Loss of IL-10 signaling in macrophages limits bacterial killing driven by prostaglandin E2

J Exp Med. 2020 Feb 3;217(2):e20180649. doi: 10.1084/jem.20180649.

Abstract

Loss of IL-10 signaling in macrophages (Mφs) leads to inflammatory bowel disease (IBD). Induced pluripotent stem cells (iPSCs) were generated from an infantile-onset IBD patient lacking a functional IL10RB gene. Mφs differentiated from IL-10RB-/- iPSCs lacked IL-10RB mRNA expression, were unable to phosphorylate STAT3, and failed to reduce LPS induced inflammatory cytokines in the presence of exogenous IL-10. IL-10RB-/- Mφs exhibited a striking defect in their ability to kill Salmonella enterica serovar Typhimurium, which was rescuable after experimentally introducing functional copies of the IL10RB gene. Genes involved in synthesis and receptor pathways for eicosanoid prostaglandin E2 (PGE2) were more highly induced in IL-10RB-/- Mφs, and these Mφs produced higher amounts of PGE2 after LPS stimulation compared with controls. Furthermore, pharmacological inhibition of PGE2 synthesis and PGE2 receptor blockade enhanced bacterial killing in Mφs. These results identify a regulatory interaction between IL-10 and PGE2, dysregulation of which may drive aberrant Mφ activation and impaired host defense contributing to IBD pathogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Differentiation / genetics
  • Cells, Cultured
  • Dinoprostone / antagonists & inhibitors
  • Dinoprostone / metabolism*
  • Female
  • Gene Knockout Techniques
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammatory Bowel Diseases / metabolism*
  • Inflammatory Bowel Diseases / pathology
  • Interleukin-10 / metabolism*
  • Interleukin-10 Receptor alpha Subunit / genetics
  • Interleukin-10 Receptor beta Subunit / genetics
  • Interleukin-10 Receptor beta Subunit / metabolism*
  • Lipopolysaccharides / pharmacology
  • Macrophage Activation / drug effects
  • Macrophage Activation / genetics
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Mutation
  • Phosphorylation / genetics
  • STAT3 Transcription Factor / metabolism
  • Salmonella typhimurium / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*

Substances

  • IL10 protein, human
  • IL10RB protein, human
  • Interleukin-10 Receptor alpha Subunit
  • Interleukin-10 Receptor beta Subunit
  • Lipopolysaccharides
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Interleukin-10
  • Dinoprostone