Aldosterone administration to mice stimulates macrophage NADPH oxidase and increases atherosclerosis development: a possible role for angiotensin-converting enzyme and the receptors for angiotensin II and aldosterone

Circulation. 2004 May 11;109(18):2213-20. doi: 10.1161/01.CIR.0000127949.05756.9D. Epub 2004 May 3.

Abstract

Background: The renin-angiotensin-aldosterone system is involved in the pathogenesis of atherosclerosis, partially because of its pro-oxidative properties. We questioned the effect and mechanisms of action of administration of aldosterone to apolipoprotein E-deficient (E(0)) mice on their macrophages and aorta oxidative status and the ability of pharmacological agents to block this effect.

Methods and results: Aldosterone (0.2 to 6 microg. mouse(-1) x d(-1)) was administered to E(0) mice alone or in combination with eplerenone (200 mg x kg(-1) x d(-1)), ramipril (5 mg x kg(-1) x d(-1)), or losartan (25 mg x kg(-1) x d(-1)). Mouse aortic atherosclerotic lesion area and macrophage and aortic oxidative status were evaluated. Aldosterone administration enhanced the mouse atherosclerotic lesion area by 32%. Mouse peritoneal macrophages and aortic segments from aldosterone-treated mice exhibited increased superoxide anion formation by up to 155% and 69%, respectively, and this effect was probably mediated by NADPH oxidase activation, because increased translocation of its cytosolic component p47phox to the macrophage plasma membrane was observed. THP-1 macrophages incubated in vitro with aldosterone (10 micromol/L) exhibited a higher capacity to release superoxide ions by 110% and increased ability to oxidize LDL by 74% compared with control cells. Aldosterone administration enhanced mouse peritoneal macrophage ACE activity and mRNA expression by 2.3-fold and 2.4-fold, respectively. Only cotreatment of eplerenone with ramipril or losartan completely blocked the oxidative effects of aldosterone.

Conclusions: Aldosterone administration to E(0) mice increased macrophage oxidative stress and atherosclerotic lesion development. Blocking of the mineralocorticoid receptor and inhibition of tissue ACE and/or the angiotensin receptor-1 reduced aldosterone deleterious pro-oxidative and proatherogenic effects.

MeSH terms

  • Aldosterone / pharmacology*
  • Aldosterone / physiology
  • Aldosterone / toxicity
  • Angiotensin II / physiology*
  • Angiotensin II Type 1 Receptor Blockers
  • Angiotensin-Converting Enzyme Inhibitors / pharmacology
  • Angiotensin-Converting Enzyme Inhibitors / therapeutic use
  • Animals
  • Aortic Diseases / chemically induced
  • Aortic Diseases / metabolism
  • Aortic Diseases / pathology
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Arteriosclerosis / chemically induced*
  • Arteriosclerosis / metabolism
  • Arteriosclerosis / pathology
  • Arteriosclerosis / prevention & control
  • Cell Line / drug effects
  • Cell Line / metabolism
  • Enzyme Induction / drug effects
  • Eplerenone
  • Hormone Antagonists / pharmacology
  • Hormone Antagonists / therapeutic use
  • Humans
  • Lipid Peroxidation / drug effects
  • Lipoproteins, LDL / metabolism
  • Losartan / pharmacology
  • Losartan / therapeutic use
  • Macrophages, Peritoneal / drug effects*
  • Macrophages, Peritoneal / enzymology
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Mineralocorticoid Receptor Antagonists
  • NADPH Oxidases / metabolism*
  • Oxidative Stress / drug effects
  • Peptidyl-Dipeptidase A / biosynthesis
  • Peptidyl-Dipeptidase A / genetics
  • Peptidyl-Dipeptidase A / physiology*
  • Phosphoproteins / metabolism
  • Protein Transport / drug effects
  • RNA, Messenger / biosynthesis
  • Ramipril / pharmacology
  • Ramipril / therapeutic use
  • Receptor, Angiotensin, Type 1 / physiology*
  • Receptors, Mineralocorticoid / physiology*
  • Spironolactone / analogs & derivatives*
  • Spironolactone / pharmacology
  • Spironolactone / therapeutic use
  • Superoxides / metabolism

Substances

  • Angiotensin II Type 1 Receptor Blockers
  • Angiotensin-Converting Enzyme Inhibitors
  • Apolipoproteins E
  • Hormone Antagonists
  • Lipoproteins, LDL
  • Membrane Proteins
  • Mineralocorticoid Receptor Antagonists
  • Phosphoproteins
  • RNA, Messenger
  • Receptor, Angiotensin, Type 1
  • Receptors, Mineralocorticoid
  • oxidized low density lipoprotein
  • Superoxides
  • Angiotensin II
  • Spironolactone
  • Aldosterone
  • Eplerenone
  • NADPH Oxidases
  • neutrophil cytosolic factor 1
  • Peptidyl-Dipeptidase A
  • Losartan
  • Ramipril