Differential role of an NF-κB transcriptional response element in endothelial versus intimal cell VCAM-1 expression

Circ Res. 2015 Jul 3;117(2):166-77. doi: 10.1161/CIRCRESAHA.117.306666. Epub 2015 Jun 1.

Abstract

Rationale: Human and murine Vcam1 promoters contain 2 adjacent nuclear factor-κB (NF-κB)-binding elements. Both are essential for cytokine-induced transcription of transiently transfected promoter-reporter constructs. However, the relevance of these insights to regulation of the endogenous Vcam1 gene and to pathophysiological processes in vivo remained unknown.

Objective: Determine the role of the 5' NF-κB-binding element in expression of the endogenous Vcam1 gene.

Methods and results: Homologous recombination in embryonic stem cells was used to inactivate the 5' NF-κB element in the Vcam1 promoter and alter 3 nucleotides in the 5' untranslated region to allow direct comparison of wild-type versus mutant allele RNA expression and chromatin configuration in heterozygous mice. Systemic treatment with inflammatory cytokines or endotoxin (lipopolysaccharide) induced lower expression of the mutant allele relative to wild-type by endothelial cells in the aorta, heart, and lungs. The mutant allele also showed lower endothelial expression in 2-week atherosclerotic lesions in Vcam1 heterozygous/low-density lipoprotein receptor-deficient mice fed a cholesterol-rich diet. In vivo chromatin immunoprecipitation assays of heart showed diminished lipopolysaccharide-induced association of RNA polymerase 2 and NF-κB p65 with the mutant promoter. In contrast, expression of mutant and wild-type alleles was comparable in intimal cells of wire-injured carotid artery and 4- to 12-week atherosclerotic lesions.

Conclusions: This study highlights differences between in vivo and in vitro promoter analyses, and reveals a differential role for a NF-κB transcriptional response element in endothelial vascular cell adhesion molecule-1 expression induced by inflammatory cytokines or a cholesterol-rich diet versus intimal cell expression in atherosclerotic lesions and injured arteries.

Keywords: NF-κB; atherosclerosis; chromatin immunoprecipitation; endothelial cells; gene expression; tunica intima; vascular cell adhesion molecule-1.

Publication types

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

MeSH terms

  • 5' Untranslated Regions / genetics*
  • Animals
  • Atherosclerosis / etiology
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology
  • Carotid Artery Injuries / metabolism
  • Carotid Artery Injuries / pathology
  • Cells, Cultured
  • Chemotaxis, Leukocyte / physiology
  • Cholesterol, Dietary / adverse effects
  • E-Selectin / metabolism
  • Endothelial Cells / metabolism
  • Endothelium, Vascular / metabolism*
  • Endothelium, Vascular / pathology
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Promoter Regions, Genetic
  • Protein Interaction Mapping
  • RNA Polymerase II / metabolism
  • Receptors, LDL / deficiency
  • Response Elements / genetics
  • Response Elements / radiation effects*
  • Transcription Factor RelA / metabolism*
  • Transcription, Genetic
  • Tunica Intima / metabolism*
  • Tunica Intima / pathology
  • Vascular Cell Adhesion Molecule-1 / biosynthesis
  • Vascular Cell Adhesion Molecule-1 / genetics*

Substances

  • 5' Untranslated Regions
  • Cholesterol, Dietary
  • E-Selectin
  • Receptors, LDL
  • Rela protein, mouse
  • Transcription Factor RelA
  • Vascular Cell Adhesion Molecule-1
  • RNA Polymerase II