Angiotensin-converting enzyme inhibition down-regulates the pro-atherogenic chemokine receptor 9 (CCR9)-chemokine ligand 25 (CCL25) axis

J Biol Chem. 2010 Jul 23;285(30):23496-505. doi: 10.1074/jbc.M110.117481. Epub 2010 May 26.

Abstract

Many experimental and clinical studies suggest a relationship between enhanced angiotensin II release by the angiotensin-converting enzyme (ACE) and the pathophysiology of atherosclerosis. The atherosclerosis-enhancing effects of angiotensin II are complex and incompletely understood. To identify anti-atherogenic target genes, we performed microarray gene expression profiling of the aorta during atherosclerosis prevention with the ACE inhibitor, captopril. Atherosclerosis-prone apolipoprotein E (apoE)-deficient mice were used as a model to decipher susceptible genes regulated during atherosclerosis prevention with captopril. Microarray gene expression profiling and immunohistology revealed that captopril treatment for 7 months strongly decreased the recruitment of pro-atherogenic immune cells into the aorta. Captopril-mediated inhibition of plaque-infiltrating immune cells involved down-regulation of the C-C chemokine receptor 9 (CCR9). Reduced cell migration correlated with decreased numbers of aorta-resident cells expressing the CCR9-specific chemoattractant factor, chemokine ligand 25 (CCL25). The CCL25-CCR9 axis was pro-atherogenic, because inhibition of CCR9 by RNA interference in hematopoietic progenitors of apoE-deficient mice significantly retarded the development of atherosclerosis. Analysis of coronary artery biopsy specimens of patients with coronary artery atherosclerosis undergoing bypass surgery also showed strong infiltrates of CCR9-positive cells in atherosclerotic lesions. Thus, the C-C chemokine receptor, CCR9, exerts a significant role in atherosclerosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin-Converting Enzyme Inhibitors / pharmacology*
  • Animals
  • Aorta / drug effects
  • Aorta / immunology
  • Aorta / metabolism
  • Apolipoproteins E / deficiency
  • Atherosclerosis / genetics*
  • Atherosclerosis / immunology
  • Atherosclerosis / metabolism
  • Atherosclerosis / prevention & control
  • Captopril / pharmacology
  • Chemokines, CC / genetics*
  • Chemokines, CC / metabolism
  • Cholesterol / metabolism
  • Coronary Artery Disease / complications
  • Down-Regulation / drug effects*
  • Female
  • Hematopoietic Stem Cells / drug effects
  • Hematopoietic Stem Cells / metabolism
  • Humans
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Male
  • Mice
  • Middle Aged
  • Monocytes / drug effects
  • Monocytes / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Peptidyl-Dipeptidase A / metabolism*
  • Protein Transport / drug effects
  • Receptor, Angiotensin, Type 1 / metabolism
  • Receptors, CCR / genetics*
  • Receptors, CCR / metabolism
  • Substrate Specificity
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology

Substances

  • Angiotensin-Converting Enzyme Inhibitors
  • Apolipoproteins E
  • CC chemokine receptor 9
  • CCL25 protein, human
  • Chemokines, CC
  • Receptor, Angiotensin, Type 1
  • Receptors, CCR
  • Cholesterol
  • Captopril
  • Peptidyl-Dipeptidase A