Detection of site-specific positive Darwinian selection on pandemic influenza A/H1N1 virus genome: Integrative approaches

Genetica

Volumn 141, Issue 4-6, 2013, Pages 143-155

  Arunachalam, Ramaiah ^a,b  

^a MANONMANIAM SUNDARANAR UNIVERSITY   (India)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

Author keywords

Amino acid function; Genome; Natural selection; Novel influenza A H1N1 virus

Indexed keywords

EPITOPE; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BAYES THEOREM; CHEMISTRY; CODON; GENETIC SELECTION; GENETICS; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A H1N1; PANDEMIC; VIRUS GENOME;

AMINO ACID SUBSTITUTION; BAYES THEOREM; CODON; EPITOPES, B-LYMPHOCYTE; EPITOPES, T-LYMPHOCYTE; GENOME, VIRAL; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; PANDEMICS; SELECTION, GENETIC; VIRAL PROTEINS;

EID: 84879781847     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-013-9713-x     Document Type: Article

References (106)

1. Air GM, Els MC, Brown LE, Laver WG, Webster RG (1985) Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase. Virology 145: 237-248.
2. Arunachalam R, Paulkumar K, Annadurai G (2012a) Phylogenetic analysis of pandemic influenza A/H1N1 virus. Biologia 67(1): 14-31.
3. Arunachalam R, Paulkumar K, Annadurai G (2012b) Genetic ancestor of external antigens of pandemic influenza A/H1N1 virus. Interdiscip Sci Comput Life Sci 4: 282-290.
4. Arunachalam R, Senthilkumar B, Senbagam D, Selvamaleeswaran P, Rajasekarapandian M (2012c) Molecular phylogenetic approach for classification of Salmonella typhi. Res J Microbiol 7(1): 13-22.
5. Babon JAB, Cruz J, Orphin L, Pazoles P, Co MDT, Ennis FA, Terajima M (2009) Genome-wide screening of human T-cell epitopes in influenza A virus reveals a broad spectrum of CD4(+) T-cell responses to internal proteins, hemagglutinins, and neuraminidases. Hum Immunol 70: 711-721.
6. 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(2): 596-601.
7. Berkhoff EGM, de-Wit E, Geelhoed-Mieras MM, Boon ACM, Symons J, Fouchier RA, Osterhaus AD, Rimmelzwaan GF (2005) Functional constraints of influenza A virus epitopes limit escape from cytotoxic T lymphocytes. J Virol 79: 11239-11246.
8. Blanquer A, Uriz MJ (2007) Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Mol Phylogenet Evol 45: 392-397.
9. Boon ACM, de-Mutsert G, Graus YMF, Fouchier RAM, Sintnicolaas K, Osterhaus AD, Rimmelzwaan GF (2002a) Sequence variation in a newly identified HLA-B35-restricted epitope in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J Virol 76: 2567-2572.
10. Boon ACM, de-Mutsert G, Graus YMF, Fouchier RAM, Sintnicolaas K, Osterhaus AD, Rimmelzwaan GF (2002b) The magnitude and specificity of influenza A virus-specific cytotoxic T-lymphocyte responses in humans is related to HLA-A and -B phenotype. J Virol 76: 582-590.
11. Boon ACM, de-Mutsert G, Fouchier RAM, Osterhaus ADM, Rimmelzwaan GF (2006) The hypervariable immunodominant NP418-426 epitope from the influenza A virus nucleoprotein is recognized by cytotoxic T lymphocytes with high functional avidity. J Virol 80: 6024-6032.
12. 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.
13. Campitelli L, Ciccozzi M, Salemi M, Taglia F, Boros S, Donatelli I, Rezza G (2006) H5N1 influenza virus evolution: a comparison of different epidemics in birds and humans (1997-2004). J Gen Virol 87: 955-960.
14. Centers for Disease Control and Prevention (CDC) (2009) Swine influenza A(H1N1) infection in two children-Southern California, March-April 2009. Morb Mortal Wkly Rep 58: 400-402.
15. Chen J, Sun Y (2011) Variation in the analysis of positively selected sites using nonsynonymous/synonymous rate ratios: an example using influenza virus. PLoS One 6(5): e19996.
16. Cox RJ, Brokstad KA, Ogra P (2004) Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand J Immunol 59: 1-15.
17. Crowe SR, Miller SC, Brown DM, Adams PS, Dutton RW, Harmsen AG, Lund FE, Randall TD, Swain SL, Woodland DL (2006) Uneven distribution of MHC class II epitopes within the influenza virus. Vaccine 24: 457-467.
18. Cusick MF, Wang S, Eckels DD (2009) In vitro responses to avian influenza H5 by human CD4 T cells. J Immunol 183: 6432-6441.
19. Delport W, Poon A-FY, Frost SDW, Pond SLK (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26: 2455-2457.
20. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood estimation from incomplete data via the EM algorithm. J R Stat Soc Ser B 39: 1-38.
21. Dixit J, Srivastava H, Sharma M, Das MK, Singh OP, Raghavendra K, Nanda N, Dash AP, Saksena DN, Das A (2010) Phylogenetic inference of Indian malaria vectors from multilocus DNA sequences. Infect Genet Evol 10: 755-763.
22. Doron-Faigenboim A, Pupko T (2006) A combined empirical and mechanistic codon model. Mol Biol Evol 24: 388-397.
23. Duret L (2008) Neutral theory: the null hypothesis of molecular evolution. Nat Educ 1(1). http://www. nature. com/scitable/topicpage/neutral-theory-the-null-hypothesis-of-molecular-839.
24. Echevarria-Zuno S, Mejia-Arangure JM, Grajales-Muniz C, Gonzalez-Bonilla C, Borja-Aburto VH (2010) Seasonal vaccine effectiveness against pandemic A/H1N1 reply. Lancet 375: 802-803.
25. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
26. Furuse Y, Shimabukuro K, Odagiri T, Sawayama R, Okada T, Khandaker I, Suzuki A, Oshitani H (2010) Comparison of selection pressures on the HA gene of pandemic (2009) and seasonal human and swine influenza A H1 subtype viruses. Virology 405: 314-321.
27. Garcia-Garcia L, Valdespino-Gomez JL, Lazcano-Ponce E, Jimenez-Corona A, Higuera-Iglesias A, Cruz-Hervert P, Cano-Arellano B, Garcia-Anaya A, Ferreira-Guerrero E, Baez-Saldaña R, Ferreyra-Reyes L, Ponce-de-León-Rosales S, Alpuche-Aranda C, Rodriguez-López MH, Perez-Padilla R, Hernandez-Avila M (2009) Partial protection of seasonal trivalent inactivated vaccine against novel pandemic influenza A/H1N1 2009: case-control study in Mexico City. BMJ 339: b3928.
28. Ghedin E, Sengamalay NA, Shumway M, Zaborsk J, Feldblyum T, Subbu V, Spiro DJ, Sitz J, Koo H, Bolotov P, Dernovoy D, Tatusova T, Bao Y, George KS, Taylor J, Lipman DJ, Fraser CM, Taubenberger JK, Salzberg SL (2005) Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437: 1162-1166.
29. Gog JR, Rimmelzwaan GF, Osterhaus AD, Grenfell BT (2003) Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A. Proc Natl Acad Sci USA 100: 11143-11147.
30. Gubareva LV, Kaiser L, Hayden FG (2000) Influenza virus neuraminidase inhibitors. Lancet 355: 827-835.
31. Hardy CT, Young SA, Webster RG, Naeve CW, Owens RJ (1995) Egg fluids and cells of the chorioallantoic membrane of embryonated chicken eggs can select different variants of influenza A (H3N2) viruses. Virology 211: 302-306.
32. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH (1985) The molecular basis of the specific anti-influenza action of amantadine. EMBO J 4: 3021-3024.
33. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG (2000) A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci USA 97: 6108-6113.
34. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167-170.
35. Janies DA, Voronkin IO, Studer J, Hardman J, Alexandrov BB, Treseder TW, Valson C (2010) Selection for resistance to oseltamivir in seasonal and pandemic H1N1 influenza and widespread co-circulation of the lineages. Int J Health Geogr 9: 13.
36. Jin H, Zhou H, Liu H, Chan W, Adhikary L, Mahmood K, Lee MS, Kemble G (2005) Two residues in the hemagglutinin of A/Fujian/411/02-like influenza viruses are responsible for antigenic drift from A/Panama/2007/99. Virology 336: 113-119.
37. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.
38. Khurana S, Suguitan-Jr AL, Rivera Y, Simmons CP, Lanzavecchia A, Sallusto F, Manischewitz J, King LR, Subbarao K, Golding H (2009) Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med 6: e1000049.
39. Kilbourne ED, Smith C, Brett I, Pokorny BA, Johansson B, Cox N (2002) The total influenza vaccine failure of 1947 revisited: major intrasubtypic antigenic change can explain failure of vaccine in a post-World War II epidemic. Proc Natl Acad Sci USA 99: 10748-10752.
40. Kimura M (1968) Evolutionary rate at the molecular level. Nature 217: 624-626.
41. Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y (2004) Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364: 759-765.
42. Klein J, Horejsi V (1997) Immunology, 2nd edn. Blackwell Science, Oxford.
43. Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, Suzuki H, Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y (2004) Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431(7009): 703-707.
44. Kreijtz JHCM, de-Mutsert G, van-Baalen CA, Fouchier RAM, Osterhaus ADME, Rimmelzwaan GF (2008) Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J Virol 82: 5161-5166.
45. Lazrak A, Iles KE, Liu G, Noah DL, Noah JW, Matalon S (2009) Influenza virus M2 protein inhibits epithelial sodium channels by increasing reactive oxygen species. FASEB J 23(11): 3829-3842.
46. Lee LY-H, Ha DLAH, Simmons C, de-Jong MD, Chau NV, Schumacher R, Peng YC, McMichael AJ, Farrar JJ, Smith GL, Townsend AR, Askonas BA, Rowland-Jones S, Dong T (2008) Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest 118: 3478-3490.
47. Li W, Shi W, Qiao H, Ho SYW, Luo A, Zhang Y, Zhu C (2011) Positive selection on hemagglutinin and neuraminidase genes of H1N1 influenza viruses. Virology J 8: 183.
48. Liu W, Chen YH (2005) High epitope density in a single protein molecule significantly enhances antigenicity as well as immunogenicity: a novel strategy for modern vaccine development and a preliminary investigation about B cell discrimination of monomeric proteins. Eur J Immunol 35: 505-514.
49. Liu W, Peng Z, Liu Z, Lu Y, Ding J, Chen YH (2004) High epitope density in a single recombinant protein molecule of the extracellular domain of influenza A virus M2 protein significantly enhances protective immunity. Vaccine 23: 366-371.
50. Macken C, Lu H, Goodman J, Boykin L (2001) The value of a database in surveillance and vaccine selection. In: Osterhaus ADME, Cox N, Hampson AW (eds) Options for the control of influenza IV. Elsevier Science, Amsterdam, pp 103-106.
51. Malickbasha M, Arunachalam R, Senthilkumar B, Rajasekarapandian M, Annadurai G (2010) Effect of ompR gene mutation in expression of ompC and ompF of Salmonella typhi. Interdis Sci Comput Life Sci 2: 157-162.
52. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y (2000) Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74(18): 8502-8512.
53. Mayrose I, Graur D, Ben-Tal N, Pupko T (2004) Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior. Mol Biol Evol 21: 1781-1791.
54. Mayrose I, Mitchell A, Pupko T (2005) Site-specific evolutionary rate inference: taking phylogenetic uncertainty into account. J Mol Evol 60: 345-353.
55. Mostow SR, Schoenbaum SC, Dowdle WR, Coleman MT, Kaye HS, Hierholzer JC (1970) Studies on inactivated influenza vaccines. II. Effect of increasing dosage on antibody response and adverse reactions in man. Am J Epidemiol 92: 248-256.
56. Mozdzanowska K, Feng JQ, Eid M, Kragol G, Cudic M, Otvos L Jr, Gerhard W (2003) Induction of influenza type A virus-specific resistance by immunization of mice with a synthetic multiple antigenic peptide vaccine that contains ectodomains of matrix protein 2. Vaccine 21: 2616-2626.
57. Mullick J, Cherian SS, Potdar VA, Chadha MS, Mishra AC (2011) Evolutionary dynamics of the influenza A pandemic (H1N1) 2009 virus with emphasis on Indian isolates: evidence for adaptive evolution in the HA gene. Infect Genet Evol 11: 997-1005.
58. Nayak JL, Richards KA, Chaves FA, Sant AJ (2010) Analyses of the specificity of CD4 T cells during the primary immune response to influenza virus reveals dramatic MHC-linked asymmetries in reactivity to individual viral proteins. Viral Immunol 23: 169-180.
59. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York.
60. Noda T, Sagara H, Yen A, Takada A, Kida H, Cheng H, Kawaoka Y (2006) Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 439: 490-492.
61. Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, Rakestraw KM, Webster RG, Hoffmann E, Krauss S, Zheng J, Zhang Z, Naeve CW (2006) Large-scale sequence analysis of avian influenza isolates. Science 311: 1576-1580.
62. Pond SLK, Frost SDW (2005) Not so different after all: a comparison of methods for detecting amino acid sited under selection. Mol Biol Evol 22(5): 1208-1222.
63. Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21(5): 676-679.
64. Pond SLK, Frost SDW, Grossman Z, Gravenor MB, Richman DD, Brown AJ (2006) Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comput Biol 2(6): e62.
65. Pond SLK, Murrell B, Fourment M, Frost SDW, Delport W, Scheffler K (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol. doi: 10. 1093/molbev/msr125.
66. Potter CW (2001) A history of influenza. J Appl Microbiol 91: 572-579.
67. Qu Y, Zhang R, Cui P, Song G, Duan Z, Lei F (2011) Evolutionary genomics of the pandemic 2009 H1N1 influenza viruses (pH1N1v). Virol J 8: 250.
68. Richards KA, Chaves FA, Krafcik FR, Topham DJ, Lazarski CA, Sant AJ (2007) Direct ex vivo analyses of HLA-DR1 transgenic mice reveal an exceptionally broad pattern of immunodominance in the primary HLA-DR1-restricted CD4 T-cell response to influenza virus hemagglutinin. J Virol 81: 7608-7619.
69. Richards KA, Chaves FA, Sant AJ (2009) Infection of HLA-DR1 transgenic mice with a human isolate of influenza a virus (H1N1) primes a diverse CD4 T-cell repertoire that includes CD4 T cells with heterosubtypic cross-reactivity to avian (H5N1) influenza virus. J Virol 83: 6566-6577.
70. Roti M, Yang J, Berger D, Huston L, James EA, Kwok WW (2008) Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J Immunol 180: 1758-1768.
71. Schanen BC, De-Groot AS, Moise L, Ardito M, McClaine E, Martin W, Wittman V, Warren WL, Drake DR (2011) Coupling sensitive in vitro and in silico techniques to assess cross-reactive CD4(+) T cells against the swine-origin H1N1 influenza virus. Vaccine 29: 3299-3309.
72. Shen J, Ma J, Wang Q (2009) Evolutionary trends of A(H1N1) influenza virus hemagglutinin since 1918. PLoS One 4(11): e7789.
73. Smith W, Andrewes CH, Laidlaw PP (1933) A virus obtained from influenza patients. Lancet 225: 66-68.
74. 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.
75. Smith KA, Colvin CJ, Weber PSD, Spatz SJ, Coussens PM (2008) High titer growth of human and avian influenza viruses in an immortalized chick embryo cell line without the need for exogenous proteases. Vaccine 26: 3778-3782.
76. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A (2009) Origin and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459(7250): 1122-1126.
77. Stern A, Doron-Faigenboim A, Erez E, Martz E, Bacharach E, Pupko T (2007) Selecton 2007: advanced models for detecting positive and purifying selection using Bayesian inference approach. Nucleic Acids Res 35: W506-W511.
78. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA (2006) Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355(5): 1143-1155.
79. Suzuki Y (2004) Negative selection on neutralization epitopes of poliovirus surface proteins: implications for prediction of candidate epitopes for immunization. Gene 328: 127-133.
80. Suzuki Y (2006) Natural selection on the Influenza virus genome. Mol Biol Evol 23(10): 1902-1911.
81. Suzuki Y, Gojobori T (1999) A method for detecting positive selection at single amino acid sites. Mol Biol Evol 16(10): 1315-1328.
82. Suzuki Y, Gojobori T (2001) Positively selected amino acid sites in the entire coding region of hepatitis C virus subtype 1b. Gene 276: 83-87.
83. Suzuki Y, Nei M (2002) Origin and evolution of influenza virus hemagglutinin genes. Mol Biol Evol 19: 501-509.
84. Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20: 18-20.
85. Tamura K, Nei M (1993) Estimation of the number of nucleotide substituions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 11: 715-724.
86. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10): 2731-2739.
87. Thomas PG, Keating R, Hulse-Post DJ, Doherty PC (2006) Cell mediated protection in influenza infection. Emerg Infect Dis 12: 48-54.
88. Thomas PG, Brown SA, Keating R, Yue W, Morris MY, So J, Webby RJ, Doherty PC (2007) Hidden epitopes emerge in secondary influenza virus-specific CD8+ T cell responses. J Immunol 178: 3091-3098.
89. Trojan A, Urosevic M, Hummerjohann J, Giger R, Schanz U, Stahel RA (2003) Immune reactivity against a novel HLA-A3-restricted influenza virus peptide identified by predictive algorithms and interferon-gamma quantitative PCR. J Immunol 26: 41-46.
90. Tu W, Mao H, Zheng J, Liu Y, Chiu SS, Qin G, Chan PL, Lam KT, Guan J, Zhang L, Guan Y, Yuen KY, Peiris JS, Lau YL (2010) Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J Virol 84(13): 6527-6535.
91. Tumpey TM, Maines TR, Van-Hoeven N, Glaser L, Solorzano A, Pappas C, Cox NJ, Swayne DE, Palese P, Katz JM, Garcia-Sastre A (2007) A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315(5812): 655-659.
92. Venkatramani L, Bochkareva E, Lee JT, Gulati U, Laver WG, Bochkarev A, Air GM (2006) An epidemiologically significant epitope of a 1998 human influenza virus neuraminidase forms a highly hydrated interface in the NA-antibody complex. J Mol Biol 356: 651-663.
93. Vita R, Zarebski L, Greenbaum JA, Emami H, Hoof I, Salimi N, Damle R, Sette A, Peters B (2010) The immune epitope database 2. 0. Nucleic Acids Res 38(Database issue): D854-D862.
94. Webby RJ, Webster RG (2003) Are we ready for pandemic influenza? Science 302(5650): 1519-1522.
95. Webster RG, Kawaoka Y, Bean WJ (1986) Vaccination as a strategy to reduce the emergence of amantadine- and rimantadine-resistant strains of A/chick/Pennsylvania/83 (H5N2) influenza virus. J Antimicrob Chemother 18: 157-164.
96. 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.
97. Wolf YI, Viboud C, Holmes EC, Koonin EV, Lipman DJ (2006) Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biol Direct 1: 34.
98. World Health Organization (WHO) (1980) A revision of the system of nomenclature for influenza viruses: a WHO memorandum. Bull WHO 58: 585-591.
99. Wu F, Yuan X-Y, Li J, Chen Y-H (2009) The co-administration of CpG-ODN influenced protective activity of influenza M2e vaccine. Vaccine 27: 4320-4324.
100. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15(12): 496-503.
101. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-449.
102. + T cells epitopes restricted by various DR alleles. Available from http://www. immuneepitope. org/assayId/1816085.
103. Zamarin D, Ortigozza MB, Palese P (2006) Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 80(16): 7976-7983.
104. Zebedee SL, Lamb RA (1988) Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J Virol 62: 2762-2772.
105. Zhao R, Cui S, Guo L, Wu C, Gonzalez R, Paranhos-Baccalà G, Vernet G, Wang J, Hung T (2011) Identification of a highly conserved h1 subtype-specific epitope with diagnostic potential in the hemagglutinin protein of influenza a virus. PLoS One 6: e23374.
106. Zharikova D, Mozdzanowska K, Feng J, Zhang M, Gerhard W (2005) Influenza type A virus escape mutants emerge in vivo in the presence of antibodies to the ectodomain of matrix protein-2. J Virol 79: 6644-6654.