A glucagon-like peptide-1 analog reverses the molecular pathology and cardiac dysfunction of a mouse model of obesity

Circulation. 2013 Jan 1;127(1):74-85. doi: 10.1161/CIRCULATIONAHA.112.091215. Epub 2012 Nov 27.

Abstract

Background: Cardiac consequences of obesity include inflammation, hypertrophy, and compromised energy metabolism. Glucagon-like peptide-1 is an incretin hormone capable of cytoprotective actions that reduces inflammation and endoplasmic reticulum stress in other tissues. Here we examine the cardiac effects of the glucagon-like peptide-1 analog liraglutide in a model of obesity, independent of changes in body weight.

Methods and results: C57Bl6 mice were placed on a 45% high-fat diet (HFD) or a regular chow diet. Mice on HFD developed 46±2% and 60±2% greater body weight relative to regular chow diet-fed mice at 16 and 32 weeks, respectively (both P<0.0001), manifesting impaired glucose tolerance, insulin resistance, and cardiac ceramide accumulation by 16 weeks. One-week treatment with liraglutide (30 µg/kg twice daily) did not reduce body weight, but reversed insulin resistance, cardiac tumor necrosis factor-α expression, nuclear factor kappa B translocation, obesity-induced perturbations in cardiac endothelial nitric oxide synthase, connexin-43, and markers of hypertrophy and fibrosis, in comparison with placebo-treated HFD controls. Liraglutide improved the cardiac endoplasmic reticulum stress response and also improved cardiac function in animals on HFD by an AMP-activated protein kinase-dependent mechanism. Supporting a direct mechanism of action, liraglutide (100 nmol/L) prevented palmitate-induced lipotoxicity in isolated mouse cardiomyocytes and primary human coronary smooth muscle cells and prevented adhesion of human monocytes to tumor necrosis factor-α-activated human endothelial cells in vitro.

Conclusions: Weight-neutral treatment with a glucagon-like peptide-1 analog activates several cardioprotective pathways, prevents HFD-induced insulin resistance and inflammation, reduces monocyte vascular adhesion, and improves cardiac function in vivo by activating AMP-activated protein kinase. These data support a role for glucagon-like peptide-1 analogs in limiting the cardiovascular risks of obesity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Glucose / drug effects
  • Cardiotonic Agents / pharmacology*
  • Cell Line
  • Connexin 43 / genetics
  • Coronary Vessels / cytology
  • Disease Models, Animal
  • Endoplasmic Reticulum Stress / drug effects
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects
  • Gene Expression / drug effects
  • Glucagon-Like Peptide 1 / analogs & derivatives*
  • Glucagon-Like Peptide 1 / pharmacology
  • Heart Diseases / epidemiology
  • Heart Diseases / prevention & control*
  • Humans
  • Hypercholesterolemia / drug therapy
  • Hypercholesterolemia / epidemiology
  • Insulin Resistance
  • Liraglutide
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / cytology
  • Monocytes / drug effects
  • Muscle, Smooth, Vascular / cytology
  • Muscle, Smooth, Vascular / drug effects
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / drug effects
  • Nitric Oxide Synthase Type III / genetics
  • Obesity / drug therapy*
  • Obesity / epidemiology
  • Risk Factors
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Blood Glucose
  • Cardiotonic Agents
  • Connexin 43
  • Tumor Necrosis Factor-alpha
  • Liraglutide
  • Glucagon-Like Peptide 1
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse