Heme oxygenase 1 determines atherosclerotic lesion progression into a vulnerable plaque

Circulation. 2009 Jun 16;119(23):3017-27. doi: 10.1161/CIRCULATIONAHA.108.808618. Epub 2009 Jun 1.

Abstract

Background: The molecular regulation for the transition from stable to vulnerable plaque remains to be elucidated. Heme oxygenase 1 (HO-1) and its metabolites have been implicated in the cytoprotective defense against oxidative injury in atherogenesis. In this study, we sought to assess the role of HO-1 in the progression toward plaque instability in carotid artery disease in patients and in a murine model of vulnerable plaque development.

Methods and results: Atherectomy biopsy from 112 patients with clinical carotid artery disease was collected and stratified according to characteristics of plaque vulnerability. HO-1 expression correlated closely with features of vulnerable human atheromatous plaque (P<0.005), including macrophage and lipid accumulation, and was inversely correlated with intraplaque vascular smooth muscle cells and collagen deposition. HO-1 expression levels correlated with the plaque destabilizing factors matrix metalloproteinase-9, interleukin-8, and interleukin-6. Likewise, in a vulnerable plaque model using apolipoprotein E(-/-) mice, HO-1 expression was upregulated in vulnerable versus stable lesions. HO-1 induction by cobalt protoporphyrin impeded lesion progression into vulnerable plaques, indicated by a reduction in necrotic core size and intraplaque lipid accumulation, whereas cap thickness and vascular smooth muscle cells were increased. In contrast, inhibition of HO-1 by zinc protoporphyrin augmented plaque vulnerability. Plaque stabilizing was prominent after adenoviral transduction of HO-1 compared with sham virus-treated animals, providing proof that the observed effects on plaque vulnerability were HO-1 specific.

Conclusions: Here we demonstrate in a well-defined patient group and a murine vulnerable plaque model that HO-1 induction reverses plaque progression from a vulnerable plaque to a more stable phenotype as part of a compensatory atheroprotective response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Apolipoproteins E / genetics
  • Carotid Artery Diseases / metabolism*
  • Carotid Artery Diseases / pathology*
  • Collagen / metabolism
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Heme Oxygenase-1 / genetics*
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Hyperlipidemias / metabolism
  • Hyperlipidemias / pathology
  • Interleukin-6 / metabolism
  • Interleukin-8 / metabolism
  • Macrophages / pathology
  • Male
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Mutant Strains
  • Middle Aged
  • Muscle, Smooth, Vascular / metabolism
  • Muscle, Smooth, Vascular / pathology
  • Thrombosis / metabolism
  • Thrombosis / pathology
  • Transfection

Substances

  • Apolipoproteins E
  • IL6 protein, human
  • Interleukin-6
  • Interleukin-8
  • Collagen
  • Heme Oxygenase-1
  • Matrix Metalloproteinase 9