Antagonism of ionotropic glutamate receptors attenuates chemical ischemia-induced injury in rat primary cultured myenteric ganglia

PLoS One. 2014 Nov 24;9(11):e113613. doi: 10.1371/journal.pone.0113613. eCollection 2014.

Abstract

Alterations of the enteric glutamatergic transmission may underlay changes in the function of myenteric neurons following intestinal ischemia and reperfusion (I/R) contributing to impairment of gastrointestinal motility occurring in these pathological conditions. The aim of the present study was to evaluate whether glutamate receptors of the NMDA and AMPA/kainate type are involved in myenteric neuron cell damage induced by I/R. Primary cultured rat myenteric ganglia were exposed to sodium azide and glucose deprivation (in vitro chemical ischemia). After 6 days of culture, immunoreactivity for NMDA, AMPA and kainate receptors subunits, GluN(1) and GluA(1-3), GluK(1-3) respectively, was found in myenteric neurons. In myenteric cultured ganglia, in normal metabolic conditions, -AP5, an NMDA antagonist, decreased myenteric neuron number and viability, determined by calcein AM/ethidium homodimer-1 assay, and increased reactive oxygen species (ROS) levels, measured with hydroxyphenyl fluorescein. CNQX, an AMPA/kainate antagonist exerted an opposite action on the same parameters. The total number and viability of myenteric neurons significantly decreased after I/R. In these conditions, the number of neurons staining for GluN1 and GluA(1-3) subunits remained unchanged, while, the number of GluK(1-3)-immunopositive neurons increased. After I/R, -AP5 and CNQX, concentration-dependently increased myenteric neuron number and significantly increased the number of living neurons. Both -AP5 and CNQX (100-500 µM) decreased I/R-induced increase of ROS levels in myenteric ganglia. On the whole, the present data provide evidence that, under normal metabolic conditions, the enteric glutamatergic system exerts a dualistic effect on cultured myenteric ganglia, either by improving or reducing neuron survival via NMDA or AMPA/kainate receptor activation, respectively. However, blockade of both receptor pathways may exert a protective role on myenteric neurons following and I/R damage. The neuroprotective effect may depend, at least in part, on the ability of both receptors to increase intraneuronal ROS production.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • Cell Count
  • Cell Survival / drug effects
  • Cells, Cultured
  • Excitatory Amino Acid Antagonists / pharmacology
  • Ganglia / blood supply
  • Ganglia / cytology
  • Ganglia / metabolism*
  • Glucose / metabolism
  • Immunohistochemistry
  • Ischemia / chemically induced
  • Ischemia / physiopathology
  • Male
  • Myenteric Plexus / blood supply
  • Myenteric Plexus / metabolism*
  • Neurons / drug effects
  • Neurons / metabolism*
  • Rats
  • Reactive Oxygen Species / metabolism
  • Receptors, AMPA / antagonists & inhibitors
  • Receptors, AMPA / metabolism
  • Receptors, Ionotropic Glutamate / antagonists & inhibitors
  • Receptors, Ionotropic Glutamate / metabolism*
  • Receptors, Kainic Acid / antagonists & inhibitors
  • Receptors, Kainic Acid / metabolism
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Reperfusion Injury / physiopathology
  • Sodium Azide / pharmacology

Substances

  • Excitatory Amino Acid Antagonists
  • Reactive Oxygen Species
  • Receptors, AMPA
  • Receptors, Ionotropic Glutamate
  • Receptors, Kainic Acid
  • Receptors, N-Methyl-D-Aspartate
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • 2-Amino-5-phosphonovalerate
  • Sodium Azide
  • Glucose

Grants and funding

The study was supported with grants from the Italian Ministry of Research and University (PRIN 2008) and from grants from the University of Insubria and of Pavia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the change.