Synthetic farnesoid X receptor agonists induce high-density lipoprotein-mediated transhepatic cholesterol efflux in mice and monkeys and prevent atherosclerosis in cholesteryl ester transfer protein transgenic low-density lipoprotein receptor (-/-) mice

J Pharmacol Exp Ther. 2012 Dec;343(3):556-67. doi: 10.1124/jpet.112.196519. Epub 2012 Aug 23.

Abstract

Farnesoid X receptor (FXR), a bile acid-activated nuclear hormone receptor, plays an important role in the regulation of cholesterol and more specifically high-density lipoprotein (HDL) homeostasis. Activation of FXR is reported to lead to both pro- and anti-atherosclerotic effects. In the present study we analyzed the impact of different FXR agonists on cholesterol homeostasis, plasma lipoprotein profiles, and transhepatic cholesterol efflux in C57BL/6J mice and cynomolgus monkeys and atherosclerosis development in cholesteryl ester transfer protein transgenic (CETPtg) low-density lipoprotein receptor (LDLR) (-/-) mice. In C57BL/6J mice on a high-fat diet the synthetic FXR agonists isopropyl 3-(3,4-difluorobenzoyl)-1,1-dimethyl-1,2,3,6-tetrahydroazepino[4,5-b]indole-5-carboxylate (FXR-450) and 4-[2-[2-chloro-4-[[5-cyclopropyl-3-(2,6-dichlorophenyl)-4-isoxazolyl]methoxy]phenyl]cyclopropyl]benzoic acid (PX20606) demonstrated potent plasma cholesterol-lowering activity that affected all lipoprotein species, whereas 3-[2-[2-chloro-4-[[3-(2,6-dichlorophenyl)-5-(1-methylethyl)-4-isoxazolyl]methoxy]phenyl]ethenyl]benzoic acid (GW4064) and 6-ethyl chenodeoxycholic acid (6-ECDCA) showed only limited effects. In FXR wild-type mice, but not FXR(-/-) mice, the more efficacious FXR agonists increased fecal cholesterol excretion and reduced intestinal cholesterol (re)uptake. In CETPtg-LDLR(-/-) mice PX20606 potently lowered total cholesterol and, despite the observed HDL cholesterol (HDLc) reduction, caused a highly significant decrease in atherosclerotic plaque size. In normolipidemic cynomolgus monkeys PX20606 and 6-ECDCA both reduced total cholesterol, and PX20606 specifically lowered HDL(2c) but not HDL(3c) or apolipoprotein A1. That pharmacological FXR activation specifically affects this cholesterol-rich HDL(2) subclass is a new and highly interesting finding and sheds new light on FXR-dependent HDLc lowering, which has been perceived as a major limitation for the clinical development of FXR agonists.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anticholesteremic Agents / chemistry
  • Anticholesteremic Agents / pharmacology*
  • Anticholesteremic Agents / therapeutic use
  • Aorta / drug effects
  • Aorta / metabolism
  • Aorta / pathology
  • Atherosclerosis / blood
  • Atherosclerosis / metabolism
  • Atherosclerosis / prevention & control*
  • Benzoates / chemistry
  • Benzoates / pharmacology*
  • Benzoates / therapeutic use
  • Biological Transport
  • Cholesterol / administration & dosage
  • Cholesterol / blood*
  • Cholesterol / metabolism
  • Cholesterol Ester Transfer Proteins / genetics
  • Cholesterol Ester Transfer Proteins / metabolism*
  • Diet, High-Fat
  • Disease Models, Animal
  • Feces / chemistry
  • Female
  • Humans
  • Isoxazoles / chemistry
  • Isoxazoles / pharmacology*
  • Isoxazoles / therapeutic use
  • Lipoproteins, HDL / blood*
  • Liver / drug effects*
  • Liver / metabolism
  • Macaca fascicularis
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Molecular Structure
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Cytoplasmic and Nuclear / agonists*
  • Receptors, LDL / genetics
  • Receptors, LDL / metabolism*
  • Species Specificity
  • Structure-Activity Relationship

Substances

  • 4-(((6-((5-cyclopropyl-3-(2,6-dichlorophenyl)-4-isoxazolyl)methoxy)-2-(trifluoromethyl)-3-pyridinyl)methylamino)methyl)benzoic acid
  • 4-(2-(2-chloro-4-((5-cyclopropyl-3-(2,6-dichlorophenyl)-4-isoxazolyl)methoxy)phenyl)cyclopropyl)benzoic acid
  • Anticholesteremic Agents
  • Benzoates
  • Cholesterol Ester Transfer Proteins
  • Isoxazoles
  • Lipoproteins, HDL
  • Receptors, Cytoplasmic and Nuclear
  • Receptors, LDL
  • farnesoid X-activated receptor
  • Cholesterol