t-PA-specific modulation of a human blood-brain barrier model involves plasmin-mediated activation of the Rho kinase pathway in astrocytes

Blood. 2012 May 17;119(20):4752-61. doi: 10.1182/blood-2011-07-369512. Epub 2012 Jan 19.

Abstract

Tissue-type plasminogen activator (t-PA) can modulate permeability of the neurovascular unit and exacerbate injury in ischemic stroke. We examined the effects of t-PA using in vitro models of the blood-brain barrier. t-PA caused a concentration-dependent increase in permeability. This effect was dependent on plasmin formation and potentiated in the presence of plasminogen. An inactive t-PA variant inhibited the t-PA-mediated increase in permeability, whereas blockade of low-density lipoprotein receptors or exposed lysine residues resulted in similar inhibition, implying a role for both a t-PA receptor, most likely a low-density lipoprotein receptor, and a plasminogen receptor. This effect was selective to t-PA and its close derivative tenecteplase. The truncated t-PA variant reteplase had a minor effect on permeability, whereas urokinase and desmoteplase were ineffective. t-PA also induced marked shape changes in both brain endothelial cells and astrocytes. Changes in astrocyte morphology coincided with increased F-actin staining intensity, larger focal adhesion size, and elevated levels of phosphorylated myosin. Inhibition of Rho kinase blocked these changes and reduced t-PA/plasminogen-mediated increase in permeability. Hence plasmin, generated on the cell surface selectively by t-PA, modulates the astrocytic cytoskeleton, leading to an increase in blood-brain barrier permeability. Blockade of the Rho/Rho kinase pathway may have beneficial consequences during thrombolytic therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects*
  • Astrocytes / metabolism
  • Astrocytes / physiology
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / metabolism*
  • Blood-Brain Barrier / pathology
  • Blood-Brain Barrier / physiology
  • Cell Membrane Permeability / drug effects
  • Cells, Cultured
  • Coculture Techniques
  • Dose-Response Relationship, Drug
  • Drug Evaluation, Preclinical
  • Enzyme Activation / drug effects
  • Fibrinolysin / metabolism
  • Fibrinolysin / pharmacology*
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Models, Theoretical
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Tissue Plasminogen Activator / pharmacology*
  • rho-Associated Kinases / metabolism*

Substances

  • rho-Associated Kinases
  • Tissue Plasminogen Activator
  • Fibrinolysin