Histone and DNA methylation-mediated epigenetic downregulation of endothelial Kruppel-like factor 2 by low-density lipoprotein cholesterol

Arterioscler Thromb Vasc Biol. 2013 Aug;33(8):1936-42. doi: 10.1161/ATVBAHA.113.301765. Epub 2013 May 30.

Abstract

Objective: Low-density lipoprotein (LDL) cholesterol induces endothelial dysfunction and is a major modifiable risk factor for coronary heart disease. Endothelial Kruppel-like Factor 2 (KLF2) is a transcription factor that is vital to endothelium-dependent vascular homeostasis. The purpose of this study is to determine whether and how LDL affects endothelial KLF2 expression.

Approach and results: LDL downregulates KLF2 expression and promoter activity in endothelial cells. LDL-induced decrease in KLF2 parallels changes in endothelial KLF2 target genes thrombomodulin, endothelial NO synthase, and plasminogen activator inhibitor-1. Pharmacological inhibition of DNA methyltransferases or knockdown of DNA methyltransferase 1 prevents downregulation of endothelial KLF2 by LDL. LDL induces endothelial DNA methyltransferase 1 expression and DNA methyltransferase activity. LDL stimulates binding of the DNA methyl-CpG-binding protein-2 and histone methyltransferase enhancer of zeste homolog 2, whereas decreases binding of the KLF2 transcriptional activator myocyte enhancing factor-2, to the KLF2 promoter in endothelial cells. Knockdown of myocyte enhancing factor-2, or mutation of the myocyte enhancing factor-2 site in the KLF2 promoter, abrogates LDL-induced downregulation of endothelial KLF2 and thrombomodulin, and KLF2 promoter activity. Similarly, knockdown of enhancer of zeste homolog 2 negates LDL-induced downregulation of KLF2 and thrombomodulin in endothelial cells. Finally, overexpression of KLF2 rescues LDL-induced clotting of platelet-rich plasma on endothelial cells.

Conclusions: LDL represses endothelial KLF2 expression via DNA and histone methylation. Downregulation of KLF2 by LDL leads to a dysfunctional, hypercoagulable endothelium.

Keywords: DNA methyltransferase; KLF2; cholesterol, LDL; endothelial cells; histone methyltransferase.

MeSH terms

  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Cholesterol, LDL / metabolism*
  • DNA Methylation / physiology*
  • Down-Regulation / physiology
  • Endothelial Cells / cytology
  • Endothelial Cells / physiology*
  • Enhancer of Zeste Homolog 2 Protein
  • Epigenesis, Genetic / physiology*
  • Histones / metabolism
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism*
  • MADS Domain Proteins / genetics
  • MADS Domain Proteins / metabolism
  • MEF2 Transcription Factors
  • Methyl-CpG-Binding Protein 2 / genetics
  • Methyl-CpG-Binding Protein 2 / metabolism
  • Myogenic Regulatory Factors / genetics
  • Myogenic Regulatory Factors / metabolism
  • Phenotype
  • Polycomb Repressive Complex 2 / genetics
  • Polycomb Repressive Complex 2 / metabolism
  • Promoter Regions, Genetic / physiology
  • Thrombosis / genetics
  • Thrombosis / metabolism
  • Transcription, Genetic / physiology
  • Vasculitis / genetics
  • Vasculitis / metabolism

Substances

  • Cholesterol, LDL
  • Histones
  • KLF2 protein, human
  • Kruppel-Like Transcription Factors
  • MADS Domain Proteins
  • MECP2 protein, human
  • MEF2 Transcription Factors
  • MEF2A protein, human
  • Methyl-CpG-Binding Protein 2
  • Myogenic Regulatory Factors
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2