki T., Kobayashi T., Kimura Y., Yamada A., Sugawara K., Nishimura H., Kitame F., Nakamura K., Deya E., Kiso M., and Hasegawa A. 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 189 (1992) 121-131
44. Wang Q., Tian X., Chen X., and Ma J. Structural basis for receptor specificity of influenza B virus hemagglutinin. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 16874-16879
45. Williams S.P., and Robertson J.S. Analysis of the restriction to the growth of nonegg-adapted human influenza virus in eggs. Virology 196 (1993) 660-665
46. Xu G., Suzuki T., Tahara H., Kiso M., Hasegawa A., and Suzuki Y. Specificity of sialyl-sugar chain mediated recognition by the hemagglutinin of human influenza B virus isolates. J. Biochem. 115 (1994) 202-207
47. Xu G., Horiike G., Suzuki T., Miyamoto D., Kumihashi H., and Suzuki Y. A novel strain, B/Gifu/2/73, differs from other influenza B viruses in the receptor binding specificities toward sialo-sugar chain linkage. Biochem. Biophys. Res. Commun. 224 (1996) 815-818