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Original Articles

Adaptive mutation in influenza A virus non-structural gene is linked to host switching and induces a novel protein by alternative splicing

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Pages 1-10 | Received 28 May 2012, Accepted 19 Sep 2012, Published online: 25 Jan 2019

  • Taubenberger JK, Morens DM. Pandemic influenza—including a risk assessment of H5N1. Rev Sci Tech2009;28: 187–202.
  • Fields BN, Knipe DM, Howley PM. Fields virology. 5th ed.Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins, 2007.
  • Smith GJ, Vijaykrishna D, Bahl J et al.Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature2009;459: 1122–1125.
  • Cauthen AN, Swayne DE, Schultz-Cherry S, Perdue ML, Suarez DL. Continued circulation in China of highly pathogenic avian influenza viruses encoding the hemagglutinin gene associated with the 1997 H5N1 outbreak in poultry and humans. J Virol2000;74: 6592–6599.
  • Taubenberger JK, Kash JC. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe2010;7: 440–451.
  • Pensaert M, Ottis K, Vandeputte J, Kaplan MM, Bachmann PA. Evidence for the natural transmission of influenza A virus from wild ducts to swine and its potential importance for man. Bull World Health Organ1981;59: 75–78.
  • Donatelli I, Campitelli L, Castrucci MR, Ruggieri A, Sidoli L, Oxford JS. Detection of two antigenic subpopulations of A(H1N1) influenza viruses from pigs: antigenic drift or interspecies transmission? J Med Virol1991;34: 248–257.
  • Vijaykrishna D, Smith GJ, Pybus OG et al.Long-term evolution and transmission dynamics of swine influenza A virus. Nature2011;473: 519–522.
  • Claas EC, Osterhaus AD, van Beek R et al.Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet1998;351: 472–477.
  • Chan PK. Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis2002;34 Suppl 2 S58–S64.
  • Guo Y, Li J, Cheng X. [Discovery of men infected by avian influenza A (H9N2) virus.] Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi1999;13: 105–108. Chinese
  • Dankar SK, Wang S, Ping J et al.Influenza A virus NS1 gene mutations F103L and M106I increase replication and virulence. Virol J2011;8: 13.
  • Forbes NE, Ping J, Dankar SK et al.Multifunctional adaptive NS1 mutations are selected upon human influenza virus evolution in the mouse. PLoS One2012;7: e31839.
  • Ping J, Dankar SK, Forbes NE et al.PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol 2010; 84: 10606–10618.
  • Ping J, Keleta L, Forbes NE et al.Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS One2011;6: e21740.
  • Brown EG, Liu H, Kit LC, Baird S, Nesrallah M. Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc Natl Acad Sci USA2001;98: 6883–6888.
  • O’Neill RE, Talon J, Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J1998;17: 288–296.
  • Hale BG, Randall RE, Ortin J, Jackson D. The multifunctional NS1 protein of influenza A viruses. J Gen Virol2008;89( Pt 10): 2359–2376.
  • Lamb RA, Lai CJ. Expression of unspliced NS1 mRNA, spliced NS2 mRNA, and a spliced chimera mRNA from cloned influenza virus NS DNA in an SV40 vector. Virology1984;135: 139–147.
  • Lamb RA, Lai CJ. Spliced and unspliced messenger RNAs synthesized from cloned influenza virus M DNA in an SV40 vector: expression of the influenza virus membrane protein (M1). Virology1982;123: 237–256.
  • de Vries W, Haasnoot J, Fouchier R, de Haan P, Berkhout B. Differential RNA silencing suppression activity of NS1 proteins from different influenza A virus strains. J Gen Virol2009;90( Pt 8): 1916–1922.
  • Lu Y, Qian XY, Krug RM. The influenza virus NS1 protein: a novel inhibitor of pre-mRNA splicing. Genes Dev1994;8: 1817–1828.
  • Fortes P, Beloso A, Ortin J. Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J1994;13: 704–712.
  • Robb NC, Jackson D, Vreede FT, Fodor E. Splicing of influenza A virus NS1 mRNA is independent of the viral NS1 protein. J Gen Virol 2010; 91( Pt 9): 2331–2340.
  • Wang M, Marin A. Characterization and prediction of alternative splice sites. Gene2006;366: 219–227.
  • Saxonov S, Daizadeh I, Fedorov A, Gilbert W. EID: the Exon-Intron Database-an exhaustive database of protein-coding intron-containing genes. Nucleic Acids Res 2000; 28: 185–190.
  • Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res2004;14: 1188–1190.
  • Bao Y, Bolotov P, Dernovoy D et al.The influenza virus resource at the National Center for Biotechnology Information. J Virol2008;82: 596–601.
  • Meintjes P, Duran C, Kearse M et al.Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics2012;28: 1647–1649.
  • Martins R, Silva B, Proenca D, Faustino P. Differential HFE gene expression is regulated by alternative splicing in human tissues. PLoS One2011;6: e17542.
  • Ast G. How did alternative splicing evolve? Nat Rev Genet2004;5: 773–782.
  • Carmel I, Tal S, Vig I, Ast G. Comparative analysis detects dependencies among the 5′ splice-site positions. RNA2004;10: 828–840.
  • Li S, Min JY, Krug RM, Sen GC. Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology2006;349: 13–21.
  • Min JY, Li S, Sen GC, Krug RM. A site on the influenza A virus NS1 protein mediates both inhibition of PKR activation and temporal regulation of viral RNA synthesis. Virology2007;363: 236–243.
  • Chen Z, Li Y, Krug RM. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J1999;18: 2273–2283.
  • Nemeroff ME, Barabino SM, Li Y, Keller W, Krug RM. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3'end formation of cellular pre-mRNAs. Mol Cell1998;1: 991–1000.
  • Li Y, Yamakita Y, Krug RM. Regulation of a nuclear export signal by an adjacent inhibitory sequence: the effector domain of the influenza virus NS1 protein. Proc Natl Acad Sci USA1998;95: 4864–4869.
  • Bornholdt ZA, Prasad BV. X-ray structure of NS1 from a highly pathogenic H5N1 influenza virus. Nature2008;456: 985–988.
  • Bornholdt ZA, Prasad BV. X-ray structure of influenza virus NS1 effector domain. Nat Struct Mol Biol2006;13: 559–560.
  • Song D, Kang B, Lee C et al.Transmission of avian influenza virus (H3N2) to dogs. Emerg Infect Dis2008;14: 741–746.
  • Narasaraju T, Sim MK, Ng HH et al.Adaptation of human influenza H3N2 virus in a mouse pneumonitis model: insights into viral virulence, tissue tropism and host pathogenesis. Microbes Infect2009;11: 2–11.
  • Lin YP, Shaw M, Gregory V et al.Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA2000;97: 9654–9658.
  • Guan Y, Shortridge KF, Krauss S, Webster RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the ‘internal’ genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA1999;96: 9363–9367.
  • Guan Y, Shortridge KF, Krauss S et al.H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. J Virol2000;74: 9372–9380.
  • Li S, Shi Z, Jiao P et al.Avian-origin H3N2 canine influenza A viruses in Southern China. Infect Genet Evol2010;10: 1286–1288.
  • Lin Y, Zhao Y, Zeng X, Lu C, Liu Y. Genetic and pathobiologic characterization of H3N2 canine influenza viruses isolated in the Jiangsu Province of China in 2009–2010. Vet Microbiol2012;158: 247–258.
  • Simulundu E, Ishii A, Igarashi M et al.Characterization of influenza A viruses isolated from wild waterfowl in Zambia. J Gen Virol2011;92( Pt 6): 1416–1427.
  • Kayali G, Webby RJ, Ducatez MF et al.The epidemiological and molecular aspects of influenza H5N1 viruses at the human-animal interface in Egypt. PLoS One2011; 6: e17730.
  • Shih SR, Suen PC, Chen YS, Chang SC. A novel spliced transcript of influenza A/WSN/33 virus. Virus Genes1998;17: 179–183.
  • Shih SR, Nemeroff ME, Krug RM. The choice of alternative 5′ splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci USA1995;92: 6324–6328.
  • Jackson D, Lamb RA. The influenza A virus spliced messenger RNA M mRNA3 is not required for viral replication in tissue culture. J Gen Virol2008;89( Pt 12): 3097–3101.
  • Chiang C, Chen GW, Shih SR. Mutations at alternative 5′ splice sites of M1 mRNA negatively affect influenza A virus viability and growth rate. J Virol.2008;82: 10873–10886.
  • Perdue ML. Naturally occurring NS gene variants in an avian influenza virus isolate. Virus Res1992;23: 223–240.
  • Wang L, Suarez DL, Pantin-Jackwood M et al.Characterization of influenza virus variants with different sizes of the non-structural (NS) genes and their potential as a live influenza vaccine in poultry. Vaccine2008;26: 3580–3586.
  • Dundon WG. Variability among the neuraminidase, non-structural 1 and PB1-F2 proteins in the influenza A virus genome. Virus Genes2012;44: 363–373.
  • Richt JA, Garcia-Sastre A. Attenuated influenza virus vaccines with modified NS1 proteins. Curr Top Microbiol Immunol2009;333: 177–195.
  • Seitz C, Frensing T, Hoper D, Kochs G, Reichl U. High yields of influenza A virus in Madin–Darby canine kidney cells are promoted by an insufficient interferon-induced antiviral state. J Gen Virol2010;91( Pt 7): 1754–1763.
  • Chen W, Calvo PA, Malide D et al.A novel influenza A virus mitochondrial protein that induces cell death. Nat Med2001;7: 1306–1312.
  • Jagger BW, Wise HM, Kash JC et al.An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science2012;337: 199–204.