Systemic delivery of microRNA-181b inhibits nuclear factor-κB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice

Circ Res. 2014 Jan 3;114(1):32-40. doi: 10.1161/CIRCRESAHA.113.302089. Epub 2013 Oct 1.

Abstract

Rationale: Activated nuclear factor (NF)-κB signaling in the vascular endothelium promotes the initiation and progression of atherosclerosis. Targeting endothelial NF-κB may provide a novel strategy to limit chronic inflammation.

Objective: To examine the role of microRNA-181b (miR-181b) in endothelial NF-κB signaling and effects on atherosclerosis.

Methods and results: MiR-181b expression was reduced in the aortic intima and plasma in apolipoprotein E-deficient mice fed a high-fat diet. Correspondingly, circulating miR-181b in the plasma was markedly reduced in human subjects with coronary artery disease. Systemic delivery of miR-181b resulted in a 2.3-fold overexpression of miR-181b in the aortic intima of apolipoprotein E-deficient mice and suppressed NF-κB signaling revealed by bioluminescence imaging and reduced target gene expression in the aortic arch in apolipoprotein E-deficient/NF-κB-luciferase transgenic mice. MiR-181b significantly inhibited atherosclerotic lesion formation, proinflammatory gene expression and the influx of lesional macrophages and CD4+ T cells in the vessel wall. Mechanistically, miR-181b inhibited the expression of the target gene importin-α3, an effect that reduced NF-κB nuclear translocation specifically in the vascular endothelium of lesions, whereas surprisingly leukocyte NF-κB signaling was unaffected despite a 7-fold overexpression of miR-181b. Our findings uncover that NF-κB nuclear translocation in leukocytes does not involve importin-α3, but rather importin-α5, which miR-181b does not target, highlighting that inhibition of NF-κB signaling in the endothelium is sufficient to mediate miR-181b's protective effects.

Conclusions: Systemic delivery of miR-181b inhibits the activation of NF-κB and atherosclerosis through cell-specific mechanisms in the vascular endothelium. These findings support the rationale that delivery of miR-181b may provide a novel therapeutic approach to treat chronic inflammatory diseases such as atherosclerosis.

Keywords: NF-κB; atherosclerosis; endothelial cells; inflammation; karyopherins; microRNAs.

MeSH terms

  • Animals
  • Aorta / metabolism*
  • Aorta / pathology
  • Apolipoproteins E / genetics
  • Atherosclerosis / etiology
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Atherosclerosis / therapy*
  • CD4-Positive T-Lymphocytes / metabolism
  • Diet, High-Fat / adverse effects
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Inflammation / metabolism
  • Karyopherins / genetics
  • Karyopherins / metabolism
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / administration & dosage
  • MicroRNAs / blood
  • MicroRNAs / metabolism
  • MicroRNAs / therapeutic use*
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / metabolism*
  • Tunica Intima / metabolism*
  • Tunica Intima / pathology

Substances

  • Apolipoproteins E
  • Karyopherins
  • MIrn181 microRNA, human
  • MicroRNAs
  • NF-kappa B
  • mirn181 microRNA, mouse