Paigen diet-fed apolipoprotein E knockout mice develop severe pulmonary hypertension in an interleukin-1-dependent manner

Am J Pathol. 2011 Oct;179(4):1693-705. doi: 10.1016/j.ajpath.2011.06.037. Epub 2011 Aug 9.

Abstract

Inflammatory mechanisms are proposed to play a significant role in the pathogenesis of pulmonary arterial hypertension (PAH). Previous studies have described PAH in fat-fed apolipoprotein E knockout (ApoE(-/-)) mice. We have reported that signaling in interleukin-1-receptor-knockout (IL-1R1(-/-)) mice leads to a reduction in diet-induced systemic atherosclerosis. We subsequently hypothesized that double-null (ApoE(-/-)/IL-1R1(-/-)) mice would show a reduced PAH phenotype compared with that of ApoE(-/-) mice. Male IL-1R1(-/-), ApoE(-/-), and ApoE(-/-)/IL-1R1(-/-) mice were fed regular chow or a high-fat diet (Paigen diet) for 8 weeks before phenotyping for PAH. No abnormal phenotype was observed in the IL-1R1(-/-) mice. Fat-fed ApoE(-/-) mice developed significantly increased right ventricular systolic pressure and substantial pulmonary vascular remodeling. Surprisingly, ApoE(-/-)/IL-1R1(-/-) mice showed an even more severe PAH phenotype. Further molecular investigation revealed the expression of a putative, alternatively primed IL-1R1 transcript expressed within the lungs but not aorta of ApoE(-/-)/IL-1R1(-/-) mice. Treatment of ApoE(-/-) and ApoE(-/-)/IL-1R1(-/-) mice with IL-1-receptor antagonist prevented progression of the PAH phenotype in both strains. Blocking IL-1 signaling may have beneficial effects in treating PAH, and alternative IL-1-receptor signaling in the lung may be important in driving PAH pathogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apolipoproteins E / deficiency*
  • Apolipoproteins E / metabolism
  • Biomarkers / metabolism
  • Diet, High-Fat / adverse effects*
  • Disease Progression
  • Feeding Behavior / drug effects
  • Hemodynamics / drug effects
  • Hypertension, Pulmonary / complications
  • Hypertension, Pulmonary / drug therapy
  • Hypertension, Pulmonary / pathology*
  • Hypertension, Pulmonary / physiopathology
  • Hypertrophy, Right Ventricular / complications
  • Hypertrophy, Right Ventricular / pathology
  • Hypertrophy, Right Ventricular / physiopathology
  • Inflammation Mediators / metabolism
  • Interleukin 1 Receptor Antagonist Protein / pharmacology
  • Interleukin 1 Receptor Antagonist Protein / therapeutic use
  • Interleukin-1 / metabolism*
  • Lung / drug effects
  • Lung / pathology
  • Lung / physiopathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Organ Size / drug effects
  • Osteoprotegerin / metabolism
  • Phenotype
  • Pulmonary Artery / pathology
  • Pulmonary Artery / physiopathology
  • Receptors, Interleukin-1 / deficiency
  • Receptors, Interleukin-1 / metabolism
  • TNF-Related Apoptosis-Inducing Ligand / metabolism
  • Up-Regulation / drug effects
  • Ventricular Function, Right / drug effects
  • Ventricular Remodeling / drug effects

Substances

  • Apolipoproteins E
  • Biomarkers
  • Inflammation Mediators
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1
  • Osteoprotegerin
  • Receptors, Interleukin-1
  • TNF-Related Apoptosis-Inducing Ligand