Endothelial barrier stabilization by a cyclic tandem peptide targeting VE-cadherin transinteraction in vitro and in vivo

J Cell Sci. 2009 May 15;122(Pt 10):1616-25. doi: 10.1242/jcs.040212.

Abstract

Inflammatory stimuli result in vascular leakage with potentially life threatening consequences. As a key barrier component, loss of vascular endothelial (VE-) cadherin-mediated adhesion often precedes endothelial breakdown. This study aimed to stabilize VE-cadherin transinteraction and endothelial barrier function using peptides targeting the VE-cadherin adhesive interface. After modelling the transinteracting VE-cadherin structure, an inhibiting single peptide (SP) against a VE-cadherin binding pocket was selected, which specifically blocked VE-cadherin transinteraction as analyzed by single molecule atomic force microscopy (AFM). The tandem peptide (TP) consisting of two SP sequences in tandem was designed to strengthen VE-cadherin adhesion by simultaneously binding and cross-bridging two interacting cadherin molecules. Indeed, in AFM experiments TP specifically rendered VE-cadherin transinteraction resistant against an inhibitory monoclonal antibody. Moreover, TP reduced VE-cadherin lateral mobility and enhanced binding of VE-cadherin-coated microbeads to cultured endothelial cells, but acted independently of the actin cytoskeleton. TP also stabilized endothelial barrier properties against the Ca(2+) ionophore A23187 and the inhibitory antibody. Finally, TP abolished endothelial permeability increase induced by tumour necrosis factor-alpha in microperfused venules in vivo. Stabilization of VE-cadherin adhesion by cross-bridging peptides may therefore be a novel therapeutic approach for the treatment of vascular hyperpermeability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adherens Junctions / drug effects
  • Adherens Junctions / metabolism
  • Animals
  • Antigens, CD / chemistry
  • Antigens, CD / drug effects*
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Binding Sites
  • CHO Cells
  • Cadherins / chemistry
  • Cadherins / drug effects*
  • Cadherins / genetics
  • Cadherins / metabolism
  • Calcimycin / pharmacology
  • Calcium / metabolism
  • Capillary Permeability / drug effects*
  • Cell Adhesion / drug effects*
  • Computer Simulation
  • Computer-Aided Design
  • Cricetinae
  • Cricetulus
  • Diffusion
  • Electric Impedance
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Fluorescence Recovery After Photobleaching
  • Humans
  • Ionophores / pharmacology
  • Luminescent Proteins / genetics
  • Mice
  • Microscopy, Atomic Force
  • Models, Molecular
  • Peptides, Cyclic / chemistry
  • Peptides, Cyclic / metabolism
  • Peptides, Cyclic / pharmacology*
  • Protein Conformation
  • Protein Structure, Tertiary
  • Protein Transport
  • Rats
  • Rats, Wistar
  • Recombinant Fusion Proteins / metabolism
  • Time Factors
  • Transfection
  • Tumor Necrosis Factor-alpha / metabolism
  • Venules / drug effects
  • Venules / metabolism

Substances

  • Antigens, CD
  • Cadherins
  • Ionophores
  • Luminescent Proteins
  • Peptides, Cyclic
  • Recombinant Fusion Proteins
  • Tumor Necrosis Factor-alpha
  • cadherin 5
  • Calcimycin
  • Calcium