Activation of Interferon Regulatory Factor 3 Is Inhibited by the Influenza A Virus NS1 Protein

doi:10.1128/JVI.74.17.7989-7996.2000

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Journal of Virology, September 2000, p. 7989-7996, Vol. 74, No. 17
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Activation of Interferon Regulatory Factor 3 Is Inhibited by the Influenza A Virus NS1 Protein

Julie Talon,¹ Curt M. Horvath,² Rosalind Polley,³ Christopher F. Basler,¹ Thomas Muster,⁴ Peter Palese,¹^,^* and Adolfo García-Sastre¹

Department of Microbiology¹ and Immunobiology Center,² Mount Sinai School of Medicine, New York, New York 10029; Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath, England³; and Department of Dermatology, University of Vienna Medical School, 1090 Vienna, Austria⁴

Received 1 February 2000/Accepted 8 June 2000

We present a novel mechanism by which viruses may inhibit the alpha/beta interferon (IFN- $alpha$ / $beta$ ) cascade. The double-strandedRNA (dsRNA) binding protein NS1 of influenza virus is shown toprevent the potent antiviral interferon response by inhibitingthe activation of interferon regulatory factor 3 (IRF-3), a keyregulator of IFN- $alpha$ / $beta$ gene expression. IRF-3 activation and, asa consequence, IFN- $beta$ mRNA induction are inhibited in wild-type(PR8) influenza virus-infected cells but not in cells infectedwith an isogenic virus lacking the NS1 gene (delNS1 virus). Furthermore,NS1 is shown to be a general inhibitor of the interferon signalingpathway. Inhibition of IRF-3 activation can be achieved by theexpression of wild-type NS1 in trans, not only in delNS1 virus-infectedcells but also in cells infected with a heterologous RNA virus(Newcastle disease virus). We propose that inhibition of IRF-3activation by a dsRNA binding protein significantly contributesto the virulence of influenza A viruses and possibly to that ofotherviruses.

^* Corresponding author. Mailing address: Department of Microbiology, Mount Sinai School of Medicine, One Gustave Levy Pl., NewYork, NY 10029. Phone: (212) 241-7318. Fax: (212) 722-3634. E-mail:peter.palese{at}mssm.edu.

Journal of Virology, September 2000, p. 7989-7996, Vol. 74, No. 17
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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Basler, C. F., Mikulasova, A., Martinez-Sobrido, L., Paragas, J., Muhlberger, E., Bray, M., Klenk, H.-D., Palese, P., Garcia-Sastre, A. (2003). The Ebola Virus VP35 Protein Inhibits Activation of Interferon Regulatory Factor 3. J. Virol. 77: 7945-7956 [Abstract] [Full Text]
Kohl, A., Clayton, R. F., Weber, F., Bridgen, A., Randall, R. E., Elliott, R. M. (2003). Bunyamwera Virus Nonstructural Protein NSs Counteracts Interferon Regulatory Factor 3-Mediated Induction of Early Cell Death. J. Virol. 77: 7999-8008 [Abstract] [Full Text]
Efferson, C. L., Schickli, J., Ko, B. K., Kawano, K., Mouzi, S., Palese, P., Garcia-Sastre, A., Ioannides, C. G. (2003). Activation of Tumor Antigen-Specific Cytotoxic T Lymphocytes (CTLs) by Human Dendritic Cells Infected with an Attenuated Influenza A Virus Expressing a CTL Epitope Derived from the HER-2/neu Proto-Oncogene. J. Virol. 77: 7411-7424 [Abstract] [Full Text]
Hagmaier, K., Jennings, S., Buse, J., Weber, F., Kochs, G. (2003). Novel Gene Product of Thogoto Virus Segment 6 Codes for an Interferon Antagonist. J. Virol. 77: 2747-2752 [Abstract] [Full Text]
Skiadopoulos, M. H., Schmidt, A. C., Riggs, J. M., Surman, S. R., Elkins, W. R., St. Claire, M., Collins, P. L., Murphy, B. R. (2002). Determinants of the Host Range Restriction of Replication of Bovine Parainfluenza Virus Type 3 in Rhesus Monkeys Are Polygenic. J. Virol. 77: 1141-1148 [Abstract] [Full Text]
Park, M.-S., Shaw, M. L., Munoz-Jordan, J., Cros, J. F., Nakaya, T., Bouvier, N., Palese, P., Garcia-Sastre, A., Basler, C. F. (2002). Newcastle Disease Virus (NDV)-Based Assay Demonstrates Interferon-Antagonist Activity for the NDV V Protein and the Nipah Virus V, W, and C Proteins. J. Virol. 77: 1501-1511 [Abstract] [Full Text]
Ludwig, S., Wang, X., Ehrhardt, C., Zheng, H., Donelan, N., Planz, O., Pleschka, S., Garcia-Sastre, A., Heins, G., Wolff, T. (2002). The Influenza A Virus NS1 Protein Inhibits Activation of Jun N-Terminal Kinase and AP-1 Transcription Factors. J. Virol. 76: 11166-11171 [Abstract] [Full Text]
Wang, X., Basler, C. F., Williams, B. R. G., Silverman, R. H., Palese, P., Garcia-Sastre, A. (2002). Functional Replacement of the Carboxy-Terminal Two-Thirds of the Influenza A Virus NS1 Protein with Short Heterologous Dimerization Domains. J. Virol. 76: 12951-12962 [Abstract] [Full Text]
Neumann, G., Whitt, M. A., Kawaoka, Y. (2002). A decade after the generation of a negative-sense RNA virus from cloned cDNA - what have we learned?. J. Gen. Virol. 83: 2635-2662 [Abstract] [Full Text]
Mahalingam, S., Lidbury, B. A. (2002). Suppression of lipopolysaccharide-induced antiviral transcription factor (STAT-1 and NF-kappa B) complexes by antibody-dependent enhancement of macrophage infection by Ross River virus. Proc. Natl. Acad. Sci. USA 99: 13819-13824 [Abstract] [Full Text]
Mahalingam, S., Meanger, J., Foster, P. S., Lidbury, B. A. (2002). The viral manipulation of the host cellular and immune environments to enhance propagation and survival: a focus on RNA viruses. J. Leukoc. Biol. 72: 429-439 [Abstract] [Full Text]
Barnes, B. J., Kellum, M. J., Field, A. E., Pitha, P. M. (2002). Multiple Regulatory Domains of IRF-5 Control Activation, Cellular Localization, and Induction of Chemokines That Mediate Recruitment of T Lymphocytes. Mol. Cell. Biol. 22: 5721-5740 [Abstract] [Full Text]
Baigent, S. J., Zhang, G., Fray, M. D., Flick-Smith, H., Goodbourn, S., McCauley, J. W. (2002). Inhibition of Beta Interferon Transcription by Noncytopathogenic Bovine Viral Diarrhea Virus Is through an Interferon Regulatory Factor 3-Dependent Mechanism. J. Virol. 76: 8979-8988 [Abstract] [Full Text]
Graff, J. W., Mitzel, D. N., Weisend, C. M., Flenniken, M. L., Hardy, M. E. (2002). Interferon Regulatory Factor 3 Is a Cellular Partner of Rotavirus NSP1. J. Virol. 76: 9545-9550 [Abstract] [Full Text]
Geiss, G. K., Salvatore, M., Tumpey, T. M., Carter, V. S., Wang, X., Basler, C. F., Taubenberger, J. K., Bumgarner, R. E., Palese, P., Katze, M. G., Garcia-Sastre, A. (2002). Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: The role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc. Natl. Acad. Sci. USA 99: 10736-10741 [Abstract] [Full Text]
Kim, M.-J., Latham, A. G., Krug, R. M. (2002). Human influenza viruses activate an interferon-independent transcription of cellular antiviral genes: Outcome with influenza A virus is unique. Proc. Natl. Acad. Sci. USA 99: 10096-10101 [Abstract] [Full Text]
Weber, F., Bridgen, A., Fazakerley, J. K., Streitenfeld, H., Kessler, N., Randall, R. E., Elliott, R. M. (2002). Bunyamwera Bunyavirus Nonstructural Protein NSs Counteracts the Induction of Alpha/Beta Interferon. J. Virol. 76: 7949-7955 [Abstract] [Full Text]
Xiang, Y., Condit, R. C., Vijaysri, S., Jacobs, B., Williams, B. R. G., Silverman, R. H. (2002). Blockade of Interferon Induction and Action by the E3L Double-Stranded RNA Binding Proteins of Vaccinia Virus. J. Virol. 76: 5251-5259 [Abstract] [Full Text]
Zhu, F. X., King, S. M., Smith, E. J., Levy, D. E., Yuan, Y. (2002). A Kaposi's sarcoma-associated herpesviral protein inhibits virus-mediated induction of type I interferon by blocking IRF-7 phosphorylation and nuclear accumulation. Proc. Natl. Acad. Sci. USA 99: 5573-5578 [Abstract] [Full Text]

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