Microbiota tryptophan metabolism induces aryl hydrocarbon receptor activation and improves alcohol-induced liver injury

Gut. 2021 Jul;70(7):1299-1308. doi: 10.1136/gutjnl-2020-321565. Epub 2020 Oct 1.

Abstract

Objective: Chronic alcohol consumption is an important cause of liver-related deaths. Specific intestinal microbiota profiles are associated with susceptibility or resistance to alcoholic liver disease in both mice and humans. We aimed to identify the mechanisms by which targeting intestinal microbiota can improve alcohol-induced liver lesions.

Design: We used human associated mice, a mouse model of alcoholic liver disease transplanted with the intestinal microbiota of alcoholic patients and used the prebiotic, pectin, to modulate the intestinal microbiota. Based on metabolomic analyses, we focused on microbiota tryptophan metabolites, which are ligands of the aryl hydrocarbon receptor (AhR). Involvement of the AhR pathway was assessed using both a pharmacological approach and AhR-deficient mice.

Results: Pectin treatment modified the microbiome and metabolome in human microbiota-associated alcohol-fed mice, leading to a specific faecal signature. High production of bacterial tryptophan metabolites was associated with an improvement of liver injury. The AhR agonist Ficz (6-formylindolo (3,2-b) carbazole) reduced liver lesions, similarly to prebiotic treatment. Conversely, inactivation of the ahr gene in alcohol-fed AhR knock-out mice abrogated the beneficial effects of the prebiotic. Importantly, patients with severe alcoholic hepatitis have low levels of bacterial tryptophan derivatives that are AhR agonists.

Conclusions: Improvement of alcoholic liver disease by targeting the intestinal microbiota involves the AhR pathway, which should be considered as a new therapeutic target.

Keywords: alcohol-induced injury; alcoholic liver disease; intestinal bacteria; mucus; prebiotic.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / agonists
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Carbazoles / pharmacology
  • Disease Models, Animal
  • Fecal Microbiota Transplantation
  • Feces / chemistry
  • Female
  • Humans
  • Intestines / microbiology*
  • Intestines / physiopathology
  • Liver Diseases, Alcoholic / drug therapy
  • Liver Diseases, Alcoholic / etiology*
  • Liver Diseases, Alcoholic / metabolism
  • Metabolome / drug effects
  • Mice
  • Mice, Knockout
  • Microbiota / drug effects
  • Microbiota / physiology*
  • Pectins / pharmacology*
  • Pectins / therapeutic use
  • Prebiotics
  • Receptors, Aryl Hydrocarbon / agonists
  • Receptors, Aryl Hydrocarbon / genetics
  • Receptors, Aryl Hydrocarbon / metabolism*
  • Tryptophan / metabolism*

Substances

  • 6-formylindolo(3,2-b)carbazole
  • Ahr protein, mouse
  • Basic Helix-Loop-Helix Transcription Factors
  • Carbazoles
  • Prebiotics
  • Receptors, Aryl Hydrocarbon
  • Pectins
  • Tryptophan