ATG16L1 orchestrates interleukin-22 signaling in the intestinal epithelium via cGAS-STING

J Exp Med. 2018 Nov 5;215(11):2868-2886. doi: 10.1084/jem.20171029. Epub 2018 Sep 25.

Abstract

A coding variant of the inflammatory bowel disease (IBD) risk gene ATG16L1 has been associated with defective autophagy and deregulation of endoplasmic reticulum (ER) function. IL-22 is a barrier protective cytokine by inducing regeneration and antimicrobial responses in the intestinal mucosa. We show that ATG16L1 critically orchestrates IL-22 signaling in the intestinal epithelium. IL-22 stimulation physiologically leads to transient ER stress and subsequent activation of STING-dependent type I interferon (IFN-I) signaling, which is augmented in Atg16l1 ΔIEC intestinal organoids. IFN-I signals amplify epithelial TNF production downstream of IL-22 and contribute to necroptotic cell death. In vivo, IL-22 treatment in Atg16l1 ΔIEC and Atg16l1 ΔIEC/Xbp1 ΔIEC mice potentiates endogenous ileal inflammation and causes widespread necroptotic epithelial cell death. Therapeutic blockade of IFN-I signaling ameliorates IL-22-induced ileal inflammation in Atg16l1 ΔIEC mice. Our data demonstrate an unexpected role of ATG16L1 in coordinating the outcome of IL-22 signaling in the intestinal epithelium.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy-Related Proteins / genetics
  • Autophagy-Related Proteins / immunology*
  • Caco-2 Cells
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology*
  • Genetic Variation
  • Humans
  • Inflammatory Bowel Diseases / genetics
  • Inflammatory Bowel Diseases / immunology
  • Inflammatory Bowel Diseases / pathology
  • Interleukin-22
  • Interleukins / genetics
  • Interleukins / immunology*
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / pathology
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology*
  • Mice
  • Mice, Knockout
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / immunology*
  • Signal Transduction / genetics
  • Signal Transduction / immunology*

Substances

  • ATG16L1 protein, human
  • Atg16l1 protein, mouse
  • Autophagy-Related Proteins
  • Carrier Proteins
  • Interleukins
  • Membrane Proteins
  • STING1 protein, human
  • Sting1 protein, mouse
  • Nucleotidyltransferases
  • cGAS protein, human
  • cGAS protein, mouse