Cyclooxygenase-2 in endothelial and vascular smooth muscle cells restrains atherogenesis in hyperlipidemic mice

Circulation. 2014 Apr 29;129(17):1761-9. doi: 10.1161/CIRCULATIONAHA.113.007913. Epub 2014 Feb 11.

Abstract

Background: Placebo-controlled trials of nonsteroidal anti-inflammatory drugs selective for inhibition of cyclooxygenase-2 (COX-2) reveal an emergent cardiovascular hazard in patients selected for low risk of heart disease. Postnatal global deletion of COX-2 accelerates atherogenesis in hyperlipidemic mice, a process delayed by selective enzyme deletion in macrophages.

Methods and results: In the present study, selective depletion of COX-2 in vascular smooth muscle cells and endothelial cells depressed biosynthesis of prostaglandin I2 and prostaglandin E2, elevated blood pressure, and accelerated atherogenesis in Ldlr knockout mice. Deletion of COX-2 in vascular smooth muscle cells and endothelial cells coincided with an increase in COX-2 expression in lesional macrophages and increased biosynthesis of thromboxane. Increased accumulation of less organized intimal collagen, laminin, α-smooth muscle actin, and matrix-rich fibrosis was also apparent in lesions of the mutants.

Conclusions: Although atherogenesis is accelerated in global COX-2 knockouts, consistent with evidence of risk transformation during chronic nonsteroidal anti-inflammatory drug administration, this masks the contrasting effects of enzyme depletion in macrophages versus vascular smooth muscle cells and endothelial cells. Targeting delivery of COX-2 inhibitors to macrophages may conserve their efficacy while limiting cardiovascular risk.

Keywords: atherogenesis; cyclooxygenase; endothelial cell; prostaglandin; vascular smooth muscle.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Aorta, Thoracic / enzymology
  • Aorta, Thoracic / pathology
  • Atherosclerosis / epidemiology
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology
  • Blood Pressure / physiology
  • Cyclooxygenase 2 / genetics*
  • Cyclooxygenase 2 / metabolism
  • Diet, Atherogenic
  • Dietary Fats / pharmacology
  • Dinoprostone / biosynthesis
  • Endothelium, Vascular / enzymology*
  • Endothelium, Vascular / pathology
  • Epoprostenol / biosynthesis
  • Female
  • Hyperlipidemias / epidemiology
  • Hyperlipidemias / metabolism*
  • Hyperlipidemias / pathology
  • Macrophages / enzymology
  • Macrophages / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Smooth, Vascular / enzymology*
  • Muscle, Smooth, Vascular / pathology
  • Receptors, LDL / genetics
  • Risk Factors

Substances

  • Dietary Fats
  • Receptors, LDL
  • Epoprostenol
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2
  • Dinoprostone