1887

Abstract

The retinoic acid-induced gene I (RIG-I) plays a crucial role in sensing viral RNA and IFN-β production. RIG-I varies in length and sequence between different species. We assessed the functional differences between RIG-I proteins derived from mammals and birds. The transfection of duck caspase recruitment domains (CARDs) and duck RIG-I (dCARDs and dRIG-I) and goose CARDs and goose RIG-I (gCARDs and gRIG-I) into chicken DF-1 cells increased the production of mRNA and IFN-stimulated genes and decreased influenza A virus (IAV) replication; whereas human CARDs and RIG-I (hCARDs and hRIG-I) and mouse CARDs and RIG-I (mCARDs and mRIG-I) had no effect. In human 293T and A549 cells, hCARDs had the strongest IFN-inducing activity, followed by mCARDs, dCARDs and gCARDs. The IFN-inducing activity of hRIG-I was stronger than that of mRIG-I, dRIG-I and gRIG-I, in that order. The results showed that, although the ability of dCARDs to activate IFN was stronger than that of gCARDs in DF-1, 293T and A549 cells, dRIG-I had a weaker ability to activate IFN than gRIG-I in DF-1 cells with or without IAV infection. These data suggest that RIG-I proteins from different species have different amino acid sequences and functions. This genetic and functional diversity renders RIG-I flexible, adaptable and capable of recognizing many viruses in different species.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.069914-0
2015-02-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/2/277.html?itemId=/content/journal/jgv/10.1099/vir.0.069914-0&mimeType=html&fmt=ahah

References

  1. Barber M. R., Aldridge J. R. Jr, Webster R. G., Magor K. E. 2010; Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci U S A 107:5913–5918 [View Article][PubMed]
    [Google Scholar]
  2. Chen C.-J., Chen G.-W., Wang C.-H., Huang C.-H., Wang Y.-C., Shih S.-R. 2010; Differential localization and function of PB1-F2 derived from different strains of influenza A virus. J Virol 84:10051–10062 [View Article][PubMed]
    [Google Scholar]
  3. Creagh E. M., O’Neill L. A. 2006; TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol 27:352–357 [View Article][PubMed]
    [Google Scholar]
  4. Gack M. U., Kirchhofer A., Shin Y. C., Inn K.-S., Liang C., Cui S., Myong S., Ha T., Hopfner K.-P., Jung J. U. 2008; Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc Natl Acad Sci U S A 105:16743–16748 [View Article][PubMed]
    [Google Scholar]
  5. Gack M. U., Nistal-Villán E., Inn K.-S., García-Sastre A., Jung J. U. 2010; Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J Virol 84:3220–3229 [View Article][PubMed]
    [Google Scholar]
  6. Gao D., Yang Y.-K., Wang R.-P., Zhou X., Diao F.-C., Li M.-D., Zhai Z.-H., Jiang Z.-F., Chen D.-Y. 2009; REUL is a novel E3 ubiquitin ligase and stimulator of retinoic-acid-inducible gene-I. PLoS ONE 4:e5760 [View Article][PubMed]
    [Google Scholar]
  7. Hausmann S., Marq J.-B., Tapparel C., Kolakofsky D., Garcin D. 2008; RIG-I and dsRNA-induced IFN-beta activation. PLoS ONE 3:e3965 [View Article][PubMed]
    [Google Scholar]
  8. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A. et al. 2005; IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434:772–777 [View Article][PubMed]
    [Google Scholar]
  9. Jiang X., Kinch L. N., Brautigam C. A., Chen X., Du F., Grishin N. V., Chen Z. J. 2012; Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36:959–973 [View Article][PubMed]
    [Google Scholar]
  10. Kawai T., Akira S. 2009; The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 21:317–337 [View Article][PubMed]
    [Google Scholar]
  11. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K. J., Takeuchi O., Akira S. 2005; IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6:981–988 [View Article][PubMed]
    [Google Scholar]
  12. Lee C.-W., Jung K., Jadhao S. J., Suarez D. L. 2008; Evaluation of chicken-origin (DF-1) and quail-origin (QT-6) fibroblast cell lines for replication of avian influenza viruses. J Virol Methods 153:22–28 [View Article][PubMed]
    [Google Scholar]
  13. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔT Method. Methods 25:402–408 [View Article][PubMed]
    [Google Scholar]
  14. Loo Y.-M., Gale M. Jr 2011; Immune signaling by RIG-I-like receptors. Immunity 34:680–692 [View Article][PubMed]
    [Google Scholar]
  15. Magor K. E., Miranzo Navarro D., Barber M. R., Petkau K., Fleming-Canepa X., Blyth G. A., Blaine A. H. 2013; Defense genes missing from the flight division. Dev Comp Immunol 41:377–388 [View Article][PubMed]
    [Google Scholar]
  16. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., Tschopp J. 2005; Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167–1172 [View Article][PubMed]
    [Google Scholar]
  17. Miranzo-Navarro D., Magor K. E. 2014; Activation of duck R IG-I by TRIM25 is independent of anchored ubiquitin. PLoS ONE 9:e86968 [View Article][PubMed]
    [Google Scholar]
  18. Nakhaei P., Paz S., Hiscott J. 2006; Activation of interferon gene expression through toll-like receptor-dependent and -independent pathways. In The Interferons: Characterization and Application pp. 35–61 Edited by Meager A. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA;
    [Google Scholar]
  19. Nistal-Villán E., Gack M. U., Martínez-Delgado G., Maharaj N. P., Inn K.-S., Yang H., Wang R., Aggarwal A. K., Jung J. U., García-Sastre A. 2010; Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-β production. J Biol Chem 285:20252–20261 [View Article][PubMed]
    [Google Scholar]
  20. Oshiumi H., Matsumoto M., Hatakeyama S., Seya T. 2009; Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-β induction during the early phase of viral infection. J Biol Chem 284:807–817 [View Article][PubMed]
    [Google Scholar]
  21. Oshiumi H., Miyashita M., Inoue N., Okabe M., Matsumoto M., Seya T. 2010; The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8:496–509 [View Article][PubMed]
    [Google Scholar]
  22. Rajsbaum R., Albrecht R. A., Wang M. K., Maharaj N. P., Versteeg G. A., Nistal-Villán 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 [View Article][PubMed]
    [Google Scholar]
  23. Reed L. J., Muench H. 1938; A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493–497
    [Google Scholar]
  24. Saito T., Hirai R., Loo Y.-M., Owen D., Johnson C. L., Sinha S. C., Akira S., Fujita T., Gale M. Jr 2007; Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci U S A 104:582–587 [View Article][PubMed]
    [Google Scholar]
  25. Sun Y., Ding N., Ding S. S., Yu S., Meng C., Chen H., Qiu X., Zhang S., Yu Y. et al. 2013; Goose RIG-I functions in innate immunity against Newcastle disease virus infections. Mol Immunol 53:321–327 [View Article][PubMed]
    [Google Scholar]
  26. Takahasi K., Yoneyama M., Nishihori T., Hirai R., Kumeta H., Narita R., Gale M. Jr, Inagaki F., Fujita T. 2008; Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol Cell 29:428–440 [View Article][PubMed]
    [Google Scholar]
  27. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. 1992; Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179[PubMed]
    [Google Scholar]
  28. Xu L.-G., Wang Y.-Y., Han K.-J., Li L.-Y., Zhai Z., Shu H.-B. 2005; VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol Cell 19:727–740 [View Article][PubMed]
    [Google Scholar]
  29. Zeng W., Sun L., Jiang X., Chen X., Hou F., Adhikari A., Xu M., Chen Z. J. 2010; Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141:315–330 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.069914-0
Loading
/content/journal/jgv/10.1099/vir.0.069914-0
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error