Skip to main content
SpringerLink
Log in

Antiviral activity of Schizonepeta tenuifolia Briquet against noroviruses via induction of antiviral interferons

  • Virology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Human noroviruses are the causative agents of non-bacterial gastroenteritis worldwide. The rapid onset and resolution of disease symptoms suggest that innate immune responses are critical for controlling norovirus infection; however, no effective antivirals are yet available. The present study was conducted to examine the antiviral activities of Schizonepeta tenuifolia Briquet extract (STE) against noroviruses. Treatment of human norovirus replicon-bearing HG23 cells with STE at 5 and 10 mg/ml concentrations resulted in the reduction in the viral RNA levels by 77.2% and 85.9%, respectively. STE had no cytotoxic effects on HG23 cells. Treatment of RAW 264.7 cells infected with murine norovirus 1 (MNV-1), a surrogate virus of human noroviruses, with STE at 10 and 20 µg/ml concentrations resulted in the reduction of viral replication by 58.5% and 84.9%, respectively. STE treatment induced the expression of mRNAs for type I and type II interferons in HG23 cells and upregulated the transcription of interferon-β in infected RAW 264.7 cells via increased phosphorylation of interferon regulatory factor 3, a critical transcription regulator for type I interferon production. These results suggest that STE inhibits norovirus replication through the induction of antiviral interferon production during virus replication and may serve as a candidate antiviral substance for treatment against noroviruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Baldridge, M.T., Turula, H., and Wobus, C.E. 2016. Norovirus regulation by host and microbe. Trends Mol. Med. 22, 1047–1059.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bok, K. and Green, K.Y. 2012. Norovirus gastroenteritis in immunocompromised patients. N. Engl. J. Med. 367, 2126–2132.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Byun, M.W. 2014. Schizonepeta tenuifolia ethanol extract exerts antiinflammatory activity through the inhibition of TLR4 signaling in lipopolysaccharide-stimulated macrophage cells. J. Med. Food 17, 350–356.

    Article  PubMed  CAS  Google Scholar 

  • Chang, K.O. and George, D.W. 2007. Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. J. Virol. 81, 12111–12118.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang, K.O., Sosnovtsev, S.V., Belliot, G., King, A.D., and Green, K.Y. 2006. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 353, 463–473.

    Article  PubMed  CAS  Google Scholar 

  • Changotra, H., Jia, Y., Moore, T.N., Liu, G., Kahan, S.M., Sosnovtsev, S.V., and Karst, S.M. 2009. Type I and type I interferons inhibit the translation of murine norovirus proteins. J. Virol. 83, 5683–5692.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, S.G., Cheng, M.L., Chen, K.H., Horng, J.T., Liu, C.C., Wang, S.M., Sakurai, H., Leu, Y.L., Wang, S.D., and Ho, H.Y. 2017. Antiviral activities of Schizonepeta tenuifolia Briq. against enterovirus 71 in vitro and in vivo. Sci. Rep. 7, 935.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cho, H.J., Jeong, S.G., Park, J.E., Han, J.A., Kang, H.R., Lee, D., and Song, M.J. 2013. Antiviral activity of angelicin against gammaherpesviruses. Antiviral Res. 100, 75–83.

    Article  PubMed  CAS  Google Scholar 

  • Chun, M.H., Kim, E.K., Lee, K.R., Jung, J.H., and Hong, J. 2010. Quality control of Schizonepeta tenuifolia Briq by solid-phase microextraction gas chromatography/mass spectrometry and principal component analysis. Microchem. J. 95, 25–31.

    Article  CAS  Google Scholar 

  • Doyle, A., Barataud, D., Gallay, A., Thiolet, J., Le, S.G., Kohli, E., and Vaillant, V. 2004. Norovirus foodborne outbreaks associated with the consumption of oysters from the Etang de Thau, France, Decembe 2002. Euro Surveill. 9, 24–26.

    Article  PubMed  CAS  Google Scholar 

  • Estes, M.K., Prasad, B.V., and Atmar, R.L. 2006. Noroviruses everywhere: has something changed? Curr. Opin. Infect. Dis. 19, 467–474.

    Article  Google Scholar 

  • Fung, D. and Lau, C.B. 2002. Schizonepeta tenuifolia: chemistry, pharmacology, and clinical applications. J. Clin. Pharmacol. 42, 30–36.

    Article  PubMed  CAS  Google Scholar 

  • Glass, R.I., Parashar, U.D., and Estes, M.K. 2009. Norovirus gastroenteritis. N. Engl. J. Med. 361, 1776–1785.

    Article  PubMed  CAS  Google Scholar 

  • Green, K. 2013. Caliciviridae: the noroviruses, pp. 508–609. In Knipe, D.M., Howley, P.M., Cohen, J.I., Griffin, D.E., Lamb, R.A., and Martin, M.A. (eds.), Fields virology, 6th ed. Lippincott Williams & Wilkins, Philadelphia, PA,USA.

    Google Scholar 

  • Honda, K., Takaoka, A., and Taniguchi, T. 2006. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25, 349–360.

    Article  PubMed  CAS  Google Scholar 

  • Hutson, A.M., Atmar, R.L., and Estes, M.K. 2004. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 12, 279–287.

    Article  PubMed  CAS  Google Scholar 

  • Hwang, S., Maloney, N.S., Bruinsma, M.W., Goel, G., Duan, E., Zhang, L., Shrestha, B., Diamond, M.S., Dani, A., Sosnovtsev, S.V., et al. 2012. Nondegradative role of Atg5-Atg12/Atg16L1 autophagy protein complex in antiviral activity of interferon gamma. Cell Host Microbe 11, 397–409.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F.B., Takeda, N., and Katayama, K. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 41, 1548–1557.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang, H., Han, S.W., Hong, J.W., and Sohn, N.W. 2010. Suppression of tumour necrosis factor-α by Schizonepeta tenuifolia water extract via inhibition of IκBα degradation and Jun N-terminal kin ase/stress-activated protein kinase activation. J. Pharm. Pharmacol. 62, 1069–1076.

    Article  PubMed  CAS  Google Scholar 

  • Karst, S.M., Wobus, C.E., Lay, M., Davidson, J., and Virgin, H.W. 2003. STAT1-dependent innate immunity to a Norwalk-like virus. Science 299, 1575–1578.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y.H., Jang, S.J., Park, J.Y., Oh, J.H., Kim, G.S., Kim, T.S., Kwon, O.S., Han, J.S., and Jheong, W.H. 2011. Recovery and adsorption rate of murine norovirus using NanoCeram® filters. J. Bacteriol. Virol. 41, 55–61.

    Article  CAS  Google Scholar 

  • Kim, S. and Ko, G. 2012. Using propidium monoazide to distinguish between viable and nonviable bacteria, MS2 and murine norovirus. Lett. Appl. Microbiol. 55, 182–188.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y.W., You, H.J., Lee, S., Kim, B., Kim, D.K., Choi, J.B., Kim, J.A., Lee, H.J., Joo, I.S., and Lee, J.S. 2017. Inactivation of norovirus by lemongrass essential oil using a norovirus surrogate system. J. Food Prot. 80, 1293–1302.

    Article  PubMed  Google Scholar 

  • Kirby, A.J. and Schmidt, R.J. 1997. The antioxidant activity of Chinese herbs for eczema and of placebo herbs-I. J. Ethnopharmacol. 56, 103–108.

    Article  PubMed  CAS  Google Scholar 

  • Koo, H.S., Lee, M.O., Ku, P.T., Hwang, S.J., Park, D.J., and Baik, H.S. 2016. Molecular epidemiology of norovirus in asymptomatic food handlers in Busan, Korea, and emergence of genotype GII. 17. J. Microbiol. 54, 686–694.

    Article  PubMed  Google Scholar 

  • Ma, S.C., Du, J., But, P.P.H., Deng, X.L., Zhang, Y.W., Ooi, V.E.C., Xu, H.X., Lee, S.H.S., and Lee, S.F. 2002. Antiviral Chinese medicinal herbs against respiratory syncytial virus. J. Ethnopharmacol. 79, 205–211.

    Article  PubMed  CAS  Google Scholar 

  • McCartney, S.A., Thackray, L.B., Gitlin, L., Gilfillan, S., Virgin IV, H.W., and Colonna, M. 2008. MDA-5 recognition of a murine norovirus. PLoS Pathog. 4, e1000108.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McFadden, N., Bailey, D., Carrara, G., Benson, A., Chaudhry, Y., Shortland, A., Heeney, J., Yarovinsky, F., Simmonds, P., Macdonald, A., et al. 2011. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog. 7, e1002413.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mumphrey, S.M., Changotra, H., Moore, T.N., Heimann-Nichols, E.R., Wobus, C.E., Reilly, M.J., Moghadamfalahi, M., Shukla, D., and Karst, S.M. 2007. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J. Virol. 81, 3251–3263.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ng, Y.C., Kim, Y.W., Ryu, S., Lee, A., Lee, J.S., and Song, M.J. 2017. Suppression of norovirus by natural phytochemicals from Aloe vera and Eriobotryae Folium. Food Control 73, 1362–1370.

    Article  CAS  Google Scholar 

  • Nice, T.J., Baldridge, M.T., McCune, B.T., Norman, J.M., Lazear, H.M., Artyomov, M., Diamond, M.S., and Virgin, H.W. 2015. Interferon-λ cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347, 269–273.

    Article  PubMed  CAS  Google Scholar 

  • Park, I.K., Kim, L.S., Choi, I.H., Lee, Y.S., and Shin, S.C. 2006. Fumigant activity of plant essential oils and components from Schizonepeta tenuifolia against Lycoriella ingenua (Diptera: Sciaridae). J. Econ. Entomol. 99, 1717–1721.

    Article  PubMed  CAS  Google Scholar 

  • Payne, D.C., Vinjé, J., Szilagyi, P.G., Edwards, K.M., Staat, M.A., Weinberg, G.A., Hall, C.B., Chappell, J., Bernstein, D.I., Curns, A.T., et al. 2013. Norovirus and medically attended gastroenteritis in USchildren. N. Engl. J. Med. 368, 1121–1130.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roth, A.N. and Karst, S.M. 2016. Norovirus mechanisms of immune antagonism. Curr. Opin. Virol. 16, 24–30.

    Article  PubMed  CAS  Google Scholar 

  • Thackray, L.B., Duan, E., Lazear, H.M., Kambal, A., Schreiber, R.D., Diamond, M.S., and Virgin, H.W. 2012. Critical role for interferon regulatory factor 3 (IRF-3) and IRF-7 in type I interferon- mediated control of murine norovirus replication. J. Virol. 86, 13515–13523.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wobus, C.E., Thackray, L.B., and Virgin, H.W. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80, 5104–5112.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoneyama, M., Suhara, W., and Fujita, T. 2002. Control of IRF-3 activation by phosphorylation. J. Interferon. Cytokine Res. 22, 73–76.

    Article  PubMed  CAS  Google Scholar 

  • Yoon, M.Y., Lee, H.J., Lee, B.B., Lee, S.M., Kim, J.Y., Kim, Y., Park, E., and Park, H.R. 2007. Protective effect of Schizonepeta tenuifolia Briquet extracts on oxidative DNA damage in human leucocytes and on hydrogen peroxide-induced cytotoxicity in PC12 cells. Food Sci. Biotechnol. 16, 858–862.

    Google Scholar 

  • Yu, S., Chen, Y., Zhang, L., Shan, M., Tang, Y., and Ding, A. 2011. Quantitative comparative analysis of the bio-active and toxic constituents of leaves and spikes of Schizonepeta tenuifolia at different harvesting times. Int. J. Mol. Sci. 12, 6635–6644.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng, D.P., Ando, T., Fankhauser, R.L., Beard, R.S., Glass, R.I., and Monroe, S.S. 2006. Norovirus classification and proposed strain nomenclature. Virology 346, 312–323.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Virus-Host Interactions Laboratory, Department of Biosystems and Biotechnology, Division of Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul, 02841, Republic of Korea

    Yee Ching Ng & Moon Jung Song

  2. Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul, 02841, Republic of Korea

    Ye Won Kim & Sung Joon Lee

  3. Food Microbiology Division, Food Safety Evaluation Department, National Institute of Food and Drug Safety Evaluation, Osong, 28159, Republic of Korea

    Jeong-Su Lee

Authors
  1. Yee Ching Ng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ye Won Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeong-Su Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sung Joon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Moon Jung Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Moon Jung Song.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ng, Y.C., Kim, Y.W., Lee, JS. et al. Antiviral activity of Schizonepeta tenuifolia Briquet against noroviruses via induction of antiviral interferons. J Microbiol. 56, 683–689 (2018). https://doi.org/10.1007/s12275-018-8228-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-018-8228-7

Keywords

Search

Navigation