Effects of ryanodine receptor activation on neurotransmitter release and neuronal cell death following kainic acid-induced status epilepticus

Epilepsy Res. 2005 Jun;65(1-2):59-70. doi: 10.1016/j.eplepsyres.2005.04.006.

Abstract

Dynamic changes in intracellular free Ca(2+) concentration play a crucial role in various neural functions. The inositol 1,4,5-trisphosphate (IP3) receptor (IP3R) and the ryanodine (Ry) receptor (RyR) are involved in Ca(2+)-induced Ca(2+)-release (CICR). Recent studies have shown that type 3 IP3R is highly expressed in rat hippocampal neurons after kainic acid (KA)-induced seizures and that dantrolene, a RyR antagonist, reduces KA-induced neuronal cell death. We investigated the RyR-associated effects of CICR agents on basal and K(+)-evoked releases of GABA and glutamate in rat hippocampus and the changes in expression of mRNA for RyRs in mouse brain after KA-induced seizures. The stimulatory effect of Ry on releases of GABA and glutamate was concentration-dependent in a biphasic manner. The inflection point in concentration-response curves for Ry on GABA release was lower than that for glutamate in both basal and K(+)-evoked conditions, suggesting that hyperactivation of RyR-associated CICR produces the imbalance between GABAergic and glutamatergic transmission. Following KA-induced seizures, transient up-regulation of brain-type RyR mRNA was observed in the hippocampal CA3 region and striatum, and signals for c-Fos mRNA increased transiently in the hippocampus, dentate gyrus and deeper layers of the neocortex. Thereafter, some dead neurons with single-stranded DNA (ssDNA) immunoreactive fragmented nuclei appeared in these areas. These findings suggest that intracellular Ca(2+) release via the RyR might be one of the mechanisms involved in KA-induced neuronal cell death.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism
  • Cell Death / drug effects
  • Chromatography, High Pressure Liquid / methods
  • DNA, Single-Stranded / metabolism
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Electrochemistry / methods
  • Extracellular Space / drug effects
  • Extracellular Space / metabolism
  • Gene Expression Regulation / drug effects
  • Glutamic Acid / metabolism
  • Hippocampus / drug effects
  • Hippocampus / pathology*
  • Immunohistochemistry / methods
  • In Situ Hybridization / methods
  • Kainic Acid
  • Male
  • Mice
  • Neurons / drug effects
  • Neurons / metabolism*
  • Neurotransmitter Agents / metabolism*
  • Potassium / pharmacology
  • Proto-Oncogene Proteins c-fos / metabolism
  • Ruthenium Red / pharmacology
  • Ryanodine / pharmacology
  • Ryanodine Receptor Calcium Release Channel / classification
  • Ryanodine Receptor Calcium Release Channel / genetics
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Status Epilepticus / chemically induced
  • Status Epilepticus / metabolism*
  • Status Epilepticus / pathology
  • Time Factors
  • gamma-Aminobutyric Acid / metabolism

Substances

  • DNA, Single-Stranded
  • Neurotransmitter Agents
  • Proto-Oncogene Proteins c-fos
  • Ryanodine Receptor Calcium Release Channel
  • Ruthenium Red
  • Ryanodine
  • Glutamic Acid
  • gamma-Aminobutyric Acid
  • Potassium
  • Kainic Acid
  • Calcium