17β-Estradiol Enhances Vascular Endothelial Ets-1/miR-126-3p Expression: The Possible Mechanism for Attenuation of Atherosclerosis

J Clin Endocrinol Metab. 2017 Feb 1;102(2):594-603. doi: 10.1210/jc.2016-2974.

Abstract

Context: Endothelial microRNA 126 (miR-126) attenuates the development of atherosclerosis (AS). However, there is no evidence showing the role of miR-126 in estrogen's antiatherogenic effects.

Objective: We hypothesized that 17β-estradiol (E2) modulates miR-126 expression and thus may improve endothelial function and retard AS development.

Design/setting/participants: This was a prospective cohort study of 12 healthy regularly menstruating female volunteers. ApoE-/- mice were used as the atherosclerosis model and human umbilical vascular endothelial cells (HUVECs) were cultured as the cell model.

Main outcome measures: Serum hormones and miR-126-3p levels were measured up to 3 times for 1 cycle. Real-time polymerase chain reaction, histology for atherosclerotic lesions, immunofluorescence, luciferase assay, transfection experiments, cell proliferation, migration and tube formation assay, and western blot were performed.

Results: Serum concentrations of miR-126-3p in cycling women were higher at the ovulatory and luteal phases than in the follicular phase, and they were positively correlated with E2 values. Administration of miR-126-3p mimics to ApoE-/- mice-attenuated atherogenesis, and antagomir-126-3p partially reversed the protective effect of E2 on atherogenesis. In HUVECs, E2 increased miR-126-3p expression via upregulation of Ets-1 (a transcription factor for miR-126). c-Src/Akt signaling was important for E2-mediated expression of Ets-1/miR-126. E2 decreased expression of miR-126-3p target Spred1 (a protein that inhibits mitogenic signaling). Overexpression of Spred1 partially blocked enhancement of endothelial cell proliferation, migration, and tube formation by E2. Additionally, E2 regulates miR-126-3p-mediated expression of vascular cell adhesion molecule-1 to inhibit monocyte adhesion into HUVECs.

Conclusions: E2 protection against atherogenesis is possibly mediated by Ets-1/miR-126.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Antagomirs / metabolism
  • Apolipoproteins E
  • Atherosclerosis / metabolism*
  • Cell Culture Techniques
  • Disease Models, Animal
  • Estradiol / physiology*
  • Female
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Menstrual Cycle / blood*
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / blood
  • MicroRNAs / metabolism*
  • Ovariectomy
  • Proto-Oncogene Protein c-ets-1 / metabolism*
  • Up-Regulation
  • Young Adult

Substances

  • Antagomirs
  • Apolipoproteins E
  • MIRN126 microRNA, human
  • MicroRNAs
  • Proto-Oncogene Protein c-ets-1
  • Estradiol