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A Membrane-Bound Diacylglycerol Species Induces PKCϵ-Mediated Hepatic Insulin Resistance

Cell Metab. 2020 Oct 6;32(4):654-664.e5. doi: 10.1016/j.cmet.2020.08.001. Epub 2020 Sep 2.

Abstract

Nonalcoholic fatty liver disease is strongly associated with hepatic insulin resistance (HIR); however, the key lipid species and molecular mechanisms linking these conditions are widely debated. We developed a subcellular fractionation method to quantify diacylglycerol (DAG) stereoisomers and ceramides in the endoplasmic reticulum (ER), mitochondria, plasma membrane (PM), lipid droplets, and cytosol. Acute knockdown (KD) of diacylglycerol acyltransferase-2 in liver induced HIR in rats. This was due to PM sn-1,2-DAG accumulation, which promoted PKCϵ activation and insulin receptor kinase (IRK)-T1160 phosphorylation, resulting in decreased IRK-Y1162 phosphorylation. Liver PM sn-1,2-DAG content and IRK-T1160 phosphorylation were also higher in humans with HIR. In rats, liver-specific PKCϵ KD ameliorated high-fat diet-induced HIR by lowering IRK-T1160 phosphorylation, while liver-specific overexpression of constitutively active PKCϵ-induced HIR by promoting IRK-T1160 phosphorylation. These data identify PM sn-1,2-DAGs as the key pool of lipids that activate PKCϵ and that hepatic PKCϵ is both necessary and sufficient in mediating HIR.

Keywords: ceramides; dicylglycerols; hepatic glucose production; hepatic glycogen synthesis; hepatic insulin resistance; insulin receptor phosphorylation; liquid chromatography-tandem mass spectrometry; nonalcoholic fatty liver disease; protein kinase C-epsilon; type 2 diabetes.

Publication types

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

MeSH terms

  • Animals
  • Cell Membrane / chemistry*
  • Cell Membrane / metabolism
  • Diglycerides / chemistry
  • Diglycerides / metabolism*
  • Humans
  • Insulin Resistance
  • Liver / metabolism*
  • Male
  • Phosphorylation
  • Protein Kinase C-epsilon / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Insulin / metabolism

Substances

  • 1,2-diacylglycerol
  • Diglycerides
  • Receptor, Insulin
  • Protein Kinase C-epsilon