Autophagy protein ATG16L1 prevents necroptosis in the intestinal epithelium

J Exp Med. 2017 Dec 4;214(12):3687-3705. doi: 10.1084/jem.20170558. Epub 2017 Oct 31.

Abstract

A variant of the autophagy gene ATG16L1 is associated with Crohn's disease, an inflammatory bowel disease (IBD), and poor survival in allogeneic hematopoietic stem cell transplant recipients. We demonstrate that ATG16L1 in the intestinal epithelium is essential for preventing loss of Paneth cells and exaggerated cell death in animal models of virally triggered IBD and allogeneic hematopoietic stem cell transplantation. Intestinal organoids lacking ATG16L1 reproduced this loss in Paneth cells and displayed TNFα-mediated necroptosis, a form of programmed necrosis. This cytoprotective function of ATG16L1 was associated with the role of autophagy in promoting mitochondrial homeostasis. Finally, therapeutic blockade of necroptosis through TNFα or RIPK1 inhibition ameliorated disease in the virally triggered IBD model. These findings indicate that, in contrast to tumor cells in which autophagy promotes caspase-independent cell death, ATG16L1 maintains the intestinal barrier by inhibiting necroptosis in the epithelium.

MeSH terms

  • Animals
  • Apoptosis*
  • Autophagy*
  • Autophagy-Related Proteins
  • Caliciviridae Infections / pathology
  • Caliciviridae Infections / virology
  • Carrier Proteins / metabolism*
  • Cell Survival
  • Cytoprotection
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Gene Deletion
  • Graft vs Host Disease / pathology
  • Graft vs Host Disease / therapy
  • Hematopoietic Stem Cell Transplantation
  • Homeostasis
  • Intestinal Mucosa / metabolism*
  • Intestinal Mucosa / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Mitochondria / ultrastructure
  • Mutation / genetics
  • Necrosis
  • Norovirus / physiology
  • Organoids / pathology
  • Paneth Cells / metabolism
  • Paneth Cells / pathology
  • Receptor-Interacting Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Atg16l1 protein, mouse
  • Autophagy-Related Proteins
  • Carrier Proteins
  • Tumor Necrosis Factor-alpha
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Ripk1 protein, mouse