Lipids activate skeletal muscle mitochondrial fission and quality control networks to induce insulin resistance in humans

Metabolism. 2021 Aug:121:154803. doi: 10.1016/j.metabol.2021.154803. Epub 2021 Jun 4.

Abstract

Background and aims: A diminution in skeletal muscle mitochondrial function due to ectopic lipid accumulation and excess nutrient intake is thought to contribute to insulin resistance and the development of type 2 diabetes. However, the functional integrity of mitochondria in insulin-resistant skeletal muscle remains highly controversial.

Methods: 19 healthy adults (age:28.4 ± 1.7 years; BMI:22.7 ± 0.3 kg/m2) received an overnight intravenous infusion of lipid (20% Intralipid) or saline followed by a hyperinsulinemic-euglycemic clamp to assess insulin sensitivity using a randomized crossover design. Skeletal muscle biopsies were obtained after the overnight lipid infusion to evaluate activation of mitochondrial dynamics proteins, ex-vivo mitochondrial membrane potential, ex-vivo oxidative phosphorylation and electron transfer capacity, and mitochondrial ultrastructure.

Results: Overnight lipid infusion increased dynamin related protein 1 (DRP1) phosphorylation at serine 616 and PTEN-induced kinase 1 (PINK1) expression (P = 0.003 and P = 0.008, respectively) in skeletal muscle while reducing mitochondrial membrane potential (P = 0.042). The lipid infusion also increased mitochondrial-associated lipid droplet formation (P = 0.011), the number of dilated cristae, and the presence of autophagic vesicles without altering mitochondrial number or respiratory capacity. Additionally, lipid infusion suppressed peripheral glucose disposal (P = 0.004) and hepatic insulin sensitivity (P = 0.014).

Conclusions: These findings indicate that activation of mitochondrial fission and quality control occur early in the onset of insulin resistance in human skeletal muscle. Targeting mitochondrial dynamics and quality control represents a promising new pharmacological approach for treating insulin resistance and type 2 diabetes.

Clinical trial registration: NCT02697201, ClinicalTrials.gov.

Publication types

  • Randomized Controlled Trial
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Biopsy
  • Cell Respiration / drug effects
  • Emulsions / administration & dosage
  • Emulsions / pharmacology
  • Fatty Acids / administration & dosage
  • Fatty Acids / pharmacology
  • Female
  • Glucose Clamp Technique
  • Healthy Volunteers
  • Humans
  • Infusions, Intravenous
  • Insulin / metabolism*
  • Insulin Resistance / physiology
  • Lipid Metabolism / drug effects
  • Lipid Metabolism / physiology
  • Lipids / administration & dosage
  • Lipids / pharmacology*
  • Male
  • Metabolic Networks and Pathways / drug effects
  • Mitochondria, Muscle / drug effects*
  • Mitochondria, Muscle / pathology
  • Mitochondria, Muscle / physiology
  • Mitochondrial Dynamics / drug effects*
  • Muscle, Skeletal / drug effects
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / pathology
  • Phospholipids / administration & dosage
  • Phospholipids / pharmacology
  • Soybean Oil / administration & dosage
  • Soybean Oil / pharmacology

Substances

  • Emulsions
  • Fatty Acids
  • Insulin
  • Lipids
  • Phospholipids
  • soybean oil, phospholipid emulsion
  • Soybean Oil

Associated data

  • ClinicalTrials.gov/NCT02697201