Computational prediction of vaccine strains for human influenza A (H3N2) viruses

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 12123-12132

  Steinbruck L ^a   Klingen, T R ^a,b   McHardy, A C ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; VIRUS ANTIGEN;

ANTIGENIC VARIATION; ANTIGENICITY; ARTICLE; COMPUTER ANALYSIS; CONTROLLED STUDY; EPIDEMIC; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; INFLUENZA VIRUS A H3N2; MEASUREMENT ACCURACY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENETIC TREE CONSTRUCTION METHOD; PREDICTION; SEASONAL INFLUENZA; SEQUENCE ANALYSIS; VACCINE PRODUCTION; VIROGENESIS; VIRUS ISOLATION; VIRUS STRAIN; BIOLOGY; IMMUNOLOGY;

ANTIGENS, VIRAL; COMPUTATIONAL BIOLOGY; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES;

EID: 84907907812     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01861-14     Document Type: Article

References (63)

1. Tognotti E. 2009. Influenza pandemics: a historical retrospect. J. Infect. Dev. Ctries. 3:331-334. http://dx.doi.org/10.3855/jidc.239.
2. World Health Organization. 2009. Fact sheet no. 211. World Health Organization, Geneva, Switzerland.
3. Lin YP, Gregory V, Bennett M, Hay A. 2004. Recent changes among human influenza viruses. Virus Res. 103:47-52. http://dx.doi.org/10.1016 /j.virusres.2004.02.011.
4. Barr IG. 2014. WHO recommendations for the viruses used in the 2013-2014 Northern Hemisphere influenza vaccine: epidemiology, antigenic and genetic characteristics of influenza A(H1N1)pdm09, A(H3N2) and B influenza viruses collected from October 2012 to January 2013. Vaccine 32:4713-4725. http://dx.doi.org/10.1016/j.vaccine.2014.02.014.
5. Medina RA, García-Sastre A. 2011. Influenza A viruses: new research developments. Nat. Rev. Microbiol. 9:590-603. http://dx.doi.org/10.1038 /nrmicro2613.
6. Muramoto Y, Noda T, Kawakami E, Akkina R, Kawaoka Y. 2013. Identification of novel influenza A virus proteins translated from PA mRNA. J. Virol. 87:2455-2462. http://dx.doi.org/10.1128/JVI.02656-12.
7. Wise HM, Hutchinson EC, Jagger BW, Stuart AD, Kang ZH, Robb N, Schwartzman LM, Kash JC, Fodor E, Firth AE, Gog JR, Taubenberger JK, Digard P. 2012. Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain. PLoS Pathog. 8:e1002998. http://dx.doi.org/10.1371/journal.ppat.1002998.
8. Fouchier RAM, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus ADME. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79:2814-2822. http://dx.doi.org /10.1128/JVI.79.5.2814-2822.2005.
9. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen L-M, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO. 2012. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U. S. A. 109:4269-4274. http://dx.doi.org/10.1073/pnas.1116200109.
10. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO. 2013. New world bats harbor diverse influenza A viruses. PLoS Pathog. 9:e1003657. http://dx.doi.org/10.1371/journal.ppat.1003657.
11. WHO. 2012. Recommended composition of influenza virus vaccines for use in the 2012-2013 northern hemisphere influenza season. Wkly. Epidemiol. Rec. 87:83-96.
12. Webster RG, Laver WG, Air GM. 1982. Molecular mechanisms of variation in influenza viruses. Nature 296:115-121. http://dx.doi.org/10.1038 /296115a0.
13. Bush RM, Fitch WM, Bender CA, Cox NJ. 1999. Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol. Biol. Evol. 16: 1457-1465. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026057.
14. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305:371-376. http://dx.doi.org/10.1126/science.1097211.
15. WHO Writing Group, Ampofo WK, Baylor N, Cobey S, Cox NJ, Daves S, Edwards S, Ferguson N, Grohmann G, Hay A, Katz J, Kullabutr K, Lambert L, Levandowski R, Mishra AC, Monto A, Siqueira M, Tashiro M, Waddell AL, Wairagkar N, Wood J, Zambon M, Zhang W. 2012. Improving influenza vaccine virus selection: report of a WHO informal consultation held at WHO headquarters, Geneva, Switzerland, 14-16 June 2010. Influenza Other Respir. Viruses 6:142-152, e1-e5. http://dx.doi.org/10.1111/j.1750-2659.2011.00277.x.
16. World Health Organization. 2012. Recommended composition of influenza virus vaccines for use in the 2013 southern hemisphere influenza season. Wkly. Epidemiol. Rec. 87:389-400.
17. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC, de Jong JC, Kelso A, Klimov AI, Kageyama T, Komadina N, Lapedes AS, Lin YP, Mosterin A, Obuchi M, Odagiri T, Osterhaus AD, Rimmelzwaan GF, Shaw MW, Skepner E, Stohr K, Tashiro M, Fouchier RA, Smith DJ. 2008. Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 26:D31-D34. http://dx.doi.org/10.1016/j.vaccine.2008.07.078.
18. Bush RM, Bender CA, Subbarao K, Cox NJ, Fitch WM. 1999. Predicting the evolution of human influenza A. Science 286:1921-1925. http://dx.doi.org/10.1126/science.286.5446.1921.
19. Plotkin JB, Dushoff J, Levin SA. 2002. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc. Natl. Acad. Sci. U. S. A. 99:6263-6268. http://dx.doi.org/10.1073/pnas.082110799.
20. Shih AC-C, Hsiao T-C, Ho M-S, Li W-H. 2007. Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc. Natl. Acad. Sci. U. S. A. 104:6283-6288. http://dx.doi.org/10.1073/pnas.0701396104.
21. Du X, Wang Z, Wu A, Song L, Cao Y, Hang H, Jiang T. 2008. Networks of genomic co-occurrence capture characteristics of human influenza A (H3N2) evolution. Genome Res. 18:178-187. http://dx.doi.org/10.1101 /gr.6969007.
22. Kosakovsky Pond SL, Poon AFY, Leigh Brown AJ, Frost SDW. 2008. A maximum likelihood method for detecting directional evolution in protein sequences and its application to influenza A virus. Mol. Biol. Evol. 25:1809-1824. http://dx.doi.org/10.1093/molbev/msn123.
23. Xia Z, Jin G, Zhu J, Zhou R. 2009. Using a mutual information-based site transition network to map the genetic evolution of influenza A/H3N2 virus. Bioinformatics 25:2309-2317. http://dx.doi.org/10.1093/bioinformatics/btp423.
24. Tusche C, Steinbrück L, McHardy AC. 2012. Detecting patches of protein sites of influenza A viruses under positive selection. Mol. Biol. Evol. 29:2063-2071. http://dx.doi.org/10.1093/molbev/mss095.
25. Lin YP, Xiong X, Wharton SA, Martin SR, Coombs PJ, Vachieri SG, Christodoulou E, Walker PA, Liu J, Skehel JJ, Gamblin SJ, Hay AJ, Daniels RS, McCauley JW. 2012. Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc. Natl. Acad. Sci. U. S. A. 109:21474-21479. http://dx.doi.org/10.1073/pnas.1218841110.
26. Lee M-S, Chen M-C, Liao Y-C, Hsiung CA. 2007. Identifying potential immunodominant positions and predicting antigenic variants of influenza A/H3N2 viruses. Vaccine 25:8133-8139.
27. Liao Y-C, Lee M-S, Ko C-Y, Hsiung CA. 2008. Bioinformatics models for predicting antigenic variants of influenza A/H3N2 virus. Bioinformatics 24:505-512. http://dx.doi.org/10.1093/bioinformatics/btm638.
28. Huang J-W, King C-C, Yang J-M. 2009. Co-evolution positions and rules for antigenic variants of human influenza A/H3N2 viruses.BMCBioinformatics 10(Suppl 1):S41. http://dx.doi.org/10.1186/1471-2105-10-S1-S41.
29. Hirst GK. 1943. Studies of antigenic differences among strains of influenza A by means of red cell agglutination. J. Exp. Med. 78:407-423. http: //dx.doi.org/10.1084/jem.78.5.407.
30. Lin YP, Gregory V, Collins P, Kloess J, Wharton S, Cattle N, Lackenby A, Daniels R, Hay A. 2010. Neuraminidase receptor binding variants of human influenza A(H3N2) viruses resulting from substitution of aspartic acid 151 in the catalytic site: a role in virus attachment? J. Virol. 84:6769-6781. http://dx.doi.org/10.1128/JVI.00458-10.
31. Fouchier RAM, Smith DJ. 2010. Use of antigenic cartography in vaccine seed strain selection. Avian Dis. 54:220-223. http://dx.doi.org/10.1637 /8740-032509-ResNote.1.
32. Steinbrück L, McHardy AC. 2011. Allele dynamics plots for the study of evolutionary dynamics in viral populations. Nucleic Acids Res. 39:e4. http: //dx.doi.org/10.1093/nar/gkq909.
33. Steinbrück L, McHardy AC. 2012. Inference of genotype-phenotype relationships in the antigenic evolution of human influenza A (H3N2) viruses. PLoS Comp. Biol. 8:e1002492. http://dx.doi.org/10.1371/journal.pcbi.1002492.
34. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC, de Jong JC, Kelso A, Klimov AI, Kageyama T, Komadina N, Lapedes AS, Lin YP, Mosterin A, Obuchi M, Odagiri T, Osterhaus ADME, Rimmelzwaan GF, Shaw MW, Skepner E, Stohr K, Tashiro M, Fouchier RAM, Smith DJ. 2008. The global circulation of seasonal influenza A (H3N2) viruses. Science 320:340-346. http: //dx.doi.org/10.1126/science.1154137.
35. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D. 2008. The influenza virus resource at the National Center for Biotechnology Information. J. Virol. 82:596-601. http://dx.doi.org/10.1128/JVI.02005-07.
36. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
37. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704. http://dx.doi.org/10.1080/10635150390235520.
38. Zwickl DJ. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. thesis. The University of Texas at Austin, Austin, TX. http: //repositories.lib.utexas.edu/handle/2152/2666?show=full.
39. Fitch WM. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool. 20:406-416. http://dx.doi.org/10.2307/2412116.
40. Yang Z, Kumar S, Nei M. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641-1650.
41. Pagel M, Meade A, Barker D. 2004. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53:673-684. http://dx.doi.org /10.1080/10635150490522232.
42. Wiley DC, Wilson IA, Skehel JJ. 1981. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373-378. http://dx.doi.org /10.1038/289373a0.
43. Wiley DC, Skehel JJ. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365-394. http://dx.doi.org/10.1146/annurev.bi.56.070187.002053.
44. Wilson IA, Cox NJ. 1990. Structural basis of immune recognition of influenza virus hemagglutinin. Annu. Rev. Immunol. 8:737-771. http: //dx.doi.org/10.1146/annurev.iy.08.040190.003513.
45. Skehel J, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569. http://dx.doi.org/10.1146/annurev.biochem.69.1.531.
46. Wilson IA, Skehel JJ, Wiley DC. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 angst resolution. Nature 289:366-373. http://dx.doi.org/10.1038/289366a0.
47. WHO. 2003. Recommended composition of influenza virus vaccines for use in the 2004 influenza season. Wkly. Epidemiol. Rec. 78:375-379.
48. WHO. 2005. Recommended composition of influenza virus vaccines for use in the 2005-2006 influenza season. Wkly. Epidemiol. Rec. 80: 66-71.
49. WHO. 2006. Recommended composition of influenza virus vaccines for use in the 2007 influenza season. Wkly. Epidemiol. Rec. 81:390-395.
50. WHO. 2007. Recommended composition of influenza virus vaccines for use in the 2008 influenza season. Wkly. Epidemiol. Rec. 82:351-356.
51. WHO. 2004. Recommended composition of influenza virus vaccines for use in the 2004-2005 influenza season. Wkly. Epidemiol. Rec. 79:88-92.
52. WHO. 2004. Recommended composition of influenza virus vaccines for use in the 2005 influenza season. Wkly. Epidemiol. Rec. 79:369-373.
53. WHO. 2006. Recommended composition of influenza virus vaccines for use in the 2006-2007 influenza season. Wkly. Epidemiol. Rec. 81:82-86.
54. WHO. 2007. Recommended composition of influenza virus vaccines for use in the 2007-2008 influenza season. Wkly. Epidemiol. Rec. 82:69-74.
55. Du X, Dong L, Lan Y, Peng Y, Wu A, Zhang Y, Huang W, Wang D, Wang M, Guo Y, Shu Y, Jiang T. 2012. Mapping of H3N2 influenza antigenic evolution in China reveals a strategy for vaccine strain recommendation. Nat. Commun. 3:709. http://dx.doi.org/10.1038/ncomms1710.
56. Luksza M, Lässig M. 2014. A predictive fitness model for influenza. Nature 507:57-61. http://dx.doi.org/10.1038/nature13087.
57. WHO. 2003. Recommended composition of influenza virus vaccines for use in the 2003-2004 influenza season. Wkly. Epidemiol. Rec. 78:58-62.
58. Hensley SE, Das SR, Bailey AL, Schmidt LM, Hickman HD, Jayaraman A, Viswanathan K, Raman R, Sasisekharan R, Bennink JR, Yewdell JW. 2009. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326:734-736. http://dx.doi.org/10.1126/science.1178258.
59. Skehel J. 2009. An overview of influenza haemagglutinin and neuraminidase. Biologicals 37:177-178. http://dx.doi.org/10.1016/j.biologicals.2009.02.012.
60. Sandbulte MR, Westgeest KB, Gao J, Xu X, Klimov AI, Russell CA, Burke DF, Smith DJ, Fouchier RA, Eichelberger MC. 2011. Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. Proc. Natl. Acad. Sci. U. S. A. 108:20748-20753. http: //dx.doi.org/10.1073/pnas.1113801108.
61. Olson-Manning CF, Wagner MR, Mitchell-Olds T. 2012. Adaptive evolution: evaluating empirical support for theoretical predictions. Nat. Rev. Genet. 13:867-877. http://dx.doi.org/10.1038/nrg3322.
62. WHO. 2005. Recommended composition of influenza virus vaccines for use in the 2006 influenza season. Wkly. Epidemiol. Rec. 80:342-347.
63. WHO. 2008. Recommended composition of influenza virus vaccines for use in the 2008-2009 influenza season. Wkly. Epidemiol. Rec. 83: 81-87.