Fatty Acids Inhibit LAMP2-Mediated Autophagy Flux via Activating ER Stress Pathway in Alcohol-Related Liver Disease

Cell Mol Gastroenterol Hepatol. 2021;12(5):1599-1615. doi: 10.1016/j.jcmgh.2021.07.002. Epub 2021 Jul 17.

Abstract

Background & aims: Alcohol-related liver disease (ALD) is characterized by accumulation of hepatic free fatty acids (FFAs) and triglyceride (TG)-enriched lipid droplets and cell death. The present study aimed to investigate how FFA or TG induces hepatocyte injury, thereby contributing to the development of ALD.

Methods: Hepatocyte-specific DGAT1 knockout (DGAT1Δhep) mice and lysosome-associated membrane protein 2 (LAMP2) overexpression mice were generated and subjected to chronic alcohol feeding. Cell studies were conducted to define the causal role and underlying mechanism of FFA-induced hepatocellular injury.

Results: Hepatocyte-specific DGAT1 deletion exacerbated alcohol-induced liver injury by increasing lipid accumulation and endoplasmic reticulum (ER) stress, reducing LAMP2 protein levels, and impairing autophagy function. Cell studies revealed that FFAs, rather than TG, induced ER stress via ATF4 activation, which, in turn, down-regulated LAMP2, thereby impairing autophagy flux. LAMP2 overexpression in the liver restored autophagy function and ameliorated alcohol-induced liver injury in mice. Reducing hepatic FFAs by peroxisome proliferator-activated receptor α activation attenuated ER stress, restored LAMP2 protein levels, and improved autophagy flux. In addition, suppression of LAMP2 and autophagy function was also detected in the liver of patients with severe alcoholic hepatitis.

Conclusions: This study demonstrates that accumulation of hepatic FFAs, rather than TG, plays a crucial role in the pathogenesis of ALD by suppressing LAMP2-autophagy flux pathway through ER stress signaling, which represents an important mechanism of FFA-induced hepatocellular injury in ALD.

Keywords: Alcohol-Induced Liver Injury; Autophagy; DGAT1; Free Fatty Acid; Lipotoxicity.

Publication types

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

MeSH terms

  • Animals
  • Autophagy* / genetics
  • Biomarkers
  • Diacylglycerol O-Acyltransferase / metabolism
  • Disease Models, Animal
  • Disease Susceptibility
  • Endoplasmic Reticulum Stress*
  • Fatty Acids / metabolism*
  • Hepatocytes / metabolism
  • Humans
  • Lipid Metabolism
  • Liver Diseases, Alcoholic / etiology*
  • Liver Diseases, Alcoholic / metabolism*
  • Liver Diseases, Alcoholic / pathology
  • Liver Function Tests
  • Lysosomal-Associated Membrane Protein 2 / genetics*
  • Lysosomal-Associated Membrane Protein 2 / metabolism
  • Mice
  • Mice, Knockout
  • Models, Biological
  • Signal Transduction*

Substances

  • Biomarkers
  • Fatty Acids
  • LAMP2 protein, human
  • Lysosomal-Associated Membrane Protein 2
  • Dgat1 protein, mouse
  • Diacylglycerol O-Acyltransferase