NSP1 of human rotaviruses commonly inhibits NF-κB signalling by inducing β-TrCP degradation

Journal of General Virology

Volumn 96, Issue 7, 2015, Pages 1768-1776

  Di Fiore, Izabel J M ^a   Pane, Jessica A ^a   Holloway, Gavan ^a   Coulson, Barbara S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 8; NONSTRUCTURAL PROTEIN 1; RANTES; SERINE; NSP1 PROTEIN, ROTAVIRUS; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HT 29 CELL LINE; HUMAN; HUMAN CELL; HUMAN ROTAVIRUS; INTESTINE EPITHELIUM CELL; NONHUMAN; PORCINE ROTAVIRUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REPORTER GENE; ROTAVIRUS INFECTION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; EPITHELIUM CELL; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PIG; ROTAVIRUS; VIROLOGY;

HUMAN ROTAVIRUS A; PORCINE ROTAVIRUS; ROTAVIRUS;

ANIMALS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CELL LINE; EPITHELIAL CELLS; HUMANS; IMMUNE EVASION; NF-KAPPA B; PROTEOLYSIS; ROTAVIRUS; SWINE; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84938319775     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.000093     Document Type: Article

References (39)

1. Angel, J., Franco, M. A. & Greenberg, H. B. (2012). Rotavirus immune responses and correlates of protection. Curr Opin Virol 2, 419-425.
2. Arnold, M. M. & Patton, J. T. (2011). Diversity of interferon antagonist activities mediated by NSP1 proteins of different rotavirus strains. J Virol 85, 1970-1979.
3. Arnold, M., Patton, J. T. & McDonald, S. M. (2009). Culturing, storage, and quantification of rotaviruses. Current Protocols in Microbiology, Chapter 15, Unit 15C.3, 15C.3.1-15C.3.24
4. Arnold, M. M., Barro, M. & Patton, J. T. (2013). Rotavirus NSP1 mediates degradation of interferon regulatory factors through targeting of the dimerization domain. J Virol 87, 9813-9821.
5. 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.
6. 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
7. Bour, S., Perrin, C., Akari, H. & Strebel, K. (2001). The human immunodeficiency virus type 1 Vpu protein inhibits NF-k B activation by interfering with b TrCP-mediated degradation of Ikappa B. J Biol Chem 276, 15920-15928.
8. Broquet, A. H., Hirata, Y., McAllister, C. S. & Kagnoff, M. F. (2011). RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium. J Immunol 186, 1618-1626.
9. Casola, A., Estes, M. K., Crawford, S. E., Ogra, P. L., Ernst, P. B., Garofalo, R. P. & Crowe, S. E. (1998). Rotavirus infection of cultured intestinal epithelial cells induces secretion of CXC and CC chemokines. Gastroenterology 114, 947-955.
10. Chevenet, F., Brun, C., Bañuls, A. L., Jacq, B. & Christen, R. (2006). TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7, 439
11. 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.
12. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V. & other authors (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36 (Web Server issue), W465-W469.
13. Dong, H. J., Qian, Y., Huang, T., Zhu, R. N., Zhao, L. Q., Zhang, Y., Li, R. C. & Li, Y. P. (2013). Identification of circulating porcine-human reassortant G4P[6] rotavirus from children with acute diarrhea in China by whole genome analyses. Infect Genet Evol 20, 155-162.
14. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
15. Feng, N., Yasukawa, L. L., Sen, A. & Greenberg, H. B. (2013). Permissive replication of homologous murine rotavirus in the mouse intestine is primarily regulated by VP4 and NSP1. J Virol 87, 8307-8316
16. 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.
17. 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.
18. Graff, J. W., Ettayebi, K. & Hardy, M. E. (2009). Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of β-TRCP: a novel mechanism of IFN antagonism. PLoS Pathog 5, e1000280
19. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59, 307-321.
20. Halasz, P., Holloway, G., Turner, S. J. & Coulson, B. S. (2008). Rotavirus replication in intestinal cells differentially regulates integrin expression by a phosphatidylinositol 3-kinase-dependent pathway, resulting in increased cell adhesion and virus yield. J Virol 82, 148-160.
21. Harte, M. T., Haga, I. R., Maloney, G., Gray, P., Reading, P. C., Bartlett, N. W., Smith, G. L., Bowie, A. & O’Neill, L. A. (2003). The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J Exp Med 197, 343-351.
22. 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.
23. Holloway, G. & Coulson, B. S. (2013). Innate cellular responses to rotavirus infection. J Gen Virol 94, 1151-1160.
24. Holloway, G., Truong, T. T. & Coulson, B. S. (2009). Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kappaB. J Virol 83, 4942-4951.
25. Holloway, G., Dang, V. T., Jans, D. A. & Coulson, B. S. (2014). Rotavirus inhibits IFN-induced STAT nuclear translocation by a mechanism that acts after STAT binding to importin-a. J Gen Virol 95, 1723-1733.
26. Liang, Q., Fu, B., Wu, F., Li, X., Yuan, Y. & Zhu, F. (2012). ORF45 of Kaposi’s sarcoma-associated herpesvirus inhibits phosphorylation of interferon regulatory factor 7 by IKKe and TBK1 as an alternative substrate. J Virol 86, 10162-10172.
27. 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.
28. Mansur, D. S., Maluquer de Motes, C., Unterholzner, L., Sumner, R. P., Ferguson, B. J., Ren, H., Strnadova, P., Bowie, A. G. & Smith, G. L. (2013). Poxvirus targeting of E3 ligase β-TRCP by molecular mimicry: a mechanism to inhibit NF-κB activation and promote immune evasion and virulence. PLoS Pathog 9, e1003183.
29. 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 39 consensus sequence on NSP1 expression and rotavirus replication. J Virol 75, 2076-2086.
30. 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.
31. Rollo, E. E., Kumar, K. P., Reich, N. C., Cohen, J., Angel, J., Greenberg, H. B., Sheth, R., Anderson, J., Oh, B. & other authors (1999). The epithelial cell response to rotavirus infection. J Immunol 163, 4442-4452.
32. Sato, T., Suzuki, H., Kitaoka, S., Konno, T. & Ishida, N. (1986). Patterns of polypeptide synthesis in human rotavirus infected cells. Arch Virol 90, 29-40.
33. Sen, A., Rott, L., Phan, N., Mukherjee, G. & Greenberg, H. B. (2014). Rotavirus NSP1 protein inhibits interferon-mediated STAT1 activa-tion. J Virol 88, 41-53.
34. Stadnyk, A. W. (2002). Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can J Gastroenterol 16, 241-246.
35. Theil, K. W., Bohl, E. H. & Agnes, A. G. (1977). Cell culture propagation of porcine rotavirus (reovirus-like agent). Am J Vet Res 38, 1765-1768.
36. Wang, X., Hussain, S., Wang, E. J., Wang, X., Li, M. O., García-Sastre, A. & Beg, A. A. (2007). Lack of essential role of NF-k B p50, RelA, and cRel subunits in virus-induced type 1 IFN expression. J Immunol 178, 6770-6776.
37. Wang, J., Basagoudanavar, S. H., Wang, X., Hopewell, E., Albrecht, R., García-Sastre, A., Balachandran, S. & Beg, A. A. (2010). NF-κB RelA subunit is crucial for early IFN-b expression and resistance to RNA virus replication. J Immunol 185, 1720-1729.
38. Zhang, R., Jha, B. K., Ogden, K. M., Dong, B., Zhao, L., Elliott, R., Patton, J. T., Silverman, R. H. & Weiss, S. R. (2013). Homologous 29,59-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. Proc Natl Acad Sci U S A 110, 13114-13119.
39. 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 U S A 99, 5573-5578