The microRNA-342-5p fosters inflammatory macrophage activation through an Akt1- and microRNA-155-dependent pathway during atherosclerosis

Circulation. 2013 Apr 16;127(15):1609-19. doi: 10.1161/CIRCULATIONAHA.112.000736. Epub 2013 Mar 19.

Abstract

Background: Atherosclerosis is a chronic inflammatory vascular disease driven by the subendothelial accumulation of macrophages. The mechanism regulating the inflammatory response in macrophages during atherogenesis remains unclear. Because microRNAs (miRNAs) play a crucial role in cellular signaling by posttranscriptional regulation of gene expression, we studied the miRNA expression profiles during the progression of atherosclerosis.

Methods and results: Using an miRNA real-time polymerase chain reaction array, we found that macrophage-derived miR-342-5p and miR-155 are selectively upregulated in early atherosclerotic lesions in Apoe(-/-) mice. miR-342-5p directly targets Akt1 through its 3'-untranslated region. Akt1 suppression by miR-342-5p induces proinflammatory mediators such as Nos2 and II6 in macrophages via the upregulation of miR-155. The local application of an miR-342-5p antagomir inhibits the development of atherosclerosis in partially ligated carotid arteries. In atherosclerotic lesions, the miR-342-5p antagomir upregulated Akt1 expression and suppressed the expression of miR-155 and Nos2. This reduced Nos2 expression was associated with a diminished generation of nitrotyrosine in the plaques. Furthermore, systemic treatment with an inhibitor of miR-342-5p reduced the progression of atherosclerosis in the aorta of Apoe(-/-) mice.

Conclusions: Macrophage-derived miR-342-5p promotes atherosclerosis and enhances the inflammatory stimulation of macrophages by suppressing the Akt1-mediated inhibition of miR-155 expression. Therefore, targeting miR-342-5p may offer a promising strategy to treat atherosclerotic vascular disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aortic Diseases / genetics
  • Aortic Diseases / pathology
  • Aortic Diseases / physiopathology
  • Apolipoproteins E / deficiency
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology*
  • Atherosclerosis / physiopathology
  • Bone Morphogenetic Protein Receptors, Type II / biosynthesis
  • Bone Morphogenetic Protein Receptors, Type II / genetics
  • Carotid Stenosis / genetics
  • Carotid Stenosis / pathology
  • Carotid Stenosis / physiopathology
  • Carotid Stenosis / prevention & control
  • Chemokine CCL2 / biosynthesis
  • Chemokine CCL2 / genetics
  • DEAD-box RNA Helicases / deficiency
  • DEAD-box RNA Helicases / genetics
  • Disease Progression
  • Gene Expression Regulation* / drug effects
  • Interleukin-6 / biosynthesis
  • Interleukin-6 / genetics
  • Macrophage Activation*
  • Macrophages / metabolism
  • Mice
  • Mice, Knockout
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / biosynthesis
  • MicroRNAs / genetics
  • MicroRNAs / physiology*
  • Nitric Oxide Synthase Type II / biosynthesis
  • Nitric Oxide Synthase Type II / genetics
  • Oligonucleotides / pharmacology
  • Oligonucleotides / therapeutic use
  • Proto-Oncogene Proteins c-akt / physiology*
  • RNA, Antisense / pharmacology
  • RNA, Antisense / therapeutic use
  • Ribonuclease III / deficiency
  • Ribonuclease III / genetics
  • Signal Transduction / physiology
  • Tyrosine / analogs & derivatives
  • Tyrosine / metabolism
  • Up-Regulation
  • Vasculitis / genetics
  • Vasculitis / pathology*
  • Vasculitis / physiopathology

Substances

  • Apolipoproteins E
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Interleukin-6
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • Mirn342 microRNA, mouse
  • Oligonucleotides
  • RNA, Antisense
  • locked nucleic acid
  • 3-nitrotyrosine
  • Tyrosine
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Akt1 protein, mouse
  • Proto-Oncogene Proteins c-akt
  • Bmpr2 protein, mouse
  • Bone Morphogenetic Protein Receptors, Type II
  • Dicer1 protein, mouse
  • Ribonuclease III
  • DEAD-box RNA Helicases