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

Emerging Microbes and Infections

Volumn 1, Issue , 2012, Pages

  Selman, Mohammed ^a   Dankar, Samar K ^a   Forbes, Nicole E ^a   Jia, Jian Jun ^a   Brown, Earl G ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

host switch; influenza A virus; non structural protein 1; NS gene; NS1; NS3; viral splicing

Indexed keywords

NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 3;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CODON; DOG; GAIN OF FUNCTION MUTATION; GENE DELETION; HOST SELECTION; HOST SWITCHING; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; MOLECULAR EVOLUTION; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SYNTHESIS; SEQUENCE HOMOLOGY; SWINE; VIRUS MUTATION; VIRUS TRANSMISSION;

AVES; INFLUENZA A VIRUS; MAMMALIA; SUIDAE; SWINE INFLUENZA VIRUS;

EID: 84874044936     PISSN: None     EISSN: 22221751     Source Type: Journal    
DOI: 10.1038/emi.2012.38     Document Type: Article

References (59)

1. Taubenberger JK, Morens DM. Pandemic influenza - including a risk assessment of H5N1. Rev Sci Tech 2009; 28: 187-202.
2. Fields BN, Knipe DM, Howley PM. Fields virology. 5th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins, 2007.
3. Smith GJ, Vijaykrishna D, Bahl J et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009; 459: 1122-1125.
4. 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 Virol 2000; 74: 6592-6599. (Pubitemid 30429828)
5. Taubenberger JK, Kash JC. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 2010; 7: 440-451.
6. 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 Organ 1981; 59: 75-78. (Pubitemid 11073209)
7. 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 Virol 1991; 34: 248-257.
8. Vijaykrishna D, Smith GJ, Pybus OG et al. Long-term evolution and transmission dynamics of swine influenza A virus. Nature 2011; 473: 519-522.
9. Claas EC, Osterhaus AD, van Beek R et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 1998; 351: 472-477. (Pubitemid 28070093)
10. Chan PK. Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 2002; 34 Suppl 2: S58-S64. (Pubitemid 34442210)
11. 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 Zhi 1999; 13: 105-108. Chinese
12. Dankar SK, Wang S, Ping J et al. Influenza A virus NS1 gene mutations F103L and M106I increase replication and virulence. Virol J 2011; 8: 13.
13. Forbes NE, Ping J, Dankar SK et al.Multifunctional adaptive NS1mutations are selected upon human influenza virus evolution in the mouse. PLoS One 2012; 7: e31839.
14. 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.
15. 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 One 2011; 6: e21740.
16. 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 USA 2001; 98: 6883-6888. (Pubitemid 32538311)
17. O'Neill RE, Talon J, Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J 1998; 17: 288-296. (Pubitemid 28041069)
18. Hale BG, Randall RE, Ortin J, Jackson D. The multifunctionalNS1 protein of influenza A viruses. J Gen Virol 2008; 89(Pt 10): 2359-2376.
19. 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. Virology 1984; 135: 139-147. (Pubitemid 14122254)
20. Lamb RA, Lai CJ. Spliced and unspliced messenger RNAs synthesized from cloned influenza virusMDNA in an SV40 vector: expression of the influenza virus membrane protein (M1). Virology 1982; 123: 237-256. (Pubitemid 13221635)
21. de VriesW, 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 Virol 2009; 90(Pt 8): 1916-1922.
22. Lu Y, Qian XY, Krug RM. The influenza virus NS1 protein: a novel inhibitor of prem RNA splicing. Genes Dev 1994; 8: 1817-1828. (Pubitemid 24265787)
23. Fortes P, Beloso A, Ortin J. Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J 1994; 13: 704-712. (Pubitemid 24050686)
24. 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.
25. Wang M, Marin A. Characterization and prediction of alternative splice sites. Gene 2006; 366: 219-227. (Pubitemid 43230165)
26. 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. (Pubitemid 30047754)
27. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14: 1188-1190. (Pubitemid 38811555)
28. Bao Y, Bolotov P, Dernovoy D et al. The influenza virus resource at the National Center for Biotechnology Information. J Virol 2008; 82: 596-601.
29. 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. Bioinformatics 2012; 28: 1647-1649.
30. Martins R, Silva B, Proenca D, Faustino P. Differential HFE gene expression is regulated by alternative splicing in human tissues. PLoS One 2011; 6: e17542.
31. Ast G. How did alternative splicing evolve? Nat Rev Genet 2004; 5: 773-782. (Pubitemid 39336361)
32. Carmel I, Tal S, Vig I, Ast G. Comparative analysis detects dependencies among the 59 splice-site positions. RNA 2004; 10: 828-840. (Pubitemid 38529746)
33. 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. Virology 2006; 349: 13-21.
34. 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. Virology 2007; 363: 236-243. (Pubitemid 46678175)
35. Chen Z, Li Y, Krug RM. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 39-end processing machinery. EMBO J 1999; 18: 2273-2283. (Pubitemid 29179183)
36. 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 Cell 1998; 1: 991-1000. (Pubitemid 128379260)
37. 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 USA 1998; 95: 4864-4869. (Pubitemid 28208516)
38. Bornholdt ZA, Prasad BV. X-ray structure of NS1 from a highly pathogenic H5N1 influenza virus. Nature 2008; 456: 985-988.
39. Bornholdt ZA, Prasad BV. X-ray structure of influenza virus NS1 effector domain. Nat Struct Mol Biol 2006; 13: 559-560. (Pubitemid 43848913)
40. Song D, Kang B, Lee C et al. Transmission of avian influenza virus (H3N2) to dogs. Emerg Infect Dis 2008; 14: 741-746. (Pubitemid 351838637)
41. 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 Infect 2009; 11: 2-11.
42. 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 USA 2000; 97: 9654-9658. (Pubitemid 30650831)
43. 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 USA 1999; 96: 9363-9367. (Pubitemid 29374760)
44. 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 Virol 2000; 74: 9372-9380.
45. Li S, Shi Z, Jiao P et al. Avian-origin H3N2 canine influenza A viruses in Southern China. Infect Genet Evol 2010; 10: 1286-1288.
46. 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 Microbiol 2012; 158: 247-258.
47. Simulundu E, Ishii A, IgarashiMet al. Characterization of influenza A viruses isolated from wild waterfowl in Zambia. J Gen Virol 2011; 92(Pt 6): 1416-1427.
48. 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 One 2011; 6: e17730.
49. Shih SR, Suen PC, Chen YS, Chang SC. A novel spliced transcript of influenza A/WSN/ 33 virus. Virus Genes 1998; 17: 179-183.
50. Shih SR, Nemeroff ME, Krug RM. The choice of alternative 59 splice sites in influenza virusM1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci USA 1995; 92: 6324-6328.
51. Jackson D, Lamb RA. The influenza A virus spliced messenger RNA M mRNA3 is not required for viral replication in tissue culture. J Gen Virol 2008; 89(Pt 12): 3097-3101.
52. Chiang C, Chen GW, Shih SR. Mutations at alternative 59 splice sites of M1 mRNA negatively affect influenza A virus viability and growth rate. J Virol. 2008; 82: 10873-10886. (Pubitemid 352691202)
53. Perdue ML. Naturally occurring NS gene variants in an avian influenza virus isolate. Virus Res 1992; 23: 223-240.
54. 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. Vaccine 2008; 26: 3580-3586.
55. Dundon WG. Variability among the neuraminidase, non-structural 1 and PB1-F2 proteins in the influenza A virus genome. Virus Genes 2012; 44: 363-373.
56. Richt JA, Garcia-Sastre A. Attenuated influenza virus vaccines with modified NS1 proteins. Curr Top Microbiol Immunol 2009; 333: 177-195.
57. 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 Virol 2010; 91(Pt 7): 1754-1763.
58. Chen W, Calvo PA, Malide D et al. A novel influenza A virusmitochondrial protein that induces cell death. Nat Med 2001; 7: 1306-1312. (Pubitemid 34007934)
59. Jagger BW, Wise HM, Kash JC et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012; 337: 199-204.