Visualization of spatiotemporal energy dynamics of hippocampal neurons by mass spectrometry during a kainate-induced seizure

Yuki Sugiura, Ryo Taguchi, Mitsutoshi Setou

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

We report the use of matrix-assisted laser desorption/ionization (MALDI) imaging mass spectrometry combined with capillary electrophoresis (CE) mass spectrometry to visualize energy metabolism in the mouse hippocampus by imaging energy-related metabolites. We show the distribution patterns of ATP, ADP, and AMP in the hippocampus as well as changes in their amounts and distribution patterns in a murine model of limbic, kainate-induced seizure. As an acute response to kainate administration, we found massive and moderate reductions in ATP and ADP levels, respectively, but no significant changes in AMP levels-especially in cells of the CA3 layer. The results suggest the existence of CA3 neuron-selective energy metabolism at the anhydride bonds of ATP and ADP in the hippocampal neurons during seizure. In addition, metabolome analysis of energy synthesis pathways indicates accelerated glycolysis and possibly TCA cycle activity during seizure, presumably due to the depletion of ATP. Consistent with this result, the observed energy depletion significantly recovered up to 180 min after kainate administration. However, the recovery rate was remarkably low in part of the data-pixel population in the CA3 cell layer region, which likely reflects acute and CA3-selective neural death. Taken together, the present approach successfully revealed the spatiotemporal energy metabolism of the mouse hippocampus at a cellular resolution-both quantitatively and qualitatively. We aim to further elucidate various metabolic processes in the neural system.

Original languageEnglish
Article numbere17952
JournalPLoS One
Volume6
Issue number3
DOIs
Publication statusPublished - 2011
Externally publishedYes

Fingerprint

Kainic Acid
hippocampus
seizures
energy metabolism
Neurons
Mass spectrometry
Mass Spectrometry
Seizures
Visualization
Adenosine Triphosphate
neurons
mass spectrometry
Adenosine Diphosphate
Energy Metabolism
Hippocampus
energy
Adenosine Monophosphate
image analysis
anhydrides
capillary electrophoresis

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Visualization of spatiotemporal energy dynamics of hippocampal neurons by mass spectrometry during a kainate-induced seizure. / Sugiura, Yuki; Taguchi, Ryo; Setou, Mitsutoshi.

In: PLoS One, Vol. 6, No. 3, e17952, 2011.

Research output: Contribution to journalArticle

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