Nanoparticle-mediated delivery of pitavastatin inhibits atherosclerotic plaque destabilization/rupture in mice by regulating the recruitment of inflammatory monocytes

Circulation. 2014 Feb 25;129(8):896-906. doi: 10.1161/CIRCULATIONAHA.113.002870. Epub 2013 Dec 4.

Abstract

Background: Preventing atherosclerotic plaque destabilization and rupture is the most reasonable therapeutic strategy for acute myocardial infarction. Therefore, we tested the hypotheses that (1) inflammatory monocytes play a causative role in plaque destabilization and rupture and (2) the nanoparticle-mediated delivery of pitavastatin into circulating inflammatory monocytes inhibits plaque destabilization and rupture.

Methods and results: We used a model of plaque destabilization and rupture in the brachiocephalic arteries of apolipoprotein E-deficient (ApoE(-/-)) mice fed a high-fat diet and infused with angiotensin II. The adoptive transfer of CCR2(+/+)Ly-6C(high) inflammatory macrophages, but not CCR2(-/-) leukocytes, accelerated plaque destabilization associated with increased serum monocyte chemoattractant protein-1 (MCP-1), monocyte-colony stimulating factor, and matrix metalloproteinase-9. We prepared poly(lactic-co-glycolic) acid nanoparticles that were incorporated by Ly-6G(-)CD11b(+) monocytes and delivered into atherosclerotic plaques after intravenous administration. Intravenous treatment with pitavastatin-incorporated nanoparticles, but not with control nanoparticles or pitavastatin alone, inhibited plaque destabilization and rupture associated with decreased monocyte infiltration and gelatinase activity in the plaque. Pitavastatin-incorporated nanoparticles inhibited MCP-1-induced monocyte chemotaxis and the secretion of MCP-1 and matrix metalloproteinase-9 from cultured macrophages. Furthermore, the nanoparticle-mediated anti-MCP-1 gene therapy reduced the incidence of plaque destabilization and rupture.

Conclusions: The recruitment of inflammatory monocytes is critical in the pathogenesis of plaque destabilization and rupture, and nanoparticle-mediated pitavastatin delivery is a promising therapeutic strategy to inhibit plaque destabilization and rupture by regulating MCP-1/CCR2-dependent monocyte recruitment in this model.

Keywords: monocytes; myocardial infarction; nanoparticles; plaque; statins, HMG-CoA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Apolipoproteins E / genetics
  • Brachiocephalic Trunk / drug effects
  • Brachiocephalic Trunk / immunology
  • Brachiocephalic Trunk / pathology
  • Cell Movement / drug effects
  • Cell Movement / immunology
  • Chemokine CCL2 / antagonists & inhibitors
  • Chemokine CCL2 / metabolism
  • Disease Models, Animal
  • Drug Delivery Systems / methods*
  • Genetic Therapy / methods
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors / pharmacokinetics
  • Male
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / drug effects*
  • Monocytes / immunology
  • Monocytes / pathology
  • Nanoparticles / metabolism*
  • Nanoparticles / therapeutic use
  • Plaque, Atherosclerotic / drug therapy*
  • Plaque, Atherosclerotic / immunology
  • Plaque, Atherosclerotic / pathology
  • Quinolines / pharmacokinetics*
  • Receptors, CCR2 / genetics

Substances

  • Apolipoproteins E
  • Ccl2 protein, mouse
  • Ccr2 protein, mouse
  • Chemokine CCL2
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors
  • Quinolines
  • Receptors, CCR2
  • pitavastatin