Exendin-4 decreases liver inflammation and atherosclerosis development simultaneously by reducing macrophage infiltration

Br J Pharmacol. 2014 Feb;171(3):723-34. doi: 10.1111/bph.12490.

Abstract

Background and purpose: The aetiology of inflammation in the liver and vessel wall, leading to non-alcoholic steatohepatitis (NASH) and atherosclerosis, respectively, shares common mechanisms including macrophage infiltration. To treat both disorders simultaneously, it is highly important to tackle the inflammatory status. Exendin-4, a glucagon-like peptide-1 (GLP-1) receptor agonist, reduces hepatic steatosis and has been suggested to reduce atherosclerosis; however, its effects on liver inflammation are underexplored. Here, we tested the hypothesis that exendin-4 reduces inflammation in both the liver and vessel wall, and investigated the common underlying mechanism.

Experimental approach: Female APOE*3-Leiden.CETP mice, a model with human-like lipoprotein metabolism, were fed a cholesterol-containing Western-type diet for 5 weeks to induce atherosclerosis and subsequently treated for 4 weeks with exendin-4.

Key results: Exendin-4 modestly improved dyslipidaemia, but markedly decreased atherosclerotic lesion severity and area (-33%), accompanied by a reduction in monocyte adhesion to the vessel wall (-42%) and macrophage content in the plaque (-44%). Furthermore, exendin-4 reduced hepatic lipid content and inflammation as well as hepatic CD68⁺ (-18%) and F4/80⁺ (-25%) macrophage content. This was accompanied by less monocyte recruitment from the circulation as the Mac-1⁺ macrophage content was decreased (-36%). Finally, exendin-4 reduced hepatic chemokine expression in vivo and suppressed oxidized low-density lipoprotein accumulation in peritoneal macrophages in vitro, effects dependent on the GLP-1 receptor.

Conclusions and implications: Exendin-4 reduces inflammation in both the liver and vessel wall by reducing macrophage recruitment and activation. These data suggest that exendin-4 could be a valuable strategy to treat NASH and atherosclerosis simultaneously.

Keywords: cholesterol; exendin-4; inflammation; macrophage content; monocyte recruitment; oxidized LDL.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / administration & dosage
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use*
  • Apolipoprotein E3 / genetics
  • Apolipoprotein E3 / metabolism
  • Atherosclerosis / etiology
  • Atherosclerosis / immunology
  • Atherosclerosis / pathology
  • Atherosclerosis / prevention & control*
  • Cholesterol Ester Transfer Proteins / genetics
  • Cholesterol Ester Transfer Proteins / metabolism
  • Diet, Atherogenic / adverse effects
  • Disease Models, Animal*
  • Drug Implants
  • Dyslipidemias / etiology
  • Dyslipidemias / immunology
  • Dyslipidemias / pathology
  • Dyslipidemias / prevention & control
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / immunology
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / pathology
  • Exenatide
  • Fatty Liver / etiology
  • Fatty Liver / immunology
  • Fatty Liver / pathology
  • Fatty Liver / prevention & control*
  • Female
  • Glucagon-Like Peptide-1 Receptor
  • Humans
  • Hypolipidemic Agents / administration & dosage
  • Hypolipidemic Agents / therapeutic use
  • Liver / drug effects*
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Macrophage Activation / drug effects*
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice
  • Mice, Transgenic
  • Non-alcoholic Fatty Liver Disease
  • Peptides / administration & dosage
  • Peptides / therapeutic use
  • Random Allocation
  • Receptors, Glucagon / antagonists & inhibitors
  • Receptors, Glucagon / metabolism
  • Venoms / administration & dosage
  • Venoms / therapeutic use

Substances

  • Anti-Inflammatory Agents, Non-Steroidal
  • Apolipoprotein E3
  • CETP protein, human
  • Cholesterol Ester Transfer Proteins
  • Drug Implants
  • GLP1R protein, human
  • Glp1r protein, mouse
  • Glucagon-Like Peptide-1 Receptor
  • Hypolipidemic Agents
  • Peptides
  • Receptors, Glucagon
  • Venoms
  • Exenatide