Lipid and insulin infusion-induced skeletal muscle insulin resistance is likely due to metabolic feedback and not changes in IRS-1, Akt, or AS160 phosphorylation

Am J Physiol Endocrinol Metab. 2009 Jul;297(1):E67-75. doi: 10.1152/ajpendo.90945.2008. Epub 2009 Apr 14.

Abstract

Type 2 diabetes is characterized by hyperlipidemia, hyperinsulinemia, and insulin resistance. The aim of this study was to investigate whether acute hyperlipidemia-induced insulin resistance in the presence of hyperinsulinemia was due to defective insulin signaling. Hyperinsulinemia (approximately 300 mU/l) with hyperlipidemia or glycerol (control) was produced in cannulated male Wistar rats for 0.5, 1 h, 3 h, or 5 h. The glucose infusion rate required to maintain euglycemia was significantly reduced by 3 h with lipid infusion and was further reduced after 5 h of infusion, with no difference in plasma insulin levels, indicating development of insulin resistance. Consistent with this finding, in vivo skeletal muscle glucose uptake (31%, P < 0.05) and glycogen synthesis rate (38%, P < 0.02) were significantly reduced after 5 h compared with 3 h of lipid infusion. Despite the development of insulin resistance, there was no difference in the phosphorylation state of multiple insulin-signaling intermediates or muscle diacylglyceride and ceramide content over the same time course. However, there was an increase in cumulative exposure to long-chain acyl-CoA (70%) with lipid infusion. Interestingly, although muscle pyruvate dehydrogenase kinase 4 protein content was decreased in hyperinsulinemic glycerol-infused rats, this decrease was blunted in muscle from hyperinsulinemic lipid-infused rats. Decreased pyruvate dehydrogenase complex activity was also observed in lipid- and insulin-infused animals (43%). Overall, these results suggest that acute reductions in muscle glucose metabolism in rats with hyperlipidemia and hyperinsulinemia are more likely a result of substrate competition than a significant early defect in insulin action or signaling.

Publication types

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

MeSH terms

  • Animals
  • Blood Glucose / analysis
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism
  • Feedback, Physiological / drug effects
  • Feedback, Physiological / physiology*
  • GTPase-Activating Proteins / metabolism*
  • Glycogen / metabolism
  • Infusions, Intravenous
  • Insulin / administration & dosage
  • Insulin / blood
  • Insulin / pharmacology*
  • Insulin Receptor Substrate Proteins / metabolism*
  • Insulin Resistance* / physiology
  • Lipids / administration & dosage
  • Lipids / blood
  • Lipids / pharmacology*
  • Male
  • Metabolic Networks and Pathways / drug effects
  • Muscle, Skeletal / drug effects*
  • Muscle, Skeletal / metabolism
  • Oncogene Protein v-akt / metabolism*
  • Phosphorylation / drug effects
  • Rats
  • Rats, Wistar

Substances

  • Blood Glucose
  • GTPase-Activating Proteins
  • Insulin
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, rat
  • Lipids
  • TBC1D4 protein, rat
  • Glycogen
  • Oncogene Protein v-akt