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.

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2015-02-01
2019-11-18
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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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  10. Kawai T., Akira S.. ( 2009;). The roles of TLRs, RLRs and NLRs in pathogen recognition. . Int Immunol 21:, 317–337. [CrossRef][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. [CrossRef][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. [CrossRef][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-ΔΔCT Method. . Methods 25:, 402–408. [CrossRef][PubMed]
    [Google Scholar]
  14. Loo Y.-M., Gale M. Jr. ( 2011;). Immune signaling by RIG-I-like receptors. . Immunity 34:, 680–692. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
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