Protease activated receptor-1 mediates cytotoxicity during ischemia using in vivo and in vitro models

Neuroscience. 2014 Dec 5:281:229-40. doi: 10.1016/j.neuroscience.2014.09.038. Epub 2014 Sep 28.

Abstract

Protease activated receptors (PARs) populate neurons and astrocytes in the brain. The serine protease thrombin, which activates PAR-1 during the first hours after stroke, appears to be associated with the cytotoxicity. Thrombin antagonists and PAR-1 inhibitors have been correlated with reduced cell death and behavioral protection after stroke, but no data yet support a mechanistic link between PAR-1 action and benefit. We sought to establish the essential role of PAR-1 in mediating ischemic damage. Using a short hairpin mRNA packaged with green fluorescent protein in a lentivirus vector, we knocked downPAR-1 in the medial caudate nucleus prior to rat middle cerebral artery occlusion (MCAo) and in rat neurons prior to oxygen-glucose deprivation. We also compared aged PAR-1 knockout mice with aged PAR-3, PAR-4 mice and young wild-type mice in a standard MCAo model. Silencing PAR-1 significantly reduced neurological deficits, reduced endothelial barrier leakage, and decreased neuronal degeneration in vivo during MCAo. PAR-1 knock-down in the ischemic medial caudate allowed cells to survive the ischemic injury; infected cells were negative for terminal deoxynucleotidyl transferase mediated dUTP Nick End Labeling (TUNEL) and c-Fos injury markers. Primary cultured neurons infected with PAR-1 short hairpin ribonucleic acid (shRNA) showed increased neuroprotection during hypoxic/aglycemic conditions with or without added thrombin. The aged PAR-1 knockout mice showed decreased infarction and vascular disruption compared to aged controls or young wild types. We demonstrated an essential role for PAR-1 during ischemia. Silencing or removing PAR-1 significantly protected neurons and astrocytes. Further development of agents that act at PAR-1 or its downstream pathways could yield powerful stroke therapy.

Keywords: cerebral ischemia; lentivirus knock-down; oxygen–glucose deprivation; protease activated receptor-1; thrombin.

MeSH terms

  • Animals
  • Astrocytes / metabolism*
  • Brain Ischemia / etiology
  • Brain Ischemia / metabolism*
  • Brain Ischemia / prevention & control
  • Caudate Nucleus / metabolism*
  • Cells, Cultured
  • Disease Models, Animal
  • Infarction, Middle Cerebral Artery / complications
  • Male
  • Mice
  • Mice, Knockout
  • Neurons / metabolism*
  • Neuroprotection*
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Transgenic
  • Receptor, PAR-1 / metabolism*
  • Thrombin / metabolism*

Substances

  • Receptor, PAR-1
  • Thrombin