Atheroprone flow enhances the endothelial-to-mesenchymal transition

Am J Physiol Heart Circ Physiol. 2018 Nov 1;315(5):H1293-H1303. doi: 10.1152/ajpheart.00213.2018. Epub 2018 Jul 27.

Abstract

The endothelial-to-mesenchymal transition (EndoMT) is a cellular process featuring decreased expression of endothelial marker genes but increased expression of mesenchymal marker genes. The EndoMT is involved in endothelial dysfunction and the pathogenesis of atherosclerosis. To investigate the dynamic expression of EndoMT genes in vascular endothelial cells under atheroprotective pulsatile shear stress (PS) and atheroprone oscillatory shear stress (OS), we analyzed RNA sequencing data from multitimepoint shear-stress experiments. This unbiased analysis involving next-generation sequencing confirmed that PS and OS had an opposite effect in regulating EndoMT genes. Further experimental validations with H2O2 and gain- and loss-of-function approaches indicated that reactive oxygen species are involved in OS-induced EndoMT, whereas AMP-activated protein kinase and sirtuin-1 could inhibit OS-induced EndoMT. Furthermore, compared with PS, OS increased the DNA methylation of the promoter regions of von Willebrand factor, CD31, and cadherin 5 genes but decreased that of cadherin 2, fibroblast-specific protein 1, and vimentin. The translational implication of the present study builds on the ability of the antidiabetic drug metformin and cholesterol-lowering drug atorvastatin to suppress the EndoMT in cultured endothelial cells and in mouse aortas. NEW & NOTEWORTHY Our RNA sequencing data provided a genome-wide and unbiased view of the shear stress regulation of the endothelial-to-mesenchymal transition (EndoMT) in the endothelium. Furthermore, epigenetic regulation (e.g., DNA methylation) is a key mechanism involved in shear stress-regulated EndoMT. The translational implication of this study is that cardiovascular medications such as statins and metformin have similar beneficial effects as that of atheroprotective flow by mitigating EndoMT.

Keywords: AMP-activated protein kinase; endothelial-to-mesenchymal transition; endothelium; shear stress; sirtuin 1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Atherosclerosis / physiopathology
  • Atorvastatin / pharmacology
  • Cadherins / genetics
  • Cadherins / metabolism
  • Cells, Cultured
  • DNA Methylation
  • Epigenesis, Genetic
  • Epithelial-Mesenchymal Transition* / drug effects
  • Epithelial-Mesenchymal Transition* / genetics
  • Gene Expression Regulation
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Human Umbilical Vein Endothelial Cells / pathology*
  • Humans
  • Metformin / pharmacology
  • Mice, Inbred C57BL
  • Platelet Endothelial Cell Adhesion Molecule-1 / genetics
  • Platelet Endothelial Cell Adhesion Molecule-1 / metabolism
  • Promoter Regions, Genetic
  • Pulsatile Flow*
  • Regional Blood Flow
  • S100 Calcium-Binding Protein A4 / genetics
  • S100 Calcium-Binding Protein A4 / metabolism
  • Sirtuin 1 / genetics
  • Sirtuin 1 / metabolism
  • Stress, Mechanical
  • Time Factors
  • Vimentin / genetics
  • Vimentin / metabolism
  • von Willebrand Factor / genetics
  • von Willebrand Factor / metabolism

Substances

  • Antigens, CD
  • CDH2 protein, human
  • Cadherins
  • Platelet Endothelial Cell Adhesion Molecule-1
  • S100 Calcium-Binding Protein A4
  • VIM protein, human
  • Vimentin
  • cadherin 5
  • von Willebrand Factor
  • S100A4 protein, human
  • Metformin
  • Atorvastatin
  • AMP-Activated Protein Kinases
  • SIRT1 protein, human
  • Sirtuin 1