Acetyl-CoA Derived from Hepatic Peroxisomal β-Oxidation Inhibits Autophagy and Promotes Steatosis via mTORC1 Activation

Mol Cell. 2020 Jul 2;79(1):30-42.e4. doi: 10.1016/j.molcel.2020.05.007. Epub 2020 May 29.

Abstract

Autophagy is activated by prolonged fasting but cannot overcome the ensuing hepatic lipid overload, resulting in fatty liver. Here, we describe a peroxisome-lysosome metabolic link that restricts autophagic degradation of lipids. Acyl-CoA oxidase 1 (Acox1), the enzyme that catalyzes the first step in peroxisomal β-oxidation, is enriched in liver and further increases with fasting or high-fat diet (HFD). Liver-specific Acox1 knockout (Acox1-LKO) protected mice against hepatic steatosis caused by starvation or HFD due to induction of autophagic degradation of lipid droplets. Hepatic Acox1 deficiency markedly lowered total cytosolic acetyl-CoA levels, which led to decreased Raptor acetylation and reduced lysosomal localization of mTOR, resulting in impaired activation of mTORC1, a central regulator of autophagy. Dichloroacetic acid treatment elevated acetyl-CoA levels, restored mTORC1 activation, inhibited autophagy, and increased hepatic triglycerides in Acox1-LKO mice. These results identify peroxisome-derived acetyl-CoA as a key metabolic regulator of autophagy that controls hepatic lipid homeostasis.

Keywords: Acox1; Autophagy; Lipid metabolism; NAFLD; Raptor; fatty acid oxidation; lipophagy; mTOR; peroxisomes.

Publication types

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

MeSH terms

  • Acetyl Coenzyme A / metabolism*
  • Acetylation
  • Acyl-CoA Oxidase / physiology*
  • Animals
  • Autophagy*
  • Autophagy-Related Protein 5 / physiology
  • Diet, High-Fat / adverse effects
  • Fasting
  • Fatty Acids / chemistry*
  • Fatty Liver / etiology
  • Fatty Liver / metabolism
  • Fatty Liver / pathology*
  • Female
  • Male
  • Mechanistic Target of Rapamycin Complex 1 / genetics
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Mice
  • Mice, Knockout
  • Mitochondria / metabolism
  • Oxidation-Reduction
  • Peroxisomes / chemistry*
  • Peroxisomes / metabolism
  • Regulatory-Associated Protein of mTOR / genetics
  • Regulatory-Associated Protein of mTOR / metabolism

Substances

  • Atg5 protein, mouse
  • Autophagy-Related Protein 5
  • Fatty Acids
  • Regulatory-Associated Protein of mTOR
  • Rptor protein, mouse
  • Acetyl Coenzyme A
  • ACOX1 protein, mouse
  • Acyl-CoA Oxidase
  • Mechanistic Target of Rapamycin Complex 1