Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract

Gastroenterology. 2011 Jul;141(1):237-48, 248.e1. doi: 10.1053/j.gastro.2011.04.007. Epub 2011 Apr 16.

Abstract

Background & aims: The pathogenesis of inflammatory bowel disease (IBD) is believed to involve an altered balance between effector and regulatory T cells. Aryl hydrocarbon receptor (AhR), a ligand-dependent transcription factor that mediates the toxicity of dioxins, controls T-cell responses. We investigated the role of AhR in inflammation and pathogenesis of IBD in humans and mouse models.

Methods: AhR expression was evaluated in intestinal tissue samples from patients with IBD and controls by real-time polymerase chain reaction (PCR) and flow cytometry. Intestinal lamina propria mononuclear cells (LPMCs) were activated in the presence or absence of the AhR agonist 6-formylindolo(3, 2-b)carbazole (Ficz). Colitis was induced in mice using trinitrobenzene sulfonic acid (TNBS), dextran sulfate sodium (DSS), or T-cell transfer. Mice were given injections of Ficz or the AhR antagonist 2-metyl-2H-pyrazole-3-carboxylic acid; some mice first received injections of a blocking antibody against interleukin (IL)-22. Cytokines were quantified by real-time PCR and flow cytometry.

Results: Intestine tissue from patients with IBD expressed significantly less AhR than controls. In LPMCs from patients with IBD, incubation with Ficz reduced levels of interferon gamma (IFN)-γ and up-regulated IL-22. Mice injected with Ficz were protected against TNBS-, DSS-, and T-cell transfer-induced colitis; they had marked down-regulation of inflammatory cytokines and induction of IL-22. Mice given AhR antagonist produced more inflammatory cytokines and less IL-22 and developed a severe colitis. Neutralization of endogenous IL-22 disrupted the protective effect of Ficz on TNBS-induced colitis.

Conclusions: AhR is down-regulated in intestinal tissue of patients with IBD; AhR signaling, via IL-22, inhibits inflammation and colitis in the gastrointestinal tract of mice. AhR-related compounds might be developed to treat patients with IBDs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / drug effects
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Biopsy
  • Carbazoles / pharmacology
  • Case-Control Studies
  • Cells, Cultured
  • Dextran Sulfate
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Female
  • Flow Cytometry
  • Humans
  • Inflammation Mediators / metabolism
  • Inflammatory Bowel Diseases / chemically induced
  • Inflammatory Bowel Diseases / genetics
  • Inflammatory Bowel Diseases / immunology
  • Inflammatory Bowel Diseases / pathology
  • Inflammatory Bowel Diseases / prevention & control*
  • Interleukin-22
  • Interleukins / metabolism*
  • Intestines / drug effects
  • Intestines / immunology*
  • Intestines / pathology
  • Mice
  • Mice, Inbred BALB C
  • Middle Aged
  • Polymerase Chain Reaction
  • Receptors, Aryl Hydrocarbon / drug effects
  • Receptors, Aryl Hydrocarbon / metabolism*
  • Severity of Illness Index
  • Signal Transduction
  • T-Lymphocytes / transplantation
  • Time Factors
  • Trinitrobenzenesulfonic Acid
  • Up-Regulation

Substances

  • 6-formylindolo(3,2-b)carbazole
  • AHR protein, human
  • Ahr protein, mouse
  • Basic Helix-Loop-Helix Transcription Factors
  • Carbazoles
  • Inflammation Mediators
  • Interleukins
  • Receptors, Aryl Hydrocarbon
  • Trinitrobenzenesulfonic Acid
  • Dextran Sulfate