The NS1 gene from bat-derived influenza-like virus H17N10 can be rescued in influenza A PR8 backbone

Journal of General Virology

Volumn 97, Issue 8, 2016, Pages 1797-1806

  Zhao, Xuejin ^a,b   Tefsen, Boris ^a,b,c   Li, Yan ^a,b   Qi, Jianxun ^a,b   Lu, Guangwen ^a,b   Shi, Yi ^b   Yan, Jinghua ^a   Xiao, Haixia ^b,d   Gao, George F ^a,b,d,e  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c XI AN JIAOTONG LIVERPOOL UNIVERSITY   (China)

^d Tianjin Airport Economic Area   (China)

^e CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Bat derived; H17N10; Influenza like virus; NEP protein; NS1 protein; Reverse genetics

Indexed keywords

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

ARTICLE; BAT; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOKINE PRODUCTION; GENETIC REASSORTMENT; HEK293 CELL LINE; INFLUENZA A VIRUS; INFLUENZA A VIRUS (A/PUERTO RICO/8/1934(H1N1)); INFLUENZA A VIRUS (H5N1); INFLUENZA VIRUS (H17N10); LUCIFERASE ASSAY; MDCK CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; SENDAI VIRUS; VIRUS GENE; VIRUS STRAIN; ANIMAL; CELL LINE; CHEMISTRY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR MODEL; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; PROTEIN CONFORMATION; REVERSE GENETICS; VETERINARY; VIROLOGY; VIRUS REPLICATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; CELL LINE; CHIROPTERA; CRYSTALLOGRAPHY, X-RAY; HUMANS; INFLUENZA A VIRUS; MODELS, MOLECULAR; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN CONFORMATION; REASSORTANT VIRUSES; REVERSE GENETICS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84985986985     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000509     Document Type: Article

References (46)

1. Akarsu, H., Burmeister, W. P., Petosa, C., Petit, I., Müller, C. W., Ruigrok, R. W. & Baudin, F. (2003). Crystal structure of the M1 proteinbinding domain of the influenza A virus nuclear export protein (NEP/NS2). EMBO J 22, 4646–4655.
2. Basler, C. F., Reid, A. H., Dybing, J. K., Janczewski, T. A., Fanning, T. G., Zheng, H., Salvatore, M., Perdue, M. L., Swayne, D. E. & other authors (2001). 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, 2746–2751.
3. Bornholdt, Z. A. & Prasad, B. V. (2006). X-ray structure of influenza virus NS1 effector domain. Nat Struct Mol Biol 13, 559–560.
4. Bornholdt, Z. A. & Prasad, B. V. (2008). X-ray structure of NS1 from a highly pathogenic H5N1 influenza virus. Nature 456, 985–988.
5. Chen, Z., Li, Y. & Krug, R. M. (1999). Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J 18, 2273–2283.
6. Desselberger, U., Racaniello, V. R., Zazra, J. J. & Palese, P. (1980). The 3′ and 5′-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8, 315–328.
7. Donelan, N. R., Basler, C. F. & García-Sastre, A. (2003). A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J Virol 77, 13257–13266.
8. Gack, M. U., Albrecht, R. A., Urano, T., Inn, K. S., Huang, I. C., Carnero, E., Farzan, M., Inoue, S., Jung, J. U. & García-Sastre, A. (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, 439–449.
9. Gao, R., Cao, B., Hu, Y., Feng, Z., Wang, D., Hu, W., Chen, J., Jie, Z., Qiu, H. & other authors (2013). Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368, 1888–1897.
10. García-Sastre, A., Egorov, A., Matassov, D., Brandt, S., Levy, D. E., Durbin, J. E., Palese, P. & Muster, T. (1998). Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252, 324–330.
11. Hale, B. G., Randall, R. E., Ortín, J. & Jackson, D. (2008). The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89, 2359–2376.
12. Heaton, N. S., Sachs, D., Chen, C. -J., Hai, R. & Palese, P. (2013). Genome-wide mutagenesis of influenza virus reveals unique plasticity of the hemagglutinin and NS1 proteins. Proc Natl Acad Sci U S A 110, 20248–20253.
13. Hoffmann, E., Neumann, G., Kawaoka, Y., Hobom, G. & Webster, R. G. (2000). A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97, 6108–6113.
14. Jackson, D., Hossain, M. J., Hickman, D., Perez, D. R. & Lamb, R. A. (2008). A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci U S A 105, 4381–4386.
15. Juozapaitis, M., Aguiar Moreira, É., Mena, I., Giese, S., Riegger, D., Pohlmann, A., Höper, D., Zimmer, G., Beer, M. & other authors (2014). An infectious bat-derived chimeric influenza virus harbouring the entry machinery of an influenza A virus. Nat Commun 5, 4448.
16. Li, J., Yu, X., Pu, X., Xie, L., Sun, Y., Xiao, H., Wang, F., Din, H., Wu, Y. & other authors (2013). Environmental connections of novel avian-origin H7N9 influenza virus infection and virus adaptation to the human. Sci China Life Sci 56, 485–492.
17. Li, Q., Sun, X., Li, Z., Liu, Y., Vavricka, C. J., Qi, J. & Gao, G. F. (2012). Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus. Proc Natl Acad Sci U S A 109, 18897–18902.
18. Li, S., Min, J. Y., Krug, R. M. & Sen, G. C. (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, 13–21.
19. Li, Y., Yamakita, Y. & Krug, R. M. (1998). 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, 4864–4869.
20. Liu, D., Shi, W., Shi, Y., Wang, D., Xiao, H., Li, W., Bi, Y., Wu, Y., Li, X. & other authors (2013). Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381, 1926–1932.
21. Liu, J., Lynch, P. A., Chien, C. Y., Montelione, G. T., Krug, R. M. & Berman, H. M. (1997). Crystal structure of the unique RNA-binding domain of the influenza virus NS1 protein. Nat Struct Biol 4, 896–899.
22. Luis, A. D., Hayman, D. T. S., O’Shea, T. J., Cryan, P. M., Gilbert, A. T., Pulliam, J. R. C., Mills, J. N., Timonin, M. E., Willis, C. K. R. & other authors (2013). A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc Biol Sci 280, 1756.
23. Min, J. Y. & Krug, R. M. (2006). The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: inhibiting the 2′-5′ oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci U S A 103, 7100–7105.
24. Min, J. Y., Li, S., Sen, G. C. & Krug, R. M. (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, 236–243.
25. Neumann, G., Hughes, M. T. & Kawaoka, Y. (2000). Influenza A virus NS2 protein mediates vRNP nuclear export through NES-independent interaction with hCRM1. EMBO J 19, 6751–6758.
26. Paterson, D. & Fodor, E. (2012). Emerging roles for the influenza A virus nuclear export protein (NEP). PLoS Pathog 8, e1003019.
27. Pflug, A., Guilligay, D., Reich, S. & Cusack, S. (2014). Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516, 355–360.
28. Qian, X. Y., Chien, C. Y., Lu, Y., Montelione, G. T. & Krug, R. M. (1995). An amino-terminal polypeptide fragment of the influenza virus NS1 protein possesses specific RNA-binding activity and largely helical backbone structure. RNA 1, 948–956.
29. Rajsbaum, R., Albrecht, R. A., Wang, M. K., Maharaj, N. P., Versteeg, G. A., Nistal-Villàn, E., García-Sastre, A. & Gack, M. U. (2012). Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog 8, e1003059.
30. Shi, Y., Wu, Y., Zhang, W., Qi, J. & Gao, G. F. (2014). Enabling the ‘host jump’: structural determinants of receptor-binding specificity in influenza A viruses. Nat Rev Microbiol 12, 822–831.
31. Shi, Z. (2010). Bat and virus. Protein Cell 1, 109–114.
32. Soubies, S. M., Volmer, C., Croville, G., Loupias, J., Peralta, B., Costes, P., Lacroux, C., Guèrin, J. L. & Volmer, R. (2010). Species-specific contribution of the four C-terminal amino acids of influenza A virus NS1 protein to virulence. J Virol 84, 6733–6747.
33. Sun, X., Shi, Y., Lu, X., He, J., Gao, F., Yan, J., Qi, J. & Gao, G. F. (2013). Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep 3, 769–778.
34. Tan, S. L. & Katze, M. G. (1998). Biochemical and genetic evidence for complex formation between the influenza A virus NS1 protein and the interferon-induced PKR protein kinase. J Interferon Cytokine Res 18, 757–766.
35. Tefsen, B., Lu, G., Zhu, Y., Haywood, J., Zhao, L., Deng, T., Qi, J. & Gao, G. F. (2013). The N-terminal domain of PA from bat-derived influenza- like virus H17N10 has endonuclease activity. J Virol 88, 1935–1941.
36. Tiley, L. S., Hagen, M., Matthews, J. T. & Krystal, M. (1994). Sequencespecific binding of the influenza virus RNA polymerase to sequences located at the 5′ ends of the viral RNAs. J Virol 68, 5108–5116.
37. Tong, S., Li, Y., Rivailler, P., Conrardy, C., Castillo, D. A., Chen, L. M., Recuenco, S., Ellison, J. A., Davis, C. T. & other authors (2012). A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A 109, 4269–4274.
38. Tong, S., Zhu, X., Li, Y., Shi, M., Zhang, J., Bourgeois, M., Yang, H., Chen, X., Recuenco, S. & other authors (2013). New World bats harbor diverse influenza A viruses. PLoS Pathog 9, e1003657.
39. Turkington, H. L., Juozapaitis, M., Kerry, P. S., Aydillo, T., Ayllon, J., García-Sastre, A., Schwemmle, M. & Hale, B. G. (2015). Novel bat influenza virus NS1 proteins bind double-stranded RNA and antagonize host innate immunity. J Virol 89, 10696–10701.
40. Wu, A., Su, C., Wang, D., Peng, Y., Liu, M., Hua, S., Li, T., Gao, G. F., Tang, H. & other authors (2013). Sequential reassortments underlie diverse influenza H7N9 genotypes in China. Cell Host Microbe 14, 446–452.
41. Wu, Y. & Gao, G. F. (2013). Lessons learnt from the human infections of avian-origin influenza A H7N9 virus: live free markets and human health. Sci China Life Sci 56, 493–494.
42. Wu, Y., Wu, Y., Tefsen, B., Shi, Y. & Gao, G. F. (2014). Bat-derived influenza- like viruses H17N10 and H18N11. Trends Microbiol 22, 183–191.
43. Zheng, H., Palese, P. & García-Sastre, A. (1996). Nonconserved nucleotides at the 3′ and 5′ ends of an influenza A virus RNA play an important role in viral RNA replication. Virology 217, 242–251.
44. Zhou, B., Ma, J., Liu, Q., Bawa, B., Wang, W., Shabman, R. S., Duff, M., Lee, J., Lang, Y. & other authors (2014). Characterization of uncultivable bat influenza virus using a replicative synthetic virus. PLoS Pathog 10, e1004420.
45. Zhu, X., Yang, H., Guo, Z., Yu, W., Carney, P. J., Li, Y., Chen, L. -M., Paulson, J. C., Donis, R. O. & other authors (2012). Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc Natl Acad Sci U S A 109, 18903–18908.
46. Zhu, X., Yu, W., McBride, R., Li, Y., Chen, L. M., Donis, R. O., Tong, S., Paulson, J. C. & Wilson, I. A. (2013). Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci U S A 110, 1458–1463.