β-catenin promotes the type I IFN synthesis and the IFN-dependent signaling response but is suppressed by influenza A virus-induced RIG-I/NF-κB signaling

Cell Commun Signal. 2014 Apr 26:12:29. doi: 10.1186/1478-811X-12-29.

Abstract

Background: The replication cycle of most pathogens, including influenza viruses, is perfectly adapted to the metabolism and signal transduction pathways of host cells. After infection, influenza viruses activate several cellular signaling cascades that support their propagation but suppress those that interfere with viral replication. Accumulation of viral RNA plays thereby a central role. Its sensing by the pattern recognition receptors of the host cells leads to the activation of several signal transduction waves that result in induction of genes, responsible for the cellular innate immune response. Type I interferon (IFN) genes and interferon-stimulated genes (ISG) coding for antiviral-acting proteins, such as MxA, OAS-1 or PKR, are primary targets of these signaling cascades. β- and γ-catenin are closely related armadillo repeat-containing proteins with dual roles. At the cell membrane they serve as adapter molecules linking cell-cell contacts to microfilaments. In the cytosol and nucleus, the proteins form a transcriptional complex with the lymphoid enhancer factor/T-cell factor (LEF/TCF), regulating the transcription of many genes, thereby controlling different cellular functions such as cell cycle progression and differentiation.

Results: In this study, we demonstrate that β- and γ-catenin are important regulators of the innate cellular immune response to influenza A virus (IAV) infections. They inhibit viral replication in lung epithelial cells by enhancing the virus-dependent induction of the IFNB1 gene and interferon-stimulated genes. Simultaneously, the prolonged infection counteracts the antiviral effect of β- and γ-catenin. Influenza viruses suppress β-catenin-dependent transcription by misusing the RIG-I/NF-κB signaling cascade that is induced in the course of infection by viral RNA.

Conclusion: We identified β- and γ-catenin as novel antiviral-acting proteins. While these factors support the induction of common target genes of the cellular innate immune response, their functional activity is suppressed by pathogen evasion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chlorocebus aethiops
  • Dogs
  • Epithelial Cells / metabolism
  • Epithelial Cells / virology
  • HEK293 Cells
  • Humans
  • Immunity, Innate
  • Influenza A Virus, H1N1 Subtype / pathogenicity*
  • Influenza A Virus, H1N1 Subtype / physiology
  • Interferon-beta / genetics
  • Interferon-beta / metabolism*
  • Lung / cytology
  • Madin Darby Canine Kidney Cells
  • NF-kappa B / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Retinoic Acid / metabolism*
  • Signal Transduction
  • Vero Cells
  • Vesicular stomatitis Indiana virus / pathogenicity
  • Vesicular stomatitis Indiana virus / physiology
  • Virus Replication
  • beta Catenin / metabolism*
  • gamma Catenin / metabolism

Substances

  • NF-kappa B
  • PLAAT4 protein, human
  • RNA, Messenger
  • Receptors, Retinoic Acid
  • beta Catenin
  • gamma Catenin
  • Interferon-beta