Recombinant ADAMTS13 reduces tissue plasminogen activator-induced hemorrhage after stroke in mice

Ann Neurol. 2013 Feb;73(2):189-98. doi: 10.1002/ana.23762. Epub 2012 Dec 31.

Abstract

Objective: Tissue plasminogen activator (tPA) is approved for treatment of acute ischemic stroke, but it increases the risk of cerebral hemorrhage. Accumulating evidence suggests that von Willebrand factor (VWF) plays a pivotal role in thrombus formation and microcirculatory disturbances after ischemic stroke. By cleaving VWF, ADAMTS13 (a disintegrin and metalloproteinase with a thrombospondin type 1 motif, member 13) protects mice from stroke. Therefore, we hypothesized that recombinant ADAMTS13 (rADAMTS13) could increase the safety of tPA thrombolysis in stroke.

Methods: We examined blood-brain barrier (BBB) permeability after intraventricular injection of tPA, VWF, and rADAMTS13 in nonischemic mice. We investigated the role of rADAMTS13 on reducing tPA-induced BBB dysfunction and cerebral hemorrhage in a mouse stroke model.

Results: Intraventricular injection of tPA or VWF under nonischemic conditions resulted in a significant increase in BBB permeability. In contrast, rADAMTS13 blocked both tPA- and VWF-induced BBB opening. BBB disruption following stroke was exacerbated by intravenous administration of tPA, but this was attenuated by injection of rADAMTS13. Correspondingly, tPA-associated hemorrhage after stroke was significantly reduced by rADAMTS13. The antihemorrhagic effect of rADAMTS13 was reversed by injection of recombinant VWF. We also showed that rADAMTS13 inhibited tPA-mediated upregulation of vascular endothelial growth factor (VEGF) in vascular endothelium after stroke. The upregulation of VEGF was suppressed by either an Akt inhibitor wortmannin or a Rho kinase inhibitor fasudil. Furthermore, rADAMTS13 downregulated tPA-induced phosphorylation of Akt and activation of RhoA.

Interpretation: These findings demonstrate that the VWF-cleaving protease rADAMTS13 reduced tPA-induced hemorrhage by regulating BBB integrity, and suggest that this effect may occur through the Akt/RhoA-mediated VEGF pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM Proteins / pharmacology*
  • ADAMTS13 Protein
  • Animals
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / metabolism
  • Brain Ischemia / drug therapy
  • Brain Ischemia / metabolism
  • Cerebral Hemorrhage / chemically induced
  • Cerebral Hemorrhage / metabolism
  • Cerebral Hemorrhage / prevention & control*
  • Disease Models, Animal
  • Drug Interactions
  • Drug Therapy, Combination / methods
  • Fibrinolytic Agents / pharmacology*
  • Humans
  • Injections, Intraventricular
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins c-akt / metabolism
  • Recombinant Proteins / pharmacology*
  • Stroke / drug therapy*
  • Stroke / metabolism
  • Tissue Plasminogen Activator / pharmacology*
  • Vascular Endothelial Growth Factor A / metabolism
  • rho GTP-Binding Proteins / metabolism
  • rhoA GTP-Binding Protein

Substances

  • Fibrinolytic Agents
  • Recombinant Proteins
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • Akt1 protein, mouse
  • Proto-Oncogene Proteins c-akt
  • Tissue Plasminogen Activator
  • ADAM Proteins
  • ADAMTS13 Protein
  • ADAMTS13 protein, human
  • RhoA protein, mouse
  • rho GTP-Binding Proteins
  • rhoA GTP-Binding Protein