Activation of AhR-NQO1 Signaling Pathway Protects Against Alcohol-Induced Liver Injury by Improving Redox Balance

Cell Mol Gastroenterol Hepatol. 2021;12(3):793-811. doi: 10.1016/j.jcmgh.2021.05.013. Epub 2021 May 31.

Abstract

Background & aims: Aryl hydrocarbon receptor (AhR) is a liver-enriched xenobiotic receptor that plays important role in detoxification response in liver. This study aimed to investigate how AhR signaling may impact the pathogenesis of alcohol-related liver disease (ALD).

Methods: Chronic alcohol feeding animal studies were conducted with mouse models of hepatocyte-specific AhR knockout (AhRΔhep) and NAD(P)H quinone dehydrogenase 1 (NQO1) overexpression, and dietary supplementation of the AhR ligand indole-3-carbinol. Cell studies were conducted to define the causal role of AhR and NQO1 in regulation of redox balance and apoptosis.

Results: Chronic alcohol consumption induced AhR activation and nuclear enrichment of NQO1 in hepatocytes of both alcoholic hepatitis patients and ALD mice. AhR deficiency exacerbated alcohol-induced liver injury, along with reduction of NQO1. Consistently, in vitro studies demonstrated that NQO1 expression was dependent on AhR. However, alcohol-induced NQO1 nuclear translocation was triggered by decreased cellular oxidized nicotinamide adenine dinucleotide (NAD+)-to-NADH ratio, rather than by AhR activation. Furthermore, both in vitro and in vivo overexpression NQO1 prevented alcohol-induced hepatic NAD+ depletion, thereby enhancing activities of NAD+-dependent enzymes and reversing alcohol-induced liver injury. In addition, therapeutic targeting of AhR in the liver with dietary indole-3-carbinol supplementation efficiently reversed alcoholic liver injury by AhR-NQO1 signaling activation.

Conclusions: This study demonstrated that AhR activation is a protective response to counteract alcohol-induced hepatic NAD+ depletion through induction of NQO1, and targeting the hepatic AhR-NQO1 pathway may serve as a novel therapeutic approach for ALD.

Keywords: AhR; Alcohol-Related Liver Disease; NAD(+)-to-NADH Ratio; NQO1.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetamides / metabolism
  • Animals
  • Apoptosis
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Biomarkers
  • Cells, Cultured
  • Chemical and Drug Induced Liver Injury / diagnosis
  • Chemical and Drug Induced Liver Injury / etiology*
  • Chemical and Drug Induced Liver Injury / metabolism*
  • Chemical and Drug Induced Liver Injury, Chronic / etiology
  • Chemical and Drug Induced Liver Injury, Chronic / metabolism
  • Chemical and Drug Induced Liver Injury, Chronic / pathology
  • Disease Models, Animal
  • Disease Susceptibility
  • Ethanol / adverse effects*
  • Gene Expression
  • Gene Knockdown Techniques
  • Hepatocytes / metabolism
  • Hepatocytes / pathology
  • Humans
  • Immunophenotyping
  • Mice
  • NAD(P)H Dehydrogenase (Quinone) / metabolism*
  • Organ Specificity
  • Oxidation-Reduction*
  • Oxidative Stress
  • Receptors, Aryl Hydrocarbon / metabolism*

Substances

  • AHR protein, human
  • Acetamides
  • Basic Helix-Loop-Helix Transcription Factors
  • Biomarkers
  • N,N'-diacetyl-1,6-diaminohexane
  • Receptors, Aryl Hydrocarbon
  • Ethanol
  • NAD(P)H Dehydrogenase (Quinone)
  • NQO1 protein, human