Hydrogen sulfide protects blood-brain barrier integrity following cerebral ischemia

J Neurochem. 2014 Jun;129(5):827-38. doi: 10.1111/jnc.12695. Epub 2014 Mar 27.

Abstract

By using two structurally unrelated hydrogen sulfide (H2 S) donors 5-(4-methoxyphenyl) -3H-1, 2-dithiole-3-thione (ADT) and sodium hydrosulfide (NaHS), this study investigated if H2 S protected blood-brain barrier (BBB) integrity following middle cerebral artery occlusion (MCAO). ICR mice underwent MCAO and received H2 S donors at 3 h after reperfusion. Infarction, neurological scores, brain edema, Evans blue (EB) extravasation, and tight junction protein expression were examined at 48 h after MCAO. We also investigated if ADT protected BBB integrity by suppressing post-ischemic inflammation-induced Matrix Metalloproteimase-9 (MMP9) and Nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX). ADT increased blood H2 S concentrations, decreased infarction, and improved neurological deficits. Particularly, ADT reduced EB extravasation, brain edema and preserved expression of tight junction proteins in the ischemic brain. NaHS also increased blood H2 S levels and reduced EB extravasation following MCAO. Moreover, ADT inhibited expression of pro-inflammatory markers induced Nitric Oxide Synthase (iNOS) and IL-1β while enhanced expression of anti-inflammatory markers arginase 1 and IL-10 in the ischemic brain. Accordingly, ADT attenuated ischemia-induced expression and activity of MMP9. Moreover, ADT reduced NOX-4 mRNA expression, NOX activity, and inhibited nuclear translocation of Nuclear Factor Kappa-B (NF-κB) in the ischemic brain. In conclusion, H2 S donors protected BBB integrity following experimental stroke possibly by acting through NF-κB inhibition to suppress neuroinflammation induction of MMP9 and NOX4-derived free radicals. To determine H2 S effects on blood-brain barrier (BBB) disruption following stroke, we used two structurally unrelated H2 S donors ADT and NaHS. Both ADT and NaHS remarkably protected BBB integrity following experimental stroke. The slow-releasing donor ADT also reduced post-ischemic inflammation-induced expression and activity of MMP9 and NOX4 in the ischemic brain possibly by inhibiting NF-κB activation.

Keywords: Blood-brain barrier; cerebral ischemia; hydrogen sulfide; vasoprotection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal / drug effects
  • Blood-Brain Barrier / drug effects*
  • Blotting, Western
  • Brain Edema / pathology
  • Brain Ischemia / drug therapy*
  • Brain Ischemia / pathology*
  • Coloring Agents
  • Enzyme-Linked Immunosorbent Assay
  • Evans Blue
  • Heterocyclic Compounds, 1-Ring / pharmacology*
  • Hydrogen Sulfide / blood
  • Hydrogen Sulfide / pharmacology*
  • Infarction, Middle Cerebral Artery / pathology
  • Infarction, Middle Cerebral Artery / prevention & control
  • Interleukin-10 / metabolism
  • Male
  • Mice
  • Mice, Inbred ICR
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / metabolism
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / metabolism
  • Neuroprotective Agents*
  • Peroxidase / metabolism
  • Real-Time Polymerase Chain Reaction
  • Thiones / pharmacology*

Substances

  • 5-(4-methoxyphenyl)-3H-1,2-dithiole-3-thione
  • Coloring Agents
  • Heterocyclic Compounds, 1-Ring
  • NF-kappa B
  • Neuroprotective Agents
  • Thiones
  • Interleukin-10
  • Evans Blue
  • Peroxidase
  • NADPH Oxidases
  • Hydrogen Sulfide