The role of nuclear NS1 protein in highly pathogenic H5N1 influenza viruses

Microbes and Infection

Volumn 19, Issue 12, 2017, Pages 587-596

  Mok, Bobo Wing Yee ^a   Liu, Honglian ^a   Chen, Pin ^a   Liu, Siwen ^a   Lau, Siu Ying ^a   Huang, Xiaofeng ^a   Liu, Yen Chin ^a   Wang, Pui ^a   Yuen, Kwok Yung ^a   Chen, Honglin ^a  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

H5N1; HPAI; Influenza virus; NS1; Nuclear localization signal

Indexed keywords

NONSTRUCTURAL PROTEIN 1; INS1 PROTEIN, INFLUENZA VIRUS; VIRAL PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; HIGHLY PATHOGENIC AVIAN INFLUENZA; HUMAN; HUMAN CELL; INFLUENZA A VIRUS (H5N1); INFLUENZA A VIRUS (H7N9); MUTATION; NONSENSE MUTATION; PATHOGENESIS; PRIORITY JOURNAL; VIRUS REPLICATION; A-549 CELL LINE; ANIMAL; BAGG ALBINO MOUSE; CELL NUCLEUS; DOG; FEMALE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS (H1N1); MDCK CELL LINE; METABOLISM; MOUSE; NUCLEAR LOCALIZATION SIGNAL; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PROTEIN DOMAIN; TUMOR CELL LINE; VIROLOGY;

A549 CELLS; ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; DOGS; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICE, INBRED BALB C; MUTATION; NUCLEAR LOCALIZATION SIGNALS; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN DOMAINS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 85029705012     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2017.08.011     Document Type: Article

References (50)

1. Tumpey, T.M., Basler, C.F., Aguilar, P.V., Zeng, H., Solorzano, A., Swayne, D.E., et al. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310 (2005), 77–80.
2. Hatta, M., Gao, P., Halfmann, P., Kawaoka, Y., Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293 (2001), 1840–1842.
3. Gabriel, G., Herwig, A., Klenk, H.D., Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog, 4, 2008, e11.
4. Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N., Kawaoka, Y., Avian flu: influenza virus receptors in the human airway. Nature 440 (2006), 435–436.
5. Hale, B.G., Randall, R.E., Ortin, J., Jackson, D., The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89 (2008), 2359–2376.
6. Kochs, G., Garcia-Sastre, A., Martinez-Sobrido, L., Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81 (2007), 7011–7021.
7. Cheng, T.F., Brzostek, S., Ando, O., Van Scoy, S., Kumar, K.P., Reich, N.C., Differential activation of IFN regulatory factor (IRF)-3 and IRF-5 transcription factors during viral infection. J Immunol 176 (2006), 7462–7470.
8. Chou, Y.T., Tam, B., Linay, F., Lai, E.C., Transgenic inhibitors of RNA interference in Drosophila. Fly (Austin) 1 (2007), 311–316.
9. Silverman, R.H., Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81 (2007), 12720–12729.
10. Garcia, M.A., Gil, J., Ventoso, I., Guerra, S., Domingo, E., Rivas, C., et al. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70 (2006), 1032–1060.
11. Hale, B.G., Kerry, P.S., Jackson, D., Precious, B.L., Gray, A., Killip, M.J., et al. Structural insights into phosphoinositide 3-kinase activation by the influenza A virus NS1 protein. Proc Natl Acad Sci U S A 107 (2010), 1954–1959.
12. Hale, B.G., Jackson, D., Chen, Y.H., Lamb, R.A., Randall, R.E., Influenza A virus NS1 protein binds p85beta and activates phosphatidylinositol-3-kinase signaling. Proc Natl Acad Sci U S A 103 (2006), 14194–14199.
13. Aragon, T., de la Luna, S., Novoa, I., Carrasco, L., Ortin, J., Nieto, A., Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol Cell Biol 20 (2000), 6259–6268.
14. Mok, B.W., Song, W., Wang, P., Tai, H., Chen, Y., Zheng, M., et al. The NS1 protein of influenza A virus interacts with cellular processing bodies and stress granules through RNA-associated protein 55 (RAP55) during virus infection. J Virol 86 (2012), 12695–12707.
15. Thulasi Raman, S.N., Liu, G., Pyo, H.M., Cui, Y.C., Xu, F., Ayalew, L.E., et al. DDX3 interacts with influenza a virus NS1 and NP proteins and exerts antiviral function through regulation of stress granule formation. J Virol 90 (2016), 3661–3675.
16. Wen, X., Huang, X., Mok, B.W., Chen, Y., Zheng, M., Lau, S.Y., et al. NF90 exerts antiviral activity through regulation of PKR phosphorylation and stress granules in infected cells. J Immunol 192 (2014), 3753–3764.
17. Chen, Z., Li, Y., Krug, R.M., Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J 18 (1999), 2273–2283.
18. Nemeroff, M.E., Barabino, S.M., Li, Y., Keller, W., Krug, R.M., 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 (1998), 991–1000.
19. Satterly, N., Tsai, P.L., van Deursen, J., Nussenzveig, D.R., Wang, Y., Faria, P.A., et al. Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104 (2007), 1853–1858.
20. Qian, X.Y., Alonso-Caplen, F., Krug, R.M., Two functional domains of the influenza virus NS1 protein are required for regulation of nuclear export of mRNA. J Virol 68 (1994), 2433–2441.
21. Marazzi, I., Ho, J.S., Kim, J., Manicassamy, B., Dewell, S., Albrecht, R.A., et al. Suppression of the antiviral response by an influenza histone mimic. Nature 483 (2012), 428–433.
22. Chen, G., Liu, C.H., Zhou, L., Krug, R.M., Cellular DDX21 RNA helicase inhibits influenza A virus replication but is counteracted by the viral NS1 protein. Cell Host Microbe 15 (2014), 484–493.
23. Pichlmair, A., Kandasamy, K., Alvisi, G., Mulhern, O., Sacco, R., Habjan, M., et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 487 (2012), 486–490.
24. Greenspan, D., Palese, P., Krystal, M., Two nuclear location signals in the influenza virus NS1 nonstructural protein. J Virol 62 (1988), 3020–3026.
25. Tonnessen, R., Hauge, A.G., Hansen, E.F., Rimstad, E., Jonassen, C.M., Host restrictions of avian influenza viruses: in silico analysis of h13 and h16 specific signatures in the internal proteins. PLoS One, 8, 2013, e63270.
26. Parvin, J.D., Young, J.F., Palese, P., Nonsense mutations affecting the lengths of the NS1 nonstructural proteins of influenza A virus isolates. Virology 128 (1983), 512–517.
27. Snyder, M.H., Buckler-White, A.J., London, W.T., Tierney, E.L., Murphy, B.R., The avian influenza virus nucleoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian-human influenza A/Pintail/79 reassortant viruses for monkeys. J Virol 61 (1987), 2857–2863.
28. Soubies, S.M., Volmer, C., Croville, G., Loupias, J., Peralta, B., Costes, P., et al. Species-specific contribution of the four C-terminal amino acids of influenza A virus NS1 protein to virulence. J Virol 84 (2010), 6733–6747.
29. Alfonso, R., Lutz, T., Rodriguez, A., Chavez, J.P., Rodriguez, P., Gutierrez, S., et al. CHD6 chromatin remodeler is a negative modulator of influenza virus replication that relocates to inactive chromatin upon infection. Cell Microbiol 13 (2011), 1894–1906.
30. Hoffmann, E., Krauss, S., Perez, D., Webby, R., Webster, R.G., Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 20 (2002), 3165–3170.
31. Zheng, M., Wang, P., Song, W., Lau, S.Y., Liu, S., Huang, X., et al. An A14U substitution in the 3′ noncoding region of the M segment of viral RNA supports replication of influenza virus with an NS1 deletion by modulating alternative splicing of M segment mRNAs. J Virol 89 (2015), 10273–10285.
32. Chen, Y., Qin, K., Wu, W.L., Li, G., Zhang, J., Du, H., et al. Broad cross-protection against H5N1 avian influenza virus infection by means of monoclonal antibodies that map to conserved viral epitopes. J Infect Dis 199 (2009), 49–58.
33. The top 10 health stories of 2009. Harv Health Lett 35 (2009), 1–4.
34. Wang, W., Riedel, K., Lynch, P., Chien, C.Y., Montelione, G.T., Krug, R.M., RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. RNA 5 (1999), 195–205.
35. Li, Y., Yamakita, Y., Krug, R.M., Regulation of a nuclear export signal by an adjacent inhibitory sequence: the effector domain of the influenza virus NS1 protein. Proc Natl Acad Sci U S A 95 (1998), 4864–4869.
36. Chen, Y., Liang, W., Yang, S., Wu, N., Gao, H., Sheng, J., et al. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381 (2013), 1916–1925.
37. Fouchier, R.A., Schneeberger, P.M., Rozendaal, F.W., Broekman, J.M., Kemink, S.A., Munster, V., et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101 (2004), 1356–1361.
38. Yuen, K.Y., Chan, P.K., Peiris, M., Tsang, D.N., Que, T.L., Shortridge, K.F., et al. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351 (1998), 467–471.
39. Zhang, Y., Liu, J., Yu, L., Zhou, N., Ding, W., Zheng, S., et al. Prevalence and characteristics of hypoxic hepatitis in the largest single-centre cohort of avian influenza A(H7N9) virus-infected patients with severe liver impairment in the intensive care unit. Emerg Microbes Infect, 5, 2016, e1.
40. Imai, H., Shinya, K., Takano, R., Kiso, M., Muramoto, Y., Sakabe, S., et al. The HA and NS genes of human H5N1 influenza A virus contribute to high virulence in ferrets. PLoS Pathog, 6, 2010.
41. Basler, C.F., Reid, A.H., Dybing, J.K., Janczewski, T.A., Fanning, T.G., Zheng, H., et al. Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proc Natl Acad Sci U S A 98 (2001), 2746–2751.
42. Li, X., Chiang, H.I., Zhu, J., Dowd, S.E., Zhou, H., Characterization of a newly developed chicken 44K Agilent microarray. BMC Genom, 9, 2008, 60.
43. Seo, S.H., Hoffmann, E., Webster, R.G., Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8 (2002), 950–954.
44. Egorov, A., Brandt, S., Sereinig, S., Romanova, J., Ferko, B., Katinger, D., et al. Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J Virol 72 (1998), 6437–6441.
45. Garcia-Sastre, A., Egorov, A., Matassov, D., Brandt, S., Levy, D.E., Durbin, J.E., et al. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252 (1998), 324–330.
46. Bornholdt, Z.A., Prasad, B.V., X-ray structure of influenza virus NS1 effector domain. Nat Struct Mol Biol 13 (2006), 559–560.
47. Marcos-Villar, L., Pazo, A., Nieto, A., Influenza virus and chromatin: role of the CHD1 chromatin remodeler in the virus life cycle. J Virol 90 (2016), 3694–3707.
48. Ludwig, S., Schultz, U., Mandler, J., Fitch, W.M., Scholtissek, C., Phylogenetic relationship of the nonstructural (NS) genes of influenza A viruses. Virology 183 (1991), 566–577.
49. Guan, Y., Shortridge, K.F., Krauss, S., Webster, R.G., Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong?. Proc Natl Acad Sci U S A 96 (1999), 9363–9367.
50. Li, J., Yu, X., Pu, X., Yang, X., Kou, Y., Zhou, Y., et al. The diversity of avian influenza virus subtypes in live poultry markets before and during the second wave of A(H7N9) infections in Hangzhou. China Emerg Microbes Infect, 4, 2015, e14.