Cerebral endothelial cell-derived small extracellular vesicles enhance neurovascular function and neurological recovery in rat acute ischemic stroke models of mechanical thrombectomy and embolic stroke treatment with tPA

J Cereb Blood Flow Metab. 2021 Aug;41(8):2090-2104. doi: 10.1177/0271678X21992980. Epub 2021 Feb 8.

Abstract

Treatment of patients with cerebral large vessel occlusion with thrombectomy and tissue plasminogen activator (tPA) leads to incomplete reperfusion. Using rat models of embolic and transient middle cerebral artery occlusion (eMCAO and tMCAO), we investigated the effect on stroke outcomes of small extracellular vesicles (sEVs) derived from rat cerebral endothelial cells (CEC-sEVs) in combination with tPA (CEC-sEVs/tPA) as a treatment of eMCAO and tMCAO in rat. The effect of sEVs derived from clots acquired from patients who had undergone mechanical thrombectomy on healthy human CEC permeability was also evaluated. CEC-sEVs/tPA administered 4 h after eMCAO reduced infarct volume by ∼36%, increased recanalization of the occluded MCA, enhanced cerebral blood flow (CBF), and reduced blood-brain barrier (BBB) leakage. Treatment with CEC-sEVs given upon reperfusion after 2 h tMCAO significantly reduced infarct volume by ∼43%, and neurological outcomes were improved in both CEC-sEVs treated models. CEC-sEVs/tPA reduced a network of microRNAs (miRs) and proteins that mediate thrombosis, coagulation, and inflammation. Patient-clot derived sEVs increased CEC permeability, which was reduced by CEC-sEVs. CEC-sEV mediated suppression of a network of pro-thrombotic, -coagulant, and -inflammatory miRs and proteins likely contribute to therapeutic effects. Thus, CEC-sEVs have a therapeutic effect on acute ischemic stroke by reducing neurovascular damage.

Keywords: Acute ischemic stroke; blood-brain barrier; endothelial cells; small extracellular vesicles; tPA.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / metabolism
  • Brain / blood supply
  • Brain / metabolism
  • Brain / pathology
  • Cerebrovascular Circulation / drug effects
  • Cerebrovascular Circulation / physiology
  • Disease Models, Animal
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Extracellular Vesicles / metabolism
  • Extracellular Vesicles / transplantation*
  • Fibrinolytic Agents / pharmacology
  • Fibrinolytic Agents / therapeutic use*
  • Humans
  • Ischemic Stroke / drug therapy
  • Ischemic Stroke / pathology
  • Ischemic Stroke / therapy*
  • Male
  • MicroRNAs / metabolism
  • Rats
  • Rats, Wistar
  • Thrombectomy / adverse effects
  • Tissue Plasminogen Activator / pharmacology
  • Tissue Plasminogen Activator / therapeutic use*

Substances

  • Fibrinolytic Agents
  • MicroRNAs
  • Tissue Plasminogen Activator