Inhibition of protein kinase C is not sufficient to prevent or reverse effects of VEGF165 on claudin-1 and permeability in microvascular retinal endothelial cells

Invest Ophthalmol Vis Sci. 2010 Jan;51(1):535-42. doi: 10.1167/iovs.09-3917. Epub 2009 Jul 30.

Abstract

Purpose: Pathogenesis of diabetic macular edema is driven by deregulated expression of VEGF. A study of long-term exposure of immortalized bovine retinal endothelial cells (iBRECs) to VEGF(165) clearly confirmed the role of the tight junction protein claudin-1, which almost completely disappeared within 24 hours, an effect that was completely reversed by addition of the VEGF-binding Fab fragment ranibizumab. This study was conducted to investigate whether the VEGF(165)-induced loss of claudin-1 is regulated by protein kinase C (PKC) and indeed affects the barrier function of iBRECs.

Methods: The effects of various PKC inhibitors on claudin-1 expression and cellular localization in iBRECs treated with VEGF(165) for up to 2 days were studied by Western blot analyses and immunofluorescence microscopy. The permeability of the cell layers was determined by transendothelial electrical resistance measurements.

Results: Activation of PKC led to decreased expression of claudin-1, which was blocked by inhibitors of PKCdelta. However, none of the PKC inhibitors significantly affected VEGF(165)-induced effects on cellular localization or expression of claudin-1. Also VEGF(165)-induced higher permeability of iBREC layers could be reversed or prevented by ranibizumab but not by PKC inhibitors. In addition, low claudin-1 expression and its delocalization from the plasma membrane were significantly associated with elevated permeability.

Conclusions: In iBRECs, PKC isoforms are not crucially involved in the VEGF(165)-initiated signal transduction that affects permeability and expression of claudin-1. This finding is in contrast to published results concerning only short-term effects of VEGF(165). The results also confirmed that claudin-1 is a highly relevant component of functional tight junctions in retinal endothelial cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Capillary Permeability
  • Cattle
  • Cell Count
  • Cells, Cultured
  • Claudin-1
  • Electric Impedance
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / metabolism
  • Membrane Proteins / metabolism*
  • Microscopy, Fluorescence
  • Protein Kinase C / antagonists & inhibitors*
  • Protein Kinase C / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Retinal Vessels / cytology
  • Retinal Vessels / metabolism
  • Tetradecanoylphorbol Acetate / pharmacology
  • Vascular Endothelial Growth Factor A / pharmacology*

Substances

  • CLDN1 protein, human
  • Claudin-1
  • Membrane Proteins
  • Protein Kinase Inhibitors
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Protein Kinase C
  • Tetradecanoylphorbol Acetate