DNA sensing and associated type 1 interferon signaling contributes to progression of radiation-induced liver injury

Cell Mol Immunol. 2021 Jul;18(7):1718-1728. doi: 10.1038/s41423-020-0395-x. Epub 2020 Mar 19.

Abstract

Liver damage upon exposure to ionizing radiation (IR), whether accidental or therapeutic, can contribute to liver dysfunction. Currently, radiotherapy (RT) is used for various cancers including hepatocellular carcinoma (HCC); however, the treatment dose is limited by radiation-induced liver disease (RILD) with a high mortality rate. Furthermore, the precise molecular mechanisms of RILD remain poorly understood. Here, we investigated RILD pathogenesis using various knockout mouse strains subjected to whole-liver irradiation. We found that hepatocytes released a large quantity of double-stranded DNA (dsDNA) after irradiation. The cGAS-STING pathway in non-parenchymal cells (NPCs) was promptly activated by this dsDNA, causing interferon (IFN)-I production and release and concomitant hepatocyte damage. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against RILD. Moreover, clinically irradiated human peri-HCC liver tissues exhibited substantially higher STING and IFNβ expression than non-irradiated tissues. Increased serum IFNβ concentrations post-radiation were associated with RILD development in patients. These results delineate cGAS-STING induced type 1 interferon release in NPCs as a key mediator of IR-induced liver damage and described a mechanism of innate-immunity-driven pathology, linking cGAS-STING activation with amplification of initial radiation-induced liver injury.

Keywords: cGAS-STING; dsDNA; radiation-induced liver disease; type 1 interferon.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / radiotherapy
  • Chemical and Drug Induced Liver Injury, Chronic*
  • DNA / metabolism
  • Humans
  • Interferon Type I* / metabolism
  • Liver Neoplasms* / radiotherapy
  • Membrane Proteins / metabolism
  • Mice
  • Signal Transduction

Substances

  • Interferon Type I
  • Membrane Proteins
  • DNA