Persistent Innate Immune Stimulation Results in IRF3-Mediated but Caspase-Independent Cytostasis

Viruses. 2020 Jun 11;12(6):635. doi: 10.3390/v12060635.

Abstract

Persistent virus infection continuously produces non-self nucleic acids that activate cell-intrinsic immune responses. However, the antiviral defense evolved as a transient, acute phase response and the effects of persistently ongoing stimulation onto cellular homeostasis are not well understood. To study the consequences of long-term innate immune activation, we expressed the NS5B polymerase of Hepatitis C virus (HCV), which in absence of viral genomes continuously produces immune-stimulatory RNAs. Surprisingly, within 3 weeks, NS5B expression declined and the innate immune response ceased. Proteomics and functional analyses indicated a reduced proliferation of those cells most strongly stimulated, which was independent of interferon signaling but required mitochondrial antiviral signaling protein (MAVS) and interferon regulatory factor 3 (IRF3). Depletion of MAVS or IRF3, or overexpression of the MAVS-inactivating HCV NS3/4A protease not only blocked interferon responses but also restored cell growth in NS5B expressing cells. However, pan-caspase inhibition could not rescue the NS5B-induced cytostasis. Our results underline an active counter selection of cells with prolonged innate immune activation, which likely constitutes a cellular strategy to prevent persistent virus infections.

Keywords: HCV; IRF3; MAVS; RIG-I; cytostasis; innate immunity; interferon.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology
  • Carrier State / immunology*
  • Carrier State / virology
  • Caspases / genetics
  • Caspases / immunology*
  • Hepacivirus / genetics
  • Hepacivirus / physiology
  • Hepatitis C / genetics
  • Hepatitis C / immunology*
  • Hepatitis C / virology
  • Humans
  • Immunity, Innate*
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / immunology*
  • Viral Nonstructural Proteins / genetics
  • Viral Nonstructural Proteins / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • IRF3 protein, human
  • Interferon Regulatory Factor-3
  • MAVS protein, human
  • NS3 protein, hepatitis C virus
  • Viral Nonstructural Proteins
  • Caspases