Predictability of antigenic evolution for H3N2 human influenza A virus

Genes and Genetic Systems

Volumn 88, Issue 4, 2013, Pages 225-232

  Suzuki, Yoshiyuki ^a  

^a NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

Antigenic distance; Antigenic evolution; Hemagglutinin; Influenza A virus; Predictability

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ;

ALGORITHM; ANTIGENIC MODULATION; ANTIGENICITY; ARTICLE; EVOLUTION; INFLUENZA VIRUS A H3N2; ISOELECTRIC POINT; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; SENSITIVITY AND SPECIFICITY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; VIRUS HEMAGGLUTINATION; VIRUS MUTATION;

ANTIGENS, VIRAL; BINDING SITES; EVOLUTION, MOLECULAR; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; MODELS, GENETIC; MODELS, IMMUNOLOGICAL; MUTATION; PHYLOGENY; SELECTION, GENETIC;

EID: 84893098393     PISSN: 13417568     EISSN: 18805779     Source Type: Journal    
DOI: 10.1266/ggs.88.225     Document Type: Article

References (55)

1. Ahmad, S., Gromiha, M. M., Fawareh, H., and Sarai, A. (2004) ASAView: database and tool for solvent accessibility representation in proteins. BMC Bioinformatics 5, 51.
2. Bao, Y., Bolotov, P., Dernovoy, D., Kiryutin, B., Zaslavsky, L., Tatusova, T., Ostell, J., and Lipman, D. (2008) The InfluenzaVirus Resource at the National Center for Biotechnology Information. J. Virol. 82, 596-601.
3. Bedford, T., Rambaut, A., and Pascual, M. (2012) Canalization of the evolutionary trajectory of the human influenza virus. BMC Biol. 10, 38.
4. Bush, R. M., Bender, C. A., Subbarao, K., Cox, N. J., and Fitch, W. M. (1999) Predicting the evolution of human influenza A. Science 286, 1921-1925.
5. DePristo, M. A., Weinreich, D. M., and Hartl, D. L. (2005) Missense meanderings in sequence space: a biophysical view of protein evolution. Nat. Rev. Genet. 6, 678-687.
6. Ekiert, D. C., Kashyap, A. K., Steel, J., Rubrum, A., Bhabha, G., Khayat, R., Lee, J. H., Dillon, M. A., O'Neil, R. E., Faynboym, A. M., et al. (2012) Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489, 526-532.
7. Fitch, W. M., Leiter, J. M., Li, X. Q., and Palese, P. (1991) PositiveDarwinian evolution in human influenza A viruses. Proc. Natl. Acad. Sci. USA 88, 4270-4274.
8. Grantham, R. (1974) Amino acid difference formula to help explain protein evolution. Science 185, 862-864.
9. Guerois, R., Nielsen, J. E., and Serrano, L. (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol. 320, 369-387.
10. Gupta, V., Earl, D. J., and Deem, M. W. (2006) Quantifying influenza vaccine efficacy and antigenic distance. Vaccine 24, 3881-3888.
11. Han, T., and Marasco, W. A. (2011) Structural basis of influenza virus neutralization. Ann. N. Y. Acad. Sci. 1217, 178-190.
12. He, J., and Deem, M. W. (2010) Low-dimensional clustering detects incipient dominant influenza strain clusters. ProteinEng. Des. Sel. 23, 935-946.
13. Hensley, S. E., Das, S. R., Bailey, A. L., Schmidt, L. M., Hickman, H. D., Jayaraman, A., Viswanathan, K., Raman, R., Sasisekharan, R., Bennink, J. R., and Yewdell, J. W. (2009) Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326, 734-736.
14. Huang, J.-W., King, C.-C., and Yang, J.-M. (2009) Co-evolution positions and rules for antigenic variants of human influenza A/H3N2 viruses. BMC Bioinformatics 10, S41.
15. Ito, K., Igarashi, M., Miyazaki, Y., Murakami, T., Iida, S., Kida, H., and Takada, A. (2011) Gnarled-trunk evolutionary model of influenza A virus hemagglutinin. PLoS ONE 6, e25953.
16. Katoh, K., Misawa, K., Kuma, K.-i., and Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066.
17. Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120.
18. Kobayashi, Y., and Suzuki, Y. (2012a) Compensatory evolution of net-charge in influenza A virus hemagglutinin. PLoS ONE, 7, e40422.
19. Kobayashi, Y., and Suzuki, Y. (2012b) Evidence for N-glycan shielding of antigenic sites during evolution of human influenza A virus hemagglutinin. J. Virol. 86, 3445-3451.
20. Kryazhimskiy, S., Dushoff, J., Bazykin, G. A., and Plotkin, J. B. (2011) Prevalence of epistasis in the evolution of influenza A surface proteins. PLoS Genet. 7, e1001301.
21. Lee, M.-S., and Chen, J. S.-E. (2004) Predicting antigenic variants of influenza A/H3N2 viruses. Emerg. Infect. Dis. 10, 1385-1390.
22. Lee, M.-S., Chen, M.-C., Liao, Y.-C., and Hsiung, C. A. (2007) Identifying potential immunodominant positions and predicting antigenic variants of influenza A/H3N2 viruses. Vaccine 25, 8133-8139.
23. Lees, W. D., Moss, D. S., and Shepherd, A. J. (2010) A computational analysis of the antigenic properties of haemagglutinin in influenza A H3N2. Bioinformatics 26, 1403-1408.
24. Liao, Y.-C., Lee, M.-S., Ko, C.-Y., and Hsiung, C. A. (2008) Bioinformatics models for predicting antigenic variants of influenza A/H3N2 virus. Bioinformatics 24, 505-512.
25. Matthews, B. W. (1975) Comparison of the predicted and observed secondary structure of T4 phage lysozyme. Biochim. Biophys. Acta 405, 442-451.
26. Mitnaul, L. J., Castrucci, M. R., Murti, K. G., and Kawaoka, Y. (1996) The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J. Virol. 70, 873-879.
27. Nei, M., and Kumar, S. (2000) Molecular Evolution and Phylogenetics. Oxford University Press, Oxford, New York.
28. Nelson, D. L., and Cox, M. M. (2008) Lehninger Principles of Biochemistry. 5th edition. W. H. Freeman and Company, New York.
29. Omori, R., and Sasaki, A. (2013) Timing of the emergence of new successful viral strains in seasonal influenza. J. Theor. Biol. 329, 32-38.
30. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
31. Schymkowitz, J. W. H., Rousseau, F., Martins, I. C., Ferkinghoff-Borg, J., Stricher, F., and Serrano, L. (2005) Prediction of water and metal binding sites and their affinities by using the Fold-X force field. Proc. Natl. Acad. Sci. USA 102, 10147-10152.
32. Shope, R. E. (1931) Swine influenza. III. Filtration experiments and etiology. J. Exp. Med. 54, 373-385.
33. Skehel, J. J., and Wiley, D. C. (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69, 531-569.
34. Smith, D. J., Lapedes, A. S., de Jong, J. C., Bestebroer, T. M., Rimmelzwaan, G. F., Osterhaus, A. D. M. E., and Fouchier, R. A. M. (2004) Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371-376.
35. Smith, W., Andrewes, C. H., and Laidlaw, P. P. (1933) A virus obtained from influenza patients. Lancet 222, 66-68.
36. Soundararajan, V., Zheng, S., Patel, N., Warnock, K., Raman, R., Wilson, I. A., Raguram, S., Sasisekharan, V., and Sasisekharan, R. (2011) Networks link antigenic and receptor-binding sites of influenza hemagglutinin: mechanistic insight into fitter strain propagation. Sci. Rep. 1, 200.
37. Suzuki, Y. (2004) Negative selection on neutralization epitopes of poliovirus surface proteins: implications for prediction of candidate epitopes for immunization. Gene 328, 127-133.
38. Suzuki, Y. (2006) Natural selection on the influenza virus genome. Mol. Biol. Evol. 23, 1902-1911.
39. Suzuki, Y. (2011) Positive selection for gains of N-linked glycosylation sites in hemagglutinin during evolution of H3N2 human influenza A virus. Genes Genet. Syst. 86, 287-294.
40. Suzuki, Y. (2013) Detection of positive selection eliminating effects of structural constraints in hemagglutinin of H3N2 human influenza A virus. Infect. Genet. Evol. 16, 93-98.
41. Tamura, K., Nei, M., and Kumar, S. (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101, 11030-11035.
42. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
43. Tokuriki, N., and Tawfik, D. S. (2009) Stability effects of mutations and protein evolvability. Curr. Opin. Struct. Biol. 19, 596-604.
44. Tokuriki, N., Stricher, F., Schymkowitz, J., Serrano, L., and Tawfik, D. S. (2007) The stability effects of protein mutations appear to be universally distributed. J. Mol. Biol. 369, 1318-1332.
45. Tokuriki, N., Oldfield, C. J., Uversky, V. N., Berezovsky, I. N., and Tawfik, D. S. (2009) Do viral proteins possess unique biophysical features? Trends Biochem. Sci. 34, 53-59.
46. Tomita, M., Hashimoto, K., Takahashi, K., Matsuzaki, Y., Matsushima, R., Saito, K., Yugi, K., Miyoshi, F., Nakano, H., Tanida, S., et al. (2000) The E-CELL project: towards integrative simulation of cellular processes. New Gener. Comput. 18, 1-12.
47. Tong, S., Li, Y., Rivailler, P., Conrardy, C., Castillo D. A. A., Chen, L.-M., Recuenco S., Ellison, J. A., Davis, C. T., York, I. A., et al. (2012) A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 109, 4269-4274.
48. Treanor, J. (2004) Weathering the influenza vaccine crisis. N. Engl. J. Med. 351, 2037-2040.
49. Whittle, J. R. R., Zhang, R., Khurana, S., King, L. R., Manischewitz, J., Golding, H., Dormitzer, P. R., Haynes, B. F., Walter, E. B., Moody, M. A., et al. (2011) Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl. Acad. Sci. USA 108, 14216-14221.
50. Wiley, D. C., Wilson, I. A., and Skehel, J. J. (1981) Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289, 373-378.
51. Wilson, I. A., Skehel, J. J., and Wiley, D. C. (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289, 366-373.
52. World Health Organization (1980) A revision of the system of nomenclature for influenza viruses: a WHO memorandum. Bull. W. H. O. 58, 585-591.
53. World Health Organization (2009) Influenza (Seasonal). http://www. who. int/mediacentre/factsheets/fs211/en/index. html.
54. Xia, Z., Jin, G., Zhu, J., and Zhou, R. (2009) Using a mutual information-based site transition network to map the genetic evolution of influenza A/H3N2 virus. Bioinformatics25, 2309-2317.
55. Xia, Z., Huynh, T., Kang, S.-g., and Zhou, R. (2012) Free-energy simulations reveal that both hydrophobic and polar interactions are important for influenza hemagglutinin antibody binding. Biophys. J. 102, 1453-1461.