Cyclosporin a inhibits rotavirus replication and restores interferon-beta signaling pathway in vitro and in vivo

PLoS One. 2013 Aug 21;8(8):e71815. doi: 10.1371/journal.pone.0071815. eCollection 2013.

Abstract

Rotavirus (RV) is the most common cause of severe diarrhea among infants and young children. Currently, there is no specific drug available against rotavirus, largely due to the lack of an ideal target molecule which has hampered drug development. Our previous studies have revealed that cyclosporin A (CsA) might be potentially useful as an anti-RV drug. We therefore used both cellular and mouse models to study the immunological safety and effectiveness of CsA as an anti-RV drug. We found that CsA treatment of HT-29 cells before, during, and after viral infection efficiently inhibited Wa strain RV replication and restored IFN-β expression in a HT-29 cell line model. Exploring the underlying mechanisms showed that CsA promoted Interferon Regulatory Factor-5 (IRF-5) expression (a key positive regulator of the type I IFN signaling pathway), but not IRF-1, IRF-3, or IRF-7. Additionally, CsA inhibited SOCS-1 expression (the key negative regulator of IFN-α/β), but not SOCS-2 or SOCS-3. The antiviral effect of CsA was confirmed in an RV-infected neonatal mouse model by evaluation of antigen clearance and assessment of changes in intestinal tissue pathology. Also, no differences in T cell frequency or proliferation between the CsA- and vehicle-treated groups were observed. Thus, both our in vitro and in vivo findings suggest that CsA, through modulating the expression of key regulators in IFN signaling pathway, promote type I IFN-based intracellular innate immunity in RV host cells. These findings suggest that CsA may be a useful candidate to develop a new anti-RV strategy, although further evaluation and characterization of CsA on RV-induced diarrhea are warranted.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Blotting, Western
  • Cell Line
  • Cyclosporine / pharmacology*
  • Diarrhea / prevention & control
  • Diarrhea / virology
  • Disease Models, Animal
  • Gene Expression / drug effects
  • HT29 Cells
  • Humans
  • Immunosuppressive Agents / pharmacology
  • Interferon Regulatory Factors / genetics
  • Interferon Regulatory Factors / metabolism
  • Interferon-beta / genetics
  • Interferon-beta / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rotavirus / drug effects*
  • Rotavirus / genetics
  • Rotavirus / physiology
  • Rotavirus Infections / prevention & control*
  • Rotavirus Infections / virology
  • Signal Transduction / drug effects*
  • Signal Transduction / genetics
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Suppressor of Cytokine Signaling Proteins / metabolism
  • Virus Replication / drug effects*

Substances

  • IRF5 protein, human
  • Immunosuppressive Agents
  • Interferon Regulatory Factors
  • SOCS1 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Interferon-beta
  • Cyclosporine

Grants and funding

This work was supported by grants from the Key Technology R&D Program of Chongqing Science and Technology Commission [grant number CSTC, 2009AB5197] http://www.ctin.ac.cn/and the National Natural Science Foundation of China [grant number 81271813 and number 81202326), http://www.nsfc.gov.cn/nsfc/cen/00/download.html. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.