Rotavirus inhibits IFN-induced STAT nuclear translocation by a mechanism that acts after STAT binding to importin-α

Journal of General Virology

Volumn 95, Issue PART 8, 2014, Pages 1723-1733

  Holloway, Gavan ^a   Dang, Vi T ^a   Jans, David A ^b   Coulson, Barbara S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANISOMYCIN; GAMMA INTERFERON; IMPORTIN ALPHA 5; INTERFERON; KARYOPHERIN ALPHA; LEPTOMYCIN B; STAT1 PROTEIN; STAT2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MUTANT; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; ROTAVIRUS; ROTAVIRUS INFECTION; STAINING; WESTERN BLOTTING;

CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERFERONS; KARYOPHERINS; ROTAVIRUS; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR;

EID: 84904438991     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.064063-0     Document Type: Article

References (38)

1. Arnold, M. M., Barro, M. & Patton, J. T. (2013a). Rotavirus NSP1 mediates degradation of interferon regulatory factors through targeting of the dimerization domain. J Virol 87, 9813-9821.
2. Arnold, M. M., Sen, A., Greenberg, H. B. & Patton, J. T. (2013b). The battle between rotavirus and its host for control of the interferon signaling pathway. PLoS Pathog 9, e1003064.
3. Banninger, G. & Reich, N. C. (2004). STAT2 nuclear trafficking. J Biol Chem 279, 39199-39206.
4. Barro, M. & Patton, J. T. (2005). Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc Natl Acad Sci U S A 102, 4114-4119.
5. Barro, M. & Patton, J. T. (2007). Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J Virol 81, 4473-4481.
6. Chen, W., Calvo, P. A., Malide, D., Gibbs, J., Schubert, U., Bacik, I., Basta, S., O'Neill, R., Schickli, J. & other authors (2001). A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7, 1306-1312.
7. Coulson, B. S. & Kirkwood, C. (1991). Relation of VP7 amino acid sequence to monoclonal antibody neutralization of rotavirus and rotavirus monotype. J Virol 65, 5968-5974.
8. Coulson, B. S., Tursi, J. M., McAdam, W. J. & Bishop, R. F. (1986). Derivation of neutralizing monoclonal antibodies to human rotaviruses and evidence that an immunodominant neutralization site is shared between serotypes 1 and 3. Virology 154, 302-312.
9. Coulson, B. S., Unicomb, L. E., Pitson, G. A. & Bishop, R. F. (1987). Simple and specific enzyme immunoassay using monoclonal antibodies for serotyping human rotaviruses. J Clin Microbiol 25, 509-515.
10. Frieman, M., Yount, B., Heise, M., Kopecky-Bromberg, S. A., Palese, P. & Baric, R. S. (2007). Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J Virol 81, 9812-9824.
11. Graff, J. W., Ewen, J., Ettayebi, K. & Hardy, M. E. (2007). Zinc-binding domain of rotavirus NSP1 is required for proteasome-dependent degradation of IRF3 and autoregulatory NSP1 stability. J Gen Virol 88, 613-620.
12. Graff, J. W., Ettayebi, K. & Hardy, M. E. (2009). Rotavirus NSP1 inhibits NFkB activation by inducing proteasome-dependent degradation of β-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog 5, e1000280.
13. Graham, K. L., Halasz, P., Tan, Y., Hewish, M. J., Takada, Y., Mackow, E. R., Robinson, M. K. & Coulson, B. S. (2003). Integrin-using rotaviruses bind α2β1 integrin α2 I domain via VP4 DGE sequence and recognize alphaXbeta2 and alphaVbeta3 by using VP7 during cell entry. J Virol 77, 9969-9978.
14. Hagmaier, K., Stock, N., Precious, B., Childs, K., Wang, L. F., Goodbourn, S. & Randall, R. E. (2007). Mapuera virus, a rubulavirus that inhibits interferon signalling in a wide variety of mammalian cells without degrading STATs. J Gen Virol 88, 956-966.
15. Holloway, G. & Coulson, B. S. (2006). Rotavirus activates JNK and p38 signaling pathways in intestinal cells, leading to AP-1-driven transcriptional responses and enhanced virus replication. J Virol 80, 10624-10633.
16. Holloway, G. & Coulson, B. S. (2013). Innate cellular responses to rotavirus infection. J Gen Virol 94, 1151-1160.
17. Holloway, G., Truong, T. T. & Coulson, B. S. (2009). Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kB. J Virol 83, 4942-4951.
18. Huang, J. A., Nagesha, H. S., Snodgrass, D. R. & Holmes, I. H. (1992). Molecular and serological analyses of two bovine rotaviruses (B-11 and B-60) causing calf scours in Australia. J Clin Microbiol 30, 85-92.
19. Jagger, B. W., Wise, H. M., Kash, J. C., Walters, K. A., Wills, N. M., Xiao, Y. L., Dunfee, R. L., Schwartzman, L. M., Ozinsky, A. & other authors (2012). An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337, 199-204.
20. Kool, D. A., Matsui, S. M., Greenberg, H. B. & Holmes, I. H. (1992). Isolation and characterization of a novel reassortant between avian Ty-1 and simian RRV rotaviruses. J Virol 66, 6836-6839.
21. Londrigan, S. L., Hewish, M. J., Thomson, M. J., Sanders, G. M., Mustafa, H. & Coulson, B. S. (2000). Growth of rotaviruses in continuous human and monkey cell lines that vary in their expression of integrins. J Gen Virol 81, 2203-2213.
22. McBride, K. M., McDonald, C. & Reich, N. C. (2000). Nuclear export signal located within the DNA-binding domain of the STAT1 transcription factor. EMBO J 19, 6196-6206.
23. Melen, K., Fagerlund, R., Franke, J., Kohler, M., Kinnunen, L. & Julkunen, I. (2003). Importin α nuclear localization signal binding sites for STAT1, STAT2, and influenza A virus nucleoprotein. J Biol Chem 278, 28193-28200.
24. Meyer, T., Marg, A., Lemke, P., Wiesner, B. & Vinkemeier, U. (2003). DNA binding controls inactivation and nuclear accumulation of the transcription factor Stat1. Genes Dev 17, 1992-2005.
25. Patton, J. T., Taraporewala, Z., Chen, D., Chizhikov, V., Jones, M., Elhelu, A., Collins, M., Kearney, K., Wagner, M. & other authors (2001). Effect of intragenic rearrangement and changes in the 3 consensus sequence on NSP1 expression and rotavirus replication. J Virol 75, 2076-2086.
26. Ramachandran, A. & Horvath, C.M. (2009). Paramyxovirus disruption of interferon signal transduction: STATus report. J Interferon Cytokine Res 29, 531-537.
27. Randall, R. E. & Goodbourn, S. (2008). Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89, 1-47.
28. Reid, S. P., Leung, L. W., Hartman, A. L., Martinez, O., Shaw, M. L., Carbonnelle, C., Volchkov, V. E., Nichol, S. T. & Basler, C. F. (2006). Ebola virus VP24 binds karyopherin α1 and blocks STAT1 nuclear accumulation. J Virol 80, 5156-5167.
29. Reid, S. P., Valmas, C., Martinez, O., Sanchez, F. M. & Basler, C. F. (2007). Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin α proteins with activated STAT1. J Virol 81, 13469-13477.
30. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671-675.
31. Sekimoto, T., Imamoto, N., Nakajima, K., Hirano, T. & Yoneda, Y. (1997). Extracellular signal-dependent nuclear import of Stat1 is mediated by nuclear pore-targeting complex formation with NPI-1, but not Rch1. EMBO J 16, 7067-7077.
32. Sen, A., Rott, L., Phan, N., Mukherjee, G. & Greenberg, H. B. (2014). Rotavirus NSP1 protein inhibits interferon-mediated STAT1 activation. J Virol 88, 41-53.
33. Stirzaker, S. C., Whitfeld, P. L., Christie, D. L., Bellamy, A. R. & Both, G. W. (1987). Processing of rotavirus glycoprotein VP7: implications for the retention of the protein in the endoplasmic reticulum. J Cell Biol 105, 2897-2903.
34. Taniguchi, K., Kojima, K. & Urasawa, S. (1996). Nondefective rotavirus mutants with an NSP1 gene which has a deletion of 500 nucleotides, including a cysteine-rich zinc finger motif-encoding region (nucleotides 156 to 248), or which has a nonsense codon at nucleotides 153-155. J Virol 70, 4125-4130.
35. Torres-Vega, M. A., González, R. A., Duarte, M., Poncet, D., López, S. & Arias, C. F. (2000). The C-terminal domain of rotavirus NSP5 is essential for its multimerization, hyperphosphorylation and interaction with NSP6. J Gen Virol 81, 821-830.
36. Trojnar, E., Otto, P. & Johne, R. (2009). The first complete genome sequence of a chicken group A rotavirus indicates independent evolution of mammalian and avian strains. Virology 386, 325-333.
37. Vidy, A., El Bougrini, J., Chelbi-Alix, M. K. & Blondel, D. (2007). The nucleocytoplasmic rabies virus P protein counteracts interferon signaling by inhibiting both nuclear accumulation and DNA binding of STAT1. J Virol 81, 4255-4263.
38. Welch, S. K., Crawford, S. E. & Estes, M. K. (1989). Rotavirus SA11 genome segment 11 protein is a nonstructural phosphoprotein. J Virol 63, 3974-3982.