NAIP-NLRC4 Inflammasomes Coordinate Intestinal Epithelial Cell Expulsion with Eicosanoid and IL-18 Release via Activation of Caspase-1 and -8

Immunity. 2017 Apr 18;46(4):649-659. doi: 10.1016/j.immuni.2017.03.016. Epub 2017 Apr 11.

Abstract

Intestinal epithelial cells (IECs) form a critical barrier against pathogen invasion. By generation of mice in which inflammasome expression is restricted to IECs, we describe a coordinated epithelium-intrinsic inflammasome response in vivo. This response was sufficient to protect against Salmonella tissue invasion and involved a previously reported IEC expulsion that was coordinated with lipid mediator and cytokine production and lytic IEC death. Excessive inflammasome activation in IECs was sufficient to result in diarrhea and pathology. Experiments with IEC organoids demonstrated that IEC expulsion did not require other cell types. IEC expulsion was accompanied by a major actin rearrangement in neighboring cells that maintained epithelium integrity but did not absolutely require Caspase-1 or Gasdermin D. Analysis of Casp1-/-Casp8-/- mice revealed a functional Caspase-8 inflammasome in vivo. Thus, a coordinated IEC-intrinsic, Caspase-1 and -8 inflammasome response plays a key role in intestinal immune defense and pathology.

Keywords: ASC; Caspase-1; Caspase-8; Naip; Nlrc4; expulsion; extrusion; inflammasome; intestinal epithelial cell.

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism*
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism*
  • Caspase 1 / genetics
  • Caspase 1 / metabolism*
  • Caspase 8 / genetics
  • Caspase 8 / metabolism*
  • Eicosanoids / metabolism*
  • Enzyme Activation
  • Enzyme-Linked Immunosorbent Assay
  • Epithelial Cells / metabolism*
  • Epithelial Cells / microbiology
  • Inflammasomes / genetics
  • Inflammasomes / metabolism
  • Interleukin-18 / metabolism*
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Intestinal Mucosa / pathology
  • Intracellular Signaling Peptides and Proteins
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Confocal
  • Neuronal Apoptosis-Inhibitory Protein / metabolism*
  • Phosphate-Binding Proteins
  • Salmonella Infections / metabolism
  • Salmonella Infections / microbiology
  • Salmonella typhimurium / physiology

Substances

  • Apoptosis Regulatory Proteins
  • Calcium-Binding Proteins
  • Eicosanoids
  • Gsdmd protein, mouse
  • Inflammasomes
  • Interleukin-18
  • Intracellular Signaling Peptides and Proteins
  • Ipaf protein, mouse
  • Naip1 protein, mouse
  • Neuronal Apoptosis-Inhibitory Protein
  • Phosphate-Binding Proteins
  • Caspase 8
  • Caspase 1