Accumulation of amino acid substitutions promotes irreversible structural changes in the hemagglutinin of human influenza AH3 virus during evolution

Journal of Virology

Volumn 79, Issue 10, 2005, Pages 6472-6477

  Nakajima, Katsuhisa ^a   Nobusawa, Eri ^a   Nagy, Alexander ^b   Nakajima, Setsuko ^a  

^a NAGOYA CITY UNIV MEDICAL SCHOOL   (Japan)

^b Statni veterinarni ustav Praha   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HEMAGGLUTININ;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIGENICITY; ARTICLE; EVOLUTION; HEMADSORPTION; INFLUENZA VIRUS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; VIRUS MUTATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, VIRAL; CERCOPITHECUS AETHIOPS; COS CELLS; EVOLUTION; HEMADSORPTION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

INFLUENZA VIRUS;

EID: 18144398162     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.10.6472-6477.2005     Document Type: Article

References (41)

1. Afonnikov, D. A., D. Y. Oshepkov, and N. A. Kolchanov. 2001. Detection of conserved physico-chemical characteristics of proteins by analyzing clusters of positions with co-ordinated substitutions. Bioinformatics 17:1035-1046.
2. Bizebard, T., B. Gigant, P. Rigolet, B. Rasmussen, O. Diat, P. Bosecke, S. A. Wharton, J. J. Skehel, and M. Knossow. 1995. Structure of influenza viral haemagglutinin complexed with a neutralizing antibody. Nature 376:92-94.
3. Bush, R. M., C. A. Bender, K. Subbarao, N. J. Cox, and W. M. Fitch. 1999. Predicting the evolution of human influenza A. Science 286:1921-1925.
4. Bush, R. M., C. B. Smith, N. J. Cox, and W. M. Fitch. 2000. Effects of passage history and sampling bias on phylogenetic reconstruction of human influenza A evolution. Proc. Natl. Acad. Sci. USA 97:6974-6980.
5. Bush, R. M., W. M. Fitch, C. A. Bender, and N. J. Cox. 1999. Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol. Biol. Evol. 16:1457-1465.
6. Dokholyan, N. V., S. V. Budyrev, H. E. Stanley, and E. I. Shakhnovich. 2000. Identifying the protein folding nucleus using molecular dynamics. J. Mol. Biol. 296:1183-1188.
7. Ferguson, N. M., A. P. Galvani, and R. M. Bush. 2003. Ecological and immunological determinants of influenza evolution. Nature 422:428-433.
8. Fersht, A. R. 1997. Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7:3-9.
9. Fitch, W. M., R. M. Bush, C. A. Bender, and N. J. Cox. 1997. Longterm trends in the evolution of H(3)HA1 human influenza type A. Proc. Natl. Acad. Sci. USA 94:7712-7718.
10. Fleury, D., S. A. Wharton, J. J. Skehel, M. Knossow, and T. Bizebard. 1998. Antigen distortion allows influenza virus to escape neutralization. Nat. Struct. Biol. 5:119-123.
11. Fukami-Kobayashi, K., D. R. Schreibe, and S. A. Benner. 2002. Detecting compensatory covariation signals in protein evolution using reconstructed ancestral sequences. J. Mol. Biol. 319:729-743.
12. Govindarajan, S., J. E. Ness, S. Kim, E. C. Mundorff, J. Minshull, and C. Gustafsson. 2003. Systematic variation of amino acid substitutions for stringent assessment of pairwise covariation. J. Mol. Biol. 328:1061-1069.
13. Ha, Y., D. J. Stevens, J. J. Skehel, and D. C. Wiley. 2002. H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J. 21:865-875.
14. Kida, H., Y. Kawaoka, C. W. Naeve, and R. G. Webster. 1987. Antigenic and genetic conservation of H3 influenza virus in wild ducks. Virology 159:109-119.
15. Kok, R. G., D. M. Young, and L. N. Ornston. 1999. Phenotypic expression of PCR-generated random mutations in a Pseudomonas putida gene after its introduction into an Acinetobacter chromosome by natural transformation. Appl. Environ. Microbiol. 65:1675-1680.
16. Kostlansky, F., E. Vareckova, T. Betokova, V. Mucha, G. Russ, and S. A. Wharton. 2000. The strong positive correlation between effective affinity and infectivity neutralization of highly cross-reactive monoclonal antibodies IIB4, which recognize antigenic site B on influenza A virus haemagglutinin. J. Gen. Virol. 81:1727-1735.
17. Lambkin, R., L. McLain, S. E. Jones, A. L. Aldridge, and N. J. Dimmock. 1994. Neutralization escape mutants of type A influenza virus are readily selected by antisera from mice immunized with whole virus: a possible mechanism for antigenic drift. J. Gen. Virol. 75:3493-3502.
18. Mirny, L. A., V. I. Abkevich, and E. I. Shakhnovicch. 1998. How evolution makes proteins fold quickly. Proc. Natl. Acad. Sci. USA 95:4976-4981.
19. Morishita, T., E. Nobusawa, K. Nakajima, and S. Nakajima. 1996. Studies on the molecular basis for loss of the ability of recent influenza A(H1N1) virus strains to agglutinate chicken erythrocytes. J. Gen. Virol. 77:2499-2506.
20. Nakajima, K., E. Nobusawa, and S. Nakajima. 2004. Restriction of amino acid change on the H3 hemagglutinin protein of influenza A virus, p. 174-177. In Y. Kawaoka (ed.), Options for the control of influenza V. Elsevier, Amsterdam, The Netherlands.
21. Nakajima, K., E. Nobusawa, K. Tonegawa, and S. Nakajima. 2003. Restriction of amino acid change in influenza A virus H3HA: comparison of amino acid changes observed in nature and in vitro. J. Virol. 77:10088-10098.
22. Nakajima, S., and A. P. Kendal. 1981. Antigenic drift in influenza A/USSR/90/77 (H1N1) variants selected in vitro with monoclonal antibodies. Virology 113:656-662.
23. Nakajima, S., E. Nobusawa, and K. Nakajima. 2000. Variation in response among individuals to antigenic sites on the HA protein of human influenza virus may be responsible for the emergence of drift strains in the human population. Virology 274:220-231.
24. Nobusawa, E., T. Aoyama, Y. Suzuki, Y. Tateno, and K. Nakajima. 1991. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182:475-485.
25. Nobusawa, E., H. Ishihara, T. Morishita, K. Sato, and K. Nakajima. 2000. 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 278:587-596.
26. Plotkin, J. B., and J. Dushoff. 2003. Codon bias and frequency dependent selection on the hemagglutinin epitopes of influenza A virus. Proc. Natl. Acad. Sci. USA 100:7152-7157.
27. Plotkin, J. B., J. Dushoff, and S. A. Levin. 2002. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc. Natl. Acad. Sci. USA 99:6263-6268.
28. Rome, C., N. Zhou, J. Suss, J. Mackenzie, and R. G. Webster. 1996. Characterization of a novel influenza hemagglutinin, H15: criteria for determination of influenza A subtypes. Virology 217:508-516.
29. Russell, R. J., S. J. Gamblin, L. F. Haire, D. J. Stevens, B. Xiao, Y. Ha, and J. J. Skehel. 2004. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology 325:287-296.
30. Sato, K., T. Morishita, E. Nobusawa, K. Tonegawa., K. Sakae, S. Nakajima, and K. Nakajima. 2004. Amino-acid change on the antigenic region B1 of H3 haemagglutinin may be a trigger for the emergence of drift strains of influenza A virus. Epidemiol. Infect. 132:399-406.
31. Stevens, J., A. L. Corper, C. F. Basler, J. K. Taubenberger, P. Palese, and I. A. Wilson. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870.
32. Suzuki, Y., and T. Gojobori. 1999. A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 16:1315-1328.
33. Tonegawa, K., E. Nobusawa, K. Nakajima, T. Kato, T. Kutsune, K. Kuroda, T. Shibata, Y. Harada, A. Nakamura, and M. Itoh. 2003. Analysis of epitope recognition of antibodies induced by DNA immunization against hemagglutinin protein of influenza A virus. Vaccine 21:3118-3125.
34. Tourasse, N. J., and W. H. Li. 2000. Selective constraints, amino acid composition, and the rate of protein evolution. Mol. Biol. Evol. 17:656-664.
35. Vanlandschoot, P., E. Beinaert, S. Dewilde, X. Saelens, and A. Bestebroer. 1995. Fairly conserved epitope on the hemagglutinin of influenza A(H3N2) virus with variable accessibility to neutralizing antibody. Virology 212:526-534.
36. Wang, M.-L., J. J. Skehel, and D. C. Wiley. 1986. Comparative analysis of the specificities of anti-influenza hemagglutinin antibodies in human sera. J. Virol. 57:124-128.
37. Webster, R. G., and W. G. Laver. 1980. Determination of the number of non-overlapping antigenic areas on Hong Kong (H3N2) influenza virus hemagglutinin with monoclonal antibodies and the selection of variants with potential epidemiological significance. Virology 104:139-148.
38. Wiley, D. C., and J. J. Skehel. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365-394.
39. Wilson, I. A., and N. J. Cox. 1990. Structural basis of immune recognition of influenza hemagglutinin. Annu. Rev. Immunol. 8:737-771.
40. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolution. Nature 289:366-373.
41. Yewdell, J., A. J. Caton, and W. Gerhald. 1986. Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal anti-hemagglutinin antibodies. J. Virol. 57:632-638.