Pinocembrin Protects Blood-Brain Barrier Function and Expands the Therapeutic Time Window for Tissue-Type Plasminogen Activator Treatment in a Rat Thromboembolic Stroke Model

Biomed Res Int. 2018 Apr 22:2018:8943210. doi: 10.1155/2018/8943210. eCollection 2018.

Abstract

Tissue-type plasminogen activator (t-PA) remains the only approved therapy for acute ischemic stroke but has a restrictive treatment time window of 4.5 hr. Prolonged ischemia causes blood-brain barrier (BBB) damage and increases the incidence of hemorrhagic transformation (HT) secondary to reperfusion. In this study, we sought to determine the effect of pinocembrin (PCB; a pleiotropic neuroprotective agent) on t-PA administration-induced BBB damage in a novel rat thromboembolic stroke model. By assessing the leakage of Evans blue into the ischemic hemisphere, we demonstrated that PCB pretreatment 5 min before t-PA administration significantly reduced BBB damage following 2 hr, 4 hr, 6 hr, and even 8 hr ischemia. Consistently, PCB pretreatment significantly decreased t-PA infusion-resulting brain edema and infarction volume and improved the behavioral outcomes following 6 hr ischemia. Mechanistically, PCB pretreatment inhibited the activation of MMP-2 and MMP-9 and degradation of tight junction proteins (TJPs) occludin and claudin-5 in the ischemic hemisphere. Moreover, PCB pretreatment significantly reduced phosphorylation of platelet-derived growth factor receptor α (PDGFRα) as compared with t-PA alone. In an in vitro BBB model, PCB decreased transendothelial permeability upon hypoxia/aglycemia through inhibiting PDGF-CC secretion. In conclusion, we demonstrated that PCB pretreatment shortly before t-PA infusion significantly protects BBB function and improves neurological outcomes following prolonged ischemia beyond the regular 4.5 hr t-PA time window. PCB pretreatment may represent a novel means of increasing the safety and the therapeutic time window of t-PA following ischemic stroke.

MeSH terms

  • Animals
  • Behavior, Animal
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / pathology*
  • Brain Ischemia / complications
  • Brain Ischemia / drug therapy
  • Brain Ischemia / enzymology
  • Brain Ischemia / pathology
  • Disease Models, Animal
  • Disease Progression
  • Embolism / complications
  • Embolism / drug therapy*
  • Embolism / enzymology
  • Embolism / pathology
  • Flavanones / cerebrospinal fluid
  • Flavanones / pharmacology
  • Flavanones / therapeutic use*
  • Humans
  • Lymphokines / metabolism
  • Male
  • Matrix Metalloproteinase 2 / metabolism
  • Matrix Metalloproteinase 9 / metabolism
  • Neuroprotective Agents / pharmacology
  • Neuroprotective Agents / therapeutic use*
  • Permeability
  • Platelet-Derived Growth Factor / metabolism
  • Rats, Sprague-Dawley
  • Receptor, Platelet-Derived Growth Factor alpha / metabolism
  • Signal Transduction / drug effects
  • Stroke / complications
  • Stroke / drug therapy*
  • Stroke / enzymology
  • Stroke / pathology
  • Thrombosis / complications
  • Thrombosis / drug therapy*
  • Thrombosis / enzymology
  • Thrombosis / pathology
  • Tight Junction Proteins / metabolism
  • Time Factors
  • Tissue Plasminogen Activator / administration & dosage
  • Tissue Plasminogen Activator / pharmacology
  • Tissue Plasminogen Activator / therapeutic use*

Substances

  • Flavanones
  • Lymphokines
  • Neuroprotective Agents
  • Platelet-Derived Growth Factor
  • Tight Junction Proteins
  • platelet-derived growth factor C
  • pinocembrin
  • Receptor, Platelet-Derived Growth Factor alpha
  • Tissue Plasminogen Activator
  • Matrix Metalloproteinase 2
  • Matrix Metalloproteinase 9