Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure

Hepatology. 2009 Dec;50(6):1914-23. doi: 10.1002/hep.23203.

Abstract

Brain edema in acute liver failure (ALF) remains lethal. The role of vasogenic mechanisms of brain edema has not been explored. We previously demonstrated that matrix metalloproteinase-9 (MMP-9) contributes to the pathogenesis of brain edema. Here, we show that MMP-9 mediates disruptions in tight junction (TJ) proteins in vitro and in brains of mice with ALF. We transfected murine brain endothelial cells (ECs) with MMP-9 complementary DNA (cDNA) using pc DNA3.1 (+)/Myc-His A expression vector. Tissue inhibitor of matrix metalloproteinases (TIMP-1) cDNA transfection or GM6001 was used to inhibit MMP-9. ALF was induced in mice with azoxymethane. Endogenous overexpression of MMP-9 in brain ECs resulted in significant degradation of the TJ proteins occludin and claudin-5. The alterations in TJ proteins correlated with increased permeability to fluorescein isothiocyanate-dextran molecules. The degradation of TJ proteins and the increased permeability were reversed by TIMP-1 and GM6001. Similar results were found when MMP-9 was exogenously added to brain ECs. We also found that TJ protein degradation was reversed with GM6001 in the brains of mice with ALF.

Conclusion: TJ proteins are significantly perturbed in brains of mice with ALF. These data corroborate the important role of MMP-9 in the vasogenic mechanism of brain edema in ALF.

Publication types

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

MeSH terms

  • Animals
  • Blood-Brain Barrier*
  • Brain / metabolism*
  • Claudin-5
  • Dipeptides / pharmacology
  • Endothelial Cells / physiology*
  • Liver Failure, Acute / metabolism*
  • Matrix Metalloproteinase 9 / physiology*
  • Membrane Proteins / metabolism*
  • Mice
  • Occludin
  • Phosphoproteins / metabolism
  • Tight Junctions / physiology
  • Tissue Inhibitor of Metalloproteinase-1 / physiology
  • Zonula Occludens-1 Protein
  • Zonula Occludens-2 Protein

Substances

  • Claudin-5
  • Cldn5 protein, mouse
  • Dipeptides
  • Membrane Proteins
  • N-(2(R)-2-(hydroxamidocarbonylmethyl)-4-methylpentanoyl)-L-tryptophan methylamide
  • Occludin
  • Ocln protein, mouse
  • Phosphoproteins
  • Tissue Inhibitor of Metalloproteinase-1
  • Tjp1 protein, mouse
  • Tjp2 protein, mouse
  • Zonula Occludens-1 Protein
  • Zonula Occludens-2 Protein
  • Matrix Metalloproteinase 9