Memantine Protects From Exacerbation of Ischemic Stroke and Blood Brain Barrier Disruption in Mild But Not Severe Hyperhomocysteinemia

J Am Heart Assoc. 2020 Feb 18;9(4):e013368. doi: 10.1161/JAHA.119.013368. Epub 2020 Feb 13.

Abstract

Background Hyperhomocysteinemia is a risk factor for ischemic stroke; however, a targeted treatment strategy is lacking partly because of limited understanding of the causal role of homocysteine in cerebrovascular pathogenesis. Methods and Results In a genetic model of cystathionine beta synthase (CBS) deficiency, we tested the hypothesis that elevation in plasma total homocysteine exacerbates cerebrovascular injury and that memantine, a N-methyl-D-aspartate receptor antagonist, is protective. Mild or severe elevation in plasma total homocysteine was observed in Cbs+/- (6.1±0.3 μmol/L) or Cbs-/- (309±18 μmol/L) mice versus Cbs+/+ (3.1±0.6 μmol/L) mice. Surprisingly, Cbs-/- and Cbs+/- mice exhibited similar increases in cerebral infarct size following middle cerebral artery ischemia/reperfusion injury, despite the much higher total homocysteine levels in Cbs-/- mice. Likewise, disruption of the blood brain barrier was observed in both Cbs+/- and Cbs-/- mice. Administration of the N-methyl-D-aspartate receptor antagonist memantine protected Cbs+/- but not Cbs-/- mice from cerebral infarction and blood brain barrier disruption. Our data suggest that the differential effect of memantine in Cbs+/- versus Cbs-/- mice may be related to changes in expression of N-methyl-D-aspartate receptor subunits. Cbs-/-, but not Cbs+/- mice had increased expression of NR2B subunit, which is known to be relatively insensitive to homocysteine. Conclusions These data provide experimental evidence that even a mild increase in plasma total homocysteine can exacerbate cerebrovascular injury and suggest that N-methyl-D-aspartate receptor antagonism may represent a strategy to prevent reperfusion injury after acute ischemic stroke in patients with mild hyperhomocysteinemia.

Keywords: blood brain barrier; cystathionine beta synthase; homocysteine; stroke.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / pathology
  • Cell Death / drug effects
  • Cells, Cultured
  • Cystathionine beta-Synthase / deficiency
  • Cystathionine beta-Synthase / genetics
  • Disease Models, Animal
  • Disease Progression
  • Excitatory Amino Acid Antagonists / pharmacology*
  • Homocysteine / blood*
  • Homocystinuria / enzymology
  • Homocystinuria / genetics
  • Hyperhomocysteinemia / blood
  • Hyperhomocysteinemia / drug therapy*
  • Hyperhomocysteinemia / enzymology
  • Hyperhomocysteinemia / genetics
  • Infarction, Middle Cerebral Artery / metabolism
  • Infarction, Middle Cerebral Artery / pathology
  • Infarction, Middle Cerebral Artery / prevention & control*
  • Memantine / pharmacology*
  • Mice, Knockout
  • Neurons / drug effects*
  • Neurons / metabolism
  • Neurons / pathology
  • Neuroprotective Agents / pharmacology*
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors*
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Severity of Illness Index

Substances

  • Excitatory Amino Acid Antagonists
  • NR2B NMDA receptor
  • Neuroprotective Agents
  • Receptors, N-Methyl-D-Aspartate
  • Homocysteine
  • Cystathionine beta-Synthase
  • Memantine