Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis

Circ Res. 2014 Mar 14;114(6):947-56. doi: 10.1161/CIRCRESAHA.114.303312. Epub 2014 Jan 14.

Abstract

Rationale: Neutrophil extracellular trap (NET) formation promotes vascular damage, thrombosis, and activation of interferon-α-producing plasmacytoid dendritic cells in diseased arteries. Peptidylarginine deiminase inhibition is a strategy that can decrease in vivo NET formation.

Objective: To test whether peptidylarginine deiminase inhibition, a novel approach to targeting arterial disease, can reduce vascular damage and inhibit innate immune responses in murine models of atherosclerosis.

Methods and results: Apolipoprotein-E (Apoe)(-/-) mice demonstrated enhanced NET formation, developed autoantibodies to NETs, and expressed high levels of interferon-α in diseased arteries. Apoe(-/-) mice were treated for 11 weeks with daily injections of Cl-amidine, a peptidylarginine deiminase inhibitor. Peptidylarginine deiminase inhibition blocked NET formation, reduced atherosclerotic lesion area, and delayed time to carotid artery thrombosis in a photochemical injury model. Decreases in atherosclerosis burden were accompanied by reduced recruitment of netting neutrophils and macrophages to arteries, as well as by reduced arterial interferon-α expression.

Conclusions: Pharmacological interventions that block NET formation can reduce atherosclerosis burden and arterial thrombosis in murine systems. These results support a role for aberrant NET formation in the pathogenesis of atherosclerosis through modulation of innate immune responses.

Keywords: atherosclerosis; immunology; interferon-α; neutrophils; protein-arginine deiminase; thrombosis.

Publication types

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

MeSH terms

  • Animals
  • Aortic Diseases / drug therapy
  • Aortic Diseases / etiology
  • Aortic Diseases / pathology
  • Aortic Diseases / prevention & control
  • Apolipoproteins E / deficiency
  • Atherosclerosis / drug therapy
  • Atherosclerosis / enzymology
  • Atherosclerosis / etiology
  • Atherosclerosis / immunology
  • Atherosclerosis / pathology
  • Atherosclerosis / prevention & control*
  • Autoantibodies / biosynthesis
  • Autoantibodies / immunology
  • Citrulline / analysis
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Drug Evaluation, Preclinical
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use*
  • Extracellular Space
  • Histones / metabolism
  • Hydrolases / antagonists & inhibitors*
  • Hydrolases / physiology
  • Immunity, Innate / drug effects*
  • Interferon-alpha / biosynthesis
  • Interferon-alpha / genetics
  • L-Selectin / analysis
  • Lipids / blood
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutropenia / immunology
  • Neutrophils / drug effects
  • Neutrophils / immunology
  • Neutrophils / ultrastructure
  • Ornithine / analogs & derivatives*
  • Ornithine / pharmacology
  • Ornithine / therapeutic use
  • Photochemical Processes
  • Protein Processing, Post-Translational / drug effects
  • Protein-Arginine Deiminase Type 4
  • Receptor, Interferon alpha-beta / deficiency
  • Sinus of Valsalva / pathology
  • Tunica Intima / pathology

Substances

  • Apolipoproteins E
  • Autoantibodies
  • Enzyme Inhibitors
  • Histones
  • Interferon-alpha
  • Lipids
  • N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide
  • L-Selectin
  • Receptor, Interferon alpha-beta
  • Citrulline
  • Ornithine
  • Hydrolases
  • Protein-Arginine Deiminase Type 4
  • peptidylarginine deiminase 4, mouse