P2X7 receptor antagonism inhibits p38 mitogen-activated protein kinase activation and ameliorates neuronal apoptosis after subarachnoid hemorrhage in rats

Crit Care Med. 2013 Dec;41(12):e466-74. doi: 10.1097/CCM.0b013e31829a8246.

Abstract

Objectives: Brilliant blue G, a selective P2X7 receptor antagonist, exhibits neuroprotective properties. This study examined whether brilliant blue G treatment ameliorates early brain injury after experimental subarachnoid hemorrhage, specifically via inhibiting p38 mitogen-activated protein kinase-related proapoptotic pathways.

Design: Controlled in vivo laboratory study.

Setting: Animal research laboratory.

Subjects: One hundred fifty-four adult male Sprague-Dawley rats weighing 280-320 g.

Interventions: Subarachnoid hemorrhage was induced in rats by endovascular perforation. Experiment 1 implemented sham-operated rats (sham) and subarachnoid hemorrhage animals, which received vehicle (subarachnoid hemorrhage + vehicle), brilliant blue G (subarachnoid hemorrhage + brilliant blue G), or brilliant blue G plus 2'(3')-O-(4-Benzoylbenzoyl)adenosine 5'-triphosphate (BzATP) (subarachnoid hemorrhage + brilliant blue G + BzATP). The animals were intraperitoneally treated with brilliant blue G (30 mg/kg) at 30 minutes after subarachnoid hemorrhage. BzATP (50 μg/rat), a P2X7 receptor agonist, was intracerebroventricularly administered. Experiment 2 implemented sham-operated rats (sham) and subarachnoid hemorrhage animals, which received vehicle (subarachnoid hemorrhage + vehicle), scramble small interfering RNA (subarachnoid hemorrhage + scramble small interfering RNA), or P2X7 receptor small interfering RNA (subarachnoid hemorrhage + P2X7 receptor small interfering RNA). Subarachnoid hemorrhage grading, neurobehavioral score, and brain edema were evaluated at 24 and 72 hours after surgery. The expression of phosphorylated p38 mitogen-activated protein kinase, phosphorylated extracellular signal-regulated kinases, phosphorylated c-Jun N-terminal kinases, P2X7 receptor, Bcl-2, and cleaved caspase-3 in the left cerebral hemisphere were determined by Western blot. Neuronal apoptosis was examined by double immunofluorescence staining using P2X7 receptor, terminal deoxynucleotidyl transferase-mediated uridine 5'-triphosphate-biotin nick end-labeling, and neuronal nuclei.

Measurements and main results: Brilliant blue G significantly improved neurobehavioral function and ameliorated brain water content at 24 and 72 hours after subarachnoid hemorrhage. BzATP reversed these treatment effects. Brilliant blue G attenuated neuronal apoptosis in the subcortex, which was associated with decreased expression of phosphorylated p38 mitogen-activated protein kinase and cleaved caspase-3 and an increased expression of Bcl-2 in the left cerebral hemisphere. The beneficial effects of P2X7 receptor small interfering RNA were also mediated by a p38 mitogen-activated protein kinase pathway.

Conclusions: Inhibition of P2X7 receptor by brilliant blue G or P2X7 receptor small interfering RNA can prevent early brain injury via p38 mitogen-activated protein kinase after subarachnoid hemorrhage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / analogs & derivatives
  • Adenosine Triphosphate / therapeutic use
  • Animals
  • Apoptosis / drug effects
  • Caspase 3 / metabolism
  • Enzyme Activation / drug effects*
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Male
  • Neurons / physiology
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Purinergic P2X Receptor Agonists / therapeutic use
  • Purinergic P2X Receptor Antagonists / therapeutic use*
  • RNA, Small Interfering / therapeutic use
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Purinergic P2X7 / genetics
  • Receptors, Purinergic P2X7 / metabolism
  • Rosaniline Dyes / therapeutic use*
  • Subarachnoid Hemorrhage / drug therapy*
  • Subarachnoid Hemorrhage / enzymology*
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Proto-Oncogene Proteins c-bcl-2
  • Purinergic P2X Receptor Agonists
  • Purinergic P2X Receptor Antagonists
  • RNA, Small Interfering
  • Receptors, Purinergic P2X7
  • Rosaniline Dyes
  • 3'-O-(4-benzoyl)benzoyladenosine 5'-triphosphate
  • Adenosine Triphosphate
  • Extracellular Signal-Regulated MAP Kinases
  • JNK Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Caspase 3
  • coomassie Brilliant Blue