Metabolite-Sensing Receptor Ffar2 Regulates Colonic Group 3 Innate Lymphoid Cells and Gut Immunity

Immunity. 2019 Nov 19;51(5):871-884.e6. doi: 10.1016/j.immuni.2019.09.014. Epub 2019 Oct 15.

Abstract

Group 3 innate lymphoid cells (ILC3s) sense environmental signals that are critical for gut homeostasis and host defense. However, the metabolite-sensing G-protein-coupled receptors that regulate colonic ILC3s remain poorly understood. We found that colonic ILC3s expressed Ffar2, a microbial metabolite-sensing receptor, and that Ffar2 agonism promoted ILC3 expansion and function. Deficiency of Ffar2 in ILC3s decreased their in situ proliferation and ILC3-derived interleukin-22 (IL-22) production. This led to impaired gut epithelial function characterized by altered mucus-associated proteins and antimicrobial peptides and increased susceptibility to colonic injury and bacterial infection. Ffar2 increased IL-22+ CCR6+ ILC3s and influenced ILC3 abundance in colonic lymphoid tissues. Ffar2 agonism differentially activated AKT or ERK signaling and increased ILC3-derived IL-22 via an AKT and STAT3 axis. Our findings suggest that Ffar2 regulates colonic ILC3 proliferation and function, and they identify an ILC3-receptor signaling pathway modulating gut homeostasis and pathogen defense.

Keywords: AKT; CCR6; Ffar2(GPR43); IL-22; ILC3; SCFA; STAT3; colon; gut barrier integrity; innate lymphoid cell; metabolite-sensing GPCR.

Publication types

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

MeSH terms

  • Animals
  • Biomarkers
  • Cytokines / metabolism
  • Disease Susceptibility
  • Gastrointestinal Microbiome / immunology
  • Gene Expression
  • Humans
  • Immunity, Innate*
  • Immunity, Mucosal*
  • Immunomodulation
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / metabolism*
  • Intestinal Mucosa / pathology
  • Lymphocyte Activation / immunology
  • Lymphocytes / immunology*
  • Lymphocytes / metabolism*
  • Mice
  • Mice, Knockout
  • Proto-Oncogene Proteins c-akt
  • Receptors, Cell Surface / agonists
  • Receptors, Cell Surface / metabolism*
  • STAT3 Transcription Factor / metabolism

Substances

  • Biomarkers
  • Cytokines
  • FFA2R protein, human
  • Receptors, Cell Surface
  • STAT3 Transcription Factor
  • Proto-Oncogene Proteins c-akt