Multifunctional adaptive NS1 mutations are selected upon human influenza virus evolution in the mouse

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Forbes, Nicole E ^a   Ping, Jihui ^a   Dankar, Samar K ^a   Jia, Jian Jun ^a   Selman, Mohammed ^a   Keleta, Liya ^a   Zhou, Yan ^a,b   Brown, Earl G ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; NONSTRUCTURAL PROTEIN 1; INS1 PROTEIN, INFLUENZA VIRUS; MESSENGER RNA; MUTANT PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME SYNTHESIS; FEMALE; GENE MUTATION; INFLUENZA VIRUS A; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYADENYLATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN FUNCTION; REVERSE GENETICS; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; SURVIVAL; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; WEIGHT REDUCTION; WILD TYPE; ADAPTATION; ANIMAL; BIOASSAY; BIOSYNTHESIS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HALF LIFE TIME; HOST RANGE; HUMAN; INFLUENZA; LUNG; METABOLISM; MOLECULAR GENETICS; MUTATION; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PROTEIN SYNTHESIS; VIROLOGY; VIRULENCE;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL ASSAY; GENE EXPRESSION REGULATION, VIRAL; HALF-LIFE; HOST SPECIFICITY; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; INTERFERON-BETA; LUNG; MICE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RECOMBINATION, GENETIC; RNA, MESSENGER; SELECTION, GENETIC; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE;

EID: 84857425220     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031839     Document Type: Article

References (65)

1. Guan Y, Peiris JS, Lipatov AS, Ellis TM, Dyrting KC, et al. (2002) Emergence of multiple genotypes of H5N1 avian influenza viruses in hong kong SAR. Proc Natl Acad Sci U S A 99 (13): 8950-8955.
2. Webster RG, Hulse-Post DJ, Sturm-Ramirez KM, Guan Y, Peiris M, et al. (2007) Changing epidemiology and ecology of highly pathogenic avian H5N1 influenza viruses. Avian Dis 51 (1 Suppl): 269-272.
3. World Health Organization. (2011) Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003-2011. 2011(17 October, 2011).
4. Taubenberger JK, Kash JC, (2010) Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7 (6): 440-451.
5. Ping J, Keleta L, Forbes NE, Dankar S, Stecho W, et al. (2011) Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS One 6 (6): e21740.
6. Li Z, Jiang Y, Jiao P, Wang A, Zhao F, et al. (2006) The NS1 gene contributes to the virulence of H5N1 avian influenza viruses. J Virol 80 (22): 11115-11123.
7. Dankar SK, Wang S, Ping J, Forbes NE, Keleta L, et al. (2011) Influenza A virus NS1 gene mutations F103L and M106I increase replication and virulence. Virol J 8 (1): 13.
8. Long JX, Peng DX, Liu YL, Wu YT, Liu XF, (2008) Virulence of H5N1 avian influenza virus enhanced by a 15-nucleotide deletion in the viral nonstructural gene. Virus Genes 36 (3): 471-478.
9. Seo SH, Hoffmann E, Webster RG, (2002) Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8 (9): 950-954.
10. Hale BG, Randall RE, Ortin J, Jackson D, (2008) The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89 (Pt 10): 2359-2376.
11. Guo Z, Chen LM, Zeng H, Gomez JA, Plowden J, et al. (2007) NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am J Respir Cell Mol Biol 36 (3): 263-269.
12. Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M Jr, et al. (2007) Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 81 (2): 514-524.
13. Opitz B, Rejaibi A, Dauber B, Eckhard J, Vinzing M, et al. (2007) IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell Microbiol 9 (4): 930-938.
14. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, et al. (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5 (5): 439-449.
15. Jia D, Rahbar R, Chan RW, Lee SM, Chan MC, et al. (2010) Influenza virus non-structural protein 1 (NS1) disrupts interferon signaling. PLoS One 5 (11): e13927.
16. Kochs G, Garcia-Sastre A, Martinez-Sobrido L, (2007) Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81 (13): 7011-7021.
17. Nemeroff ME, Barabino SM, Li Y, Keller W, Krug RM, (1998) Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3′end formation of cellular pre-mRNAs. Mol Cell 1 (7): 991-1000.
18. Noah DL, Twu KY, Krug RM, (2003) Cellular antiviral responses against influenza A virus are countered at the posttranscriptional level by the viral NS1A protein via its binding to a cellular protein required for the 3′ end processing of cellular pre-mRNAS. Virology 307 (2): 386-395.
19. Chen Z, Li Y, Krug RM, (1999) Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J 18 (8): 2273-2283.
20. Satterly N, Tsai PL, van Deursen J, Nussenzveig DR, Wang Y, et al. (2007) Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104 (6): 1853-1858.
21. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, et al. (2006) Impact of protein kinase PKR in cell biology: From antiviral to antiproliferative action. Microbiol Mol Biol Rev 70 (4): 1032-1060.
22. Li S, Min JY, Krug RM, Sen GC, (2006) Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349 (1): 13-21.
23. Min JY, Li S, Sen GC, Krug RM, (2007) A site on the influenza A virus NS1 protein mediates both inhibition of PKR activation and temporal regulation of viral RNA synthesis. Virology 363 (1): 236-243.
24. Robb NC, Fodor E, (2011) The accumulation of influenza A virus segment 7 spliced mRNAs is regulated by the NS1 protein. J Gen Virol.
25. Robb NC, Jackson D, Vreede FT, Fodor E, (2010) Splicing of influenza A virus NS1 mRNA is independent of the viral NS1 protein. J Gen Virol 91 (Pt 9): 2331-2340.
26. Lu Y, Qian XY, Krug RM, (1994) The influenza virus NS1 protein: A novel inhibitor of pre-mRNA splicing. Genes Dev 8 (15): 1817-1828.
27. Fortes P, Beloso A, Ortin J, (1994) Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J 13 (3): 704-712.
28. Garaigorta U, Ortin J, (2007) Mutation analysis of a recombinant NS replicon shows that influenza virus NS1 protein blocks the splicing and nucleo-cytoplasmic transport of its own viral mRNA. Nucleic Acids Res 35 (14): 4573-4582.
29. Marion RM, Zurcher T, de la Luna S, Ortin J, (1997) Influenza virus NS1 protein interacts with viral transcription-replication complexes in vivo. J Gen Virol 78 (Pt 10) (Pt 10): 2447-2451.
30. Robb NC, Chase G, Bier K, Vreede FT, Shaw PC, et al. (2011) The influenza A virus NS1 protein interacts with the nucleoprotein of viral ribonucleoprotein complexes. J Virol 85 (10): 5228-5231.
31. Lee JH, Kim SH, Pascua PN, Song MS, Baek YH, et al. (2010) Direct interaction of cellular hnRNP-F and NS1 of influenza A virus accelerates viral replication by modulation of viral transcriptional activity and host gene expression. Virology 397 (1): 89-99.
32. Falcon AM, Marion RM, Zurcher T, Gomez P, Portela A, et al. (2004) Defective RNA replication and late gene expression in temperature-sensitive influenza viruses expressing deleted forms of the NS1 protein. J Virol 78 (8): 3880-3888.
33. Wang Z, Robb NC, Lenz E, Wolff T, Fodor E, et al. (2010) NS reassortment of an H7-type highly pathogenic avian influenza virus affects its propagation by altering the regulation of viral RNA production and antiviral host response. J Virol 84 (21): 11323-11335.
34. Kuo RL, Krug RM, (2009) Influenza a virus polymerase is an integral component of the CPSF30-NS1A protein complex in infected cells. J Virol 83 (4): 1611-1616.
35. Aragon T, de la Luna S, Novoa I, Carrasco L, Ortin J, et al. (2000) Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol Cell Biol 20 (17): 6259-6268.
36. Burgui I, Aragon T, Ortin J, Nieto A, (2003) PABP1 and eIF4GI associate with influenza virus NS1 protein in viral mRNA translation initiation complexes. J Gen Virol 84 (Pt 12): 3263-3274.
37. Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, et al. (2004) H5N1 influenza: A protean pandemic threat. Proc Natl Acad Sci U S A 101 (21): 8156-8161.
38. Li KS, Guan Y, Wang J, Smith GJ, Xu KM, et al. (2004) Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern asia. Nature 430 (6996): 209-213.
39. Jiao P, Tian G, Li Y, Deng G, Jiang Y, et al. (2008) A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 82 (3): 1146-1154.
40. Brown EG, (1990) Increased virulence of a mouse-adapted variant of influenza A/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol 64 (9): 4523-4533.
41. Brown EG, Bailly JE, (1999) Genetic analysis of mouse-adapted influenza A virus identifies roles for the NA, PB1, and PB2 genes in virulence. Virus Res 61 (1): 63-76.
42. Brown EG, Liu H, Kit LC, Baird S, Nesrallah M, (2001) 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 U S A 98 (12): 6883-6888.
43. Ilyushina NA, Khalenkov AM, Seiler JP, Forrest HL, Bovin NV, et al. (2010) Adaptation of pandemic H1N1 influenza viruses in mice. J Virol 84 (17): 8607-8616.
44. Narasaraju T, Sim MK, Ng HH, Phoon MC, Shanker N, et al. (2009) Adaptation of human influenza H3N2 virus in a mouse pneumonitis model: Insights into viral virulence, tissue tropism and host pathogenesis. Microbes Infect 11 (1): 2-11.
45. Keleta L, Ibricevic A, Bovin NV, Brody SL, Brown EG, (2008) Experimental evolution of human influenza virus H3 hemagglutinin in the mouse lung identifies adaptive regions in HA1 and HA2. J Virol 82 (23): 11599-11608.
46. Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, et al. (2010) PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol 84 (20): 10606-10618.
47. Steidle S, Martinez-Sobrido L, Mordstein M, Lienenklaus S, Garcia-Sastre A, et al. (2010) Glycine 184 in nonstructural protein NS1 determines the virulence of influenza A virus strain PR8 without affecting the host interferon response. J Virol 84 (24): 12761-12770.
48. Hale BG, Steel J, Medina RA, Manicassamy B, Ye J, et al. (2010) Inefficient control of host gene expression by the 2009 pandemic H1N1 influenza A virus NS1 protein. J Virol 84 (14): 6909-6922.
49. Bouloy M, Plotch SJ, Krug RM, (1978) Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. Proc Natl Acad Sci U S A 75 (10): 4886-4890.
50. Watanabe T, Watanabe S, Kawaoka Y, (2010) Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 7 (6): 427-439.
51. Akarsu H, Burmeister WP, Petosa C, Petit I, Muller CW, et al. (2003) Crystal structure of the M1 protein-binding domain of the influenza A virus nuclear export protein (NEP/NS2). EMBO J 22 (18): 4646-4655.
52. Lamb RA, Lai CJ, Choppin PW, (1981) Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: Colinear and interrupted mRNAs code for overlapping proteins. Proc Natl Acad Sci U S A 78 (7): 4170-4174.
53. Lamb RA, Choppin PW, Chanock RM, Lai CJ, (1980) Mapping of the two overlapping genes for polypeptides NS1 and NS2 on RNA segment 8 of influenza virus genome. Proc Natl Acad Sci U S A 77 (4): 1857-1861.
54. Shimizu T, Takizawa N, Watanabe K, Nagata K, Kobayashi N, (2011) Crucial role of the influenza virus NS2 (NEP) C-terminal domain in M1 binding and nuclear export of vRNP. FEBS Lett 585 (1): 41-46.
55. Robb NC, Smith M, Vreede FT, Fodor E, (2009) NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J Gen Virol 90 (Pt 6): 1398-1407.
56. Perez JT, Varble A, Sachidanandam R, Zlatev I, Manoharan M, et al. (2010) Influenza A virus-generated small RNAs regulate the switch from transcription to replication. Proc Natl Acad Sci U S A 107 (25): 11525-11530.
57. Hossain MJ, Hickman D, Perez DR, (2008) Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS ONE 3 (9): e3170 doi:10.1371/journal.pone.0003170.
58. Reid AH, Fanning TG, Hultin JV, Taubenberger JK, (1999) Origin and evolution of the 1918 "spanish" influenza virus hemagglutinin gene. Proc Natl Acad Sci U S A 96 (4): 1651-1656.
59. Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, et al. (2009) Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc Natl Acad Sci U S A 106 (9): 3455-3460.
60. Meunier I, von Messling V, (2011) NS1-mediated delay of type I interferon induction contributes to influenza A virulence in ferrets. J Gen Virol 92 (Pt 7): 1635-1644.
61. Liu Q, Wang S, Ma G, Pu J, Forbes NE, et al. (2009) Improved and simplified recombineering approach for influenza virus reverse genetics. J Mol Genet Med 3 (2): 225-231.
62. Li Z, Chen H, Jiao P, Deng G, Tian G, et al. (2005) Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79 (18): 12058-12064.
63. Ping J, Li C, Deng G, Jiang Y, Tian G, et al. (2008) Single-amino-acid mutation in the HA alters the recognition of H9N2 influenza virus by a monoclonal antibody. Biochem Biophys Res Commun 371 (1): 168-171.
64. Miller J, Ulrich R, (2004) A computer program for spearman-karber and probit analysis of psychometric function data. Behav Res Methods Instrum Comput 36 (1): 11-16.
65. Ma W, Brenner D, Wang Z, Dauber B, Ehrhardt C, et al. (2010) The NS segment of an H5N1 highly pathogenic avian influenza virus (HPAIV) is sufficient to alter replication efficiency, cell tropism, and host range of an H7N1 HPAIV. J Virol 84 (4): 2122-2133.