Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium

Microvasc Res. 2015 Jul:100:48-53. doi: 10.1016/j.mvr.2015.04.010. Epub 2015 May 4.

Abstract

Zonula occludens-1 (ZO-1) is essential to the proper assembly of interendothelial junction complexes that control blood-brain barrier (BBB) integrity. The goal of the current paper was to improve our understanding of how proinflammatory cytokines modulate ZO-1 properties within the human BBB microvascular endothelium. In this respect, we investigated the effects of TNF-α and IL-6 on ZO-1 using human brain microvascular endothelial cells (HBMvECs). Following treatment of HBMvECs with either cytokine (0-100 ng/ml, 18 h), we observed significantly decreased ZO-1 expression and ZO-1:occludin co-association, in parallel with increased ZO-1 phosphorylation (pTyr and pThr). All effects were dose-dependent. Either cytokine also caused extensive cell-cell border delocalization of ZO-1 in parallel with elevated HBMvEC permeability. Furthermore, pre-treatment of HBMvECs with antioxidants (superoxide dismutase, catalase, apocynin, N-acetylcysteine), or employing targeted inhibition of NADPH oxidase activation (NSC23766, gp91/p47 siRNA), were all found to comparably attenuate the cytokine-dependent decrease in ZO-1 protein expression. In summary, we present an in vitro model of how different proinflammatory cytokines can dysregulate ZO-1 properties in HBMvECs. A causal role for NADPH oxidase activation and oxidant signalling is also confirmed. Our findings add mechanistic depth to current in vivo models of BBB injury manifesting ZO-1 dysregulation.

Keywords: Blood–brain barrier; Cytokine; Endothelial; NADPH oxidase; Zonula occludens-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antioxidants / pharmacology
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / pathology
  • Capillary Permeability / drug effects
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Down-Regulation
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Interleukin-6 / pharmacology*
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Microvessels / drug effects*
  • Microvessels / metabolism
  • Microvessels / pathology
  • NADPH Oxidase 2
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism
  • Phosphorylation
  • RNA Interference
  • Reactive Oxygen Species / metabolism
  • Transfection
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Zonula Occludens-1 Protein / genetics
  • Zonula Occludens-1 Protein / metabolism*

Substances

  • Antioxidants
  • Enzyme Inhibitors
  • Interleukin-6
  • Membrane Glycoproteins
  • Reactive Oxygen Species
  • TJP1 protein, human
  • Tumor Necrosis Factor-alpha
  • Zonula Occludens-1 Protein
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases
  • neutrophil cytosolic factor 1