PKCε contributes to lipid-induced insulin resistance through cross talk with p70S6K and through previously unknown regulators of insulin signaling

Proc Natl Acad Sci U S A. 2018 Sep 18;115(38):E8996-E9005. doi: 10.1073/pnas.1804379115. Epub 2018 Sep 4.

Abstract

Insulin resistance drives the development of type 2 diabetes (T2D). In liver, diacylglycerol (DAG) is a key mediator of lipid-induced insulin resistance. DAG activates protein kinase C ε (PKCε), which phosphorylates and inhibits the insulin receptor. In rats, a 3-day high-fat diet produces hepatic insulin resistance through this mechanism, and knockdown of hepatic PKCε protects against high-fat diet-induced hepatic insulin resistance. Here, we employed a systems-level approach to uncover additional signaling pathways involved in high-fat diet-induced hepatic insulin resistance. We used quantitative phosphoproteomics to map global in vivo changes in hepatic protein phosphorylation in chow-fed, high-fat-fed, and high-fat-fed with PKCε knockdown rats to distinguish the impact of lipid- and PKCε-induced protein phosphorylation. This was followed by a functional siRNA-based screen to determine which dynamically regulated phosphoproteins may be involved in canonical insulin signaling. Direct PKCε substrates were identified by motif analysis of phosphoproteomics data and validated using a large-scale in vitro kinase assay. These substrates included the p70S6K substrates RPS6 and IRS1, which suggested cross talk between PKCε and p70S6K in high-fat diet-induced hepatic insulin resistance. These results identify an expanded set of proteins through which PKCε may drive high-fat diet-induced hepatic insulin resistance that may direct new therapeutic approaches for T2D.

Keywords: PKCε; cross talk; insulin resistance; phosphoproteomics; systems biology.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Diabetes Mellitus, Type 2 / etiology
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diet, High-Fat / adverse effects
  • Disease Models, Animal
  • Gene Knockdown Techniques
  • Humans
  • Insulin / metabolism*
  • Insulin Receptor Substrate Proteins / metabolism
  • Insulin Resistance / physiology*
  • Lipid Metabolism / physiology
  • Liver / metabolism
  • Phosphorylation
  • Protein Kinase C-epsilon / genetics
  • Protein Kinase C-epsilon / metabolism*
  • Proteomics / methods
  • RNA, Small Interfering / metabolism
  • Rats
  • Receptor, Insulin / metabolism
  • Ribosomal Protein S6 / metabolism
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism*
  • Signal Transduction / physiology

Substances

  • Insulin
  • Insulin Receptor Substrate Proteins
  • RNA, Small Interfering
  • Ribosomal Protein S6
  • Receptor, Insulin
  • Ribosomal Protein S6 Kinases, 70-kDa
  • ribosomal protein S6 kinase, 70kD, polypeptide 2
  • Protein Kinase C-epsilon