Estrogen Receptor Control of Atherosclerotic Calcification and Smooth Muscle Cell Osteogenic Differentiation

Arterioscler Thromb Vasc Biol. 2017 Jun;37(6):1127-1137. doi: 10.1161/ATVBAHA.117.309054. Epub 2017 May 4.

Abstract

Objective: Vascular calcification is associated with increased risk of myocardial infarction and stroke. The objective of this work was to examine the ability of 17β-estradiol (E2) to stimulate calcification of vascular smooth muscle cells (VSMC) in vivo, using aged apolipoprotein E-null mice with advanced atherosclerotic lesions, and subsequently to explore underlying mechanisms in vitro.

Approach and results: Silastic E2 capsules were implanted into male and female apolipoprotein E-null mice aged 34 weeks. Plaque and calcified area were measured in the aortic sinus and innominate artery after 8 weeks. Immunohistochemical analysis examined expression of the estrogen receptors (estrogen receptor alpha and estrogen receptor beta [ERβ]). VSMC expression of osteogenic markers was examined using digital polymerase chain reaction. Advanced atherosclerotic lesions were present in all mice at the end of 8 weeks. In both male and female mice, E2 increased calcified area in a site-specific manner in the aortic sinus independently of plaque growth or lipid levels and occurred in association with a site-specific decrease in the proportion of ERβ-positive intimal cells. Calcified lesions expressed collagen I and bone sialoprotein, with decreased matrix Gla protein. In vitro, E2 suppressed ERβ expression and increased VSMC mineralization, demonstrating increased collagen I and II, osteocalcin and bone sialoprotein, and reduced matrix Gla protein and osteopontin. Antagonism or RNA silencing of estrogen receptor alpha, ERβ, or both further increased VSMC mineralization.

Conclusions: We have demonstrated that E2 can drive calcification in advanced atherosclerotic lesions by promoting the differentiation of VSMC to osteoblast-like cells, a process which is augmented by inhibition of estrogen receptor alpha or ERβ activity.

Keywords: atherosclerosis; cell differentiation; estradiol; receptors, estrogen; vascular calcification.

MeSH terms

  • Animals
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Atherosclerosis / chemically induced*
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Calcium-Binding Proteins / metabolism
  • Cattle
  • Cell Differentiation / drug effects*
  • Cells, Cultured
  • Collagen / metabolism
  • Disease Models, Animal
  • Drug Implants
  • Estradiol / administration & dosage
  • Estradiol / toxicity*
  • Estrogen Receptor Antagonists / pharmacology
  • Estrogen Receptor alpha / agonists*
  • Estrogen Receptor alpha / genetics
  • Estrogen Receptor alpha / metabolism
  • Estrogen Receptor beta / agonists*
  • Estrogen Receptor beta / genetics
  • Estrogen Receptor beta / metabolism
  • Extracellular Matrix Proteins / metabolism
  • Female
  • Genetic Predisposition to Disease
  • Humans
  • Integrin-Binding Sialoprotein / metabolism
  • Male
  • Matrix Gla Protein
  • Mice, Knockout
  • Muscle, Smooth, Vascular / drug effects*
  • Muscle, Smooth, Vascular / metabolism
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / drug effects*
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / pathology
  • Neointima
  • Osteocalcin / metabolism
  • Osteogenesis / drug effects*
  • Osteopontin / metabolism
  • Phenotype
  • Plaque, Atherosclerotic
  • RNA Interference
  • Signal Transduction / drug effects
  • Transfection
  • Vascular Calcification / chemically induced*
  • Vascular Calcification / genetics
  • Vascular Calcification / metabolism
  • Vascular Calcification / pathology

Substances

  • Apolipoproteins E
  • Calcium-Binding Proteins
  • Drug Implants
  • ESR1 protein, human
  • ESR2 protein, human
  • Estrogen Receptor Antagonists
  • Estrogen Receptor alpha
  • Estrogen Receptor beta
  • Extracellular Matrix Proteins
  • Integrin-Binding Sialoprotein
  • Spp1 protein, mouse
  • Osteocalcin
  • Osteopontin
  • Estradiol
  • Collagen