Ischemic postconditioning prevents surge of presynaptic glutamate release by activating mitochondrial ATP-dependent potassium channels in the mouse hippocampus

PLoS One. 2019 Apr 12;14(4):e0215104. doi: 10.1371/journal.pone.0215104. eCollection 2019.

Abstract

A mild ischemic load applied after a lethal ischemic insult reduces the subsequent ischemia-reperfusion injury, and is called ischemic postconditioning (PostC). We studied the effect of ischemic PostC on synaptic glutamate release using a whole-cell patch-clamp technique. We recorded spontaneous excitatory post-synaptic currents (sEPSCs) from CA1 pyramidal cells in mouse hippocampal slices. The ischemic load was perfusion of artificial cerebrospinal fluid (ACSF) equilibrated with mixed gas (95% N2 and 5% CO2). The ischemic load was applied for 7.5 min, followed by ischemic PostC 30 s later, consisting of three cycles of 15 s of reperfusion and 15 s of re-ischemia. We found that a surging increase in sEPSCs frequency occurred during the immediate-early reperfusion period after the ischemic insult. We found a significant positive correlation between cumulative sEPSCs and the number of dead CA1 neurons (r = 0.70; p = 0.02). Ischemic PostC significantly suppressed this surge of sEPSCs. The mitochondrial KATP (mito-KATP) channel opener, diazoxide, also suppressed the surge of sEPSCs when applied for 15 min immediately after the ischemic load. The mito-KATP channel blocker, 5-hydroxydecanoate (5-HD), significantly attenuated the suppressive effect of both ischemic PostC and diazoxide application on the surge of sEPSCs. These results suggest that the opening of mito-KATP channels is involved in the suppressive effect of ischemic PostC on synaptic glutamate release and protection against neuronal death. We hypothesize that activation of mito-KATP channels prevents mitochondrial malfunction and breaks mutual facilitatory coupling between glutamate release and Ca2+ entry at presynaptic sites.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Decanoic Acids / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Glutamic Acid / metabolism*
  • Hippocampus / drug effects
  • Hippocampus / metabolism*
  • Hippocampus / pathology
  • Hydroxy Acids / pharmacology
  • Ischemic Postconditioning / methods*
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mitochondria / pathology
  • Myocardial Reperfusion Injury / metabolism
  • Myocardial Reperfusion Injury / pathology
  • Myocardial Reperfusion Injury / prevention & control*
  • Neurons / drug effects
  • Neurons / metabolism*
  • Neurons / pathology
  • Potassium Channel Blockers / pharmacology
  • Potassium Channels / chemistry
  • Potassium Channels / metabolism*

Substances

  • Decanoic Acids
  • Hydroxy Acids
  • Potassium Channel Blockers
  • Potassium Channels
  • mitochondrial K(ATP) channel
  • Glutamic Acid
  • 5-hydroxydecanoic acid
  • Adenosine Triphosphate

Grants and funding

The authors received no specific funding for this work.