A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons

J Neurosci. 2006 Feb 1;26(5):1604-15. doi: 10.1523/JNEUROSCI.4722-05.2006.

Abstract

Several lines of evidence suggest that a hypoglutamatergic condition may induce a phenotypic loss of cortical parvalbumin (PV)-positive GABAergic interneurons, such as that observed in brain tissue of schizophrenic subjects. However, it is not known whether the loss of PV interneurons is a consequence of the hypoglutamatergic condition or a secondary aspect of the disease. We characterized the signaling and subunit expression of NMDA receptors in cultured cortical PV interneurons and determined whether a hypoglutamatergic condition, created by direct application of sublethal concentrations of ketamine or subunit-selective NMDA receptor antagonists, can affect the expression of the GABAergic markers as observed in vivo. Real-time PCR performed on mRNA isolated from single neurons showed that PV interneurons present a fivefold higher NR2A/NR2B ratio than pyramidal neurons. Brief, nontoxic, exposure to NMDA led to an increase in ERK1/2 (extracellular signal-regulated kinase 1/2) and cAMP response element-binding protein phosphorylation in PV interneurons, and this increase was blocked by the NR2A-selective antagonist NVP-AAM077. Application of the nonselective NMDA receptor antagonist ketamine, at sublethal concentrations, induced a time and dose-dependent decrease in parvalbumin and GAD67 immunoreactivity specifically in PV interneurons. These effects were reversible and were also observed with the NR2A-selective antagonist, whereas the NR2B-selective antagonist Ro-25-6981 only partially reduced GAD67 immunoreactivity. Coexposure to the calcium channel opener BayK, or the group I metabotropic glutamate receptor agonist DHPG [(RS)-3,5-dihydroxyphenylglycine] attenuated the decrease in GAD67 and parvalbumin induced by the NMDA receptor antagonists. These results suggest that the activity of NR2A-containing NMDA receptors play a pivotal role in the maintenance of the GABAergic function of PV interneurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism
  • Cells, Cultured
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Excitatory Amino Acid Antagonists / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Glutamate Decarboxylase / analysis
  • Glutamate Decarboxylase / immunology
  • Glutamate Decarboxylase / metabolism*
  • Immunohistochemistry
  • Interneurons / chemistry
  • Interneurons / drug effects
  • Interneurons / metabolism*
  • Isoenzymes / analysis
  • Isoenzymes / immunology
  • Isoenzymes / metabolism*
  • Ketamine / pharmacology
  • Mice
  • N-Methylaspartate / pharmacology
  • Parvalbumins / analysis
  • Parvalbumins / immunology
  • Parvalbumins / metabolism*
  • Patch-Clamp Techniques
  • Phosphorylation
  • Prosencephalon / cytology
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / physiology*

Substances

  • Cyclic AMP Response Element-Binding Protein
  • Excitatory Amino Acid Antagonists
  • Isoenzymes
  • NR2A NMDA receptor
  • Parvalbumins
  • Receptors, N-Methyl-D-Aspartate
  • N-Methylaspartate
  • Ketamine
  • Extracellular Signal-Regulated MAP Kinases
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1
  • Calcium