Activation of extrasynaptic NMDA receptors induces a PKC-dependent switch in AMPA receptor subtypes in mouse cerebellar stellate cells

J Physiol. 2007 Sep 1;583(Pt 2):537-53. doi: 10.1113/jphysiol.2007.136788. Epub 2007 Jun 21.

Abstract

The repetitive activation of synaptic glutamate receptors can induce a lasting change in the number or subunit composition of synaptic AMPA receptors (AMPARs). However, NMDA receptors that are present extrasynaptically can also be activated by a burst of presynaptic activity, and thus may be involved in the induction of synaptic plasticity. Here we show that the physiological-like activation of extrasynaptic NMDARs induces a lasting change in the synaptic current, by changing the subunit composition of AMPARs at the parallel fibre-to-cerebellar stellate cell synapse. This extrasynaptic NMDAR-induced switch in synaptic AMPARs from GluR2-lacking (Ca(2+)-permeable) to GluR2-containing (Ca(2+)-impermeable) receptors requires the activation of protein kinase C (PKC). These results indicate that the activation of extrasynaptic NMDARs by glutamate spillover is an important mechanism that detects the pattern of afferent activity and subsequently exerts a remote regulation of AMPAR subtypes at the synapse via a PKC-dependent pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzodiazepines / pharmacology
  • Calcium / metabolism
  • Carrier Proteins / metabolism
  • Cell Cycle Proteins
  • Cerebellum / cytology
  • Cerebellum / drug effects
  • Cerebellum / enzymology
  • Cerebellum / metabolism*
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials
  • Glutamic Acid / metabolism
  • Mice
  • Mice, Inbred C57BL
  • N-Methylaspartate / metabolism
  • Neuronal Plasticity* / drug effects
  • Nuclear Proteins / metabolism
  • Organophosphonates / pharmacology
  • Peptide Fragments / pharmacology
  • Piperazines / pharmacology
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism*
  • Protein Kinase C / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Receptors, AMPA / antagonists & inhibitors
  • Receptors, AMPA / metabolism*
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Synapses / drug effects
  • Synapses / enzymology
  • Synapses / metabolism*
  • Synaptic Transmission* / drug effects
  • Time Factors

Substances

  • Carrier Proteins
  • Cell Cycle Proteins
  • Excitatory Amino Acid Antagonists
  • Nuclear Proteins
  • Organophosphonates
  • Peptide Fragments
  • Piperazines
  • Prkcabp protein, mouse
  • Protein Kinase Inhibitors
  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • carboxypiperazinyl propylphosphonic acid
  • protein kinase C (19-36)
  • GYKI 52466
  • Benzodiazepines
  • Glutamic Acid
  • N-Methylaspartate
  • Protein Kinase C
  • glutamate receptor ionotropic, AMPA 2
  • Calcium