Rapid synaptic remodeling by protein kinase C: reciprocal translocation of NMDA receptors and calcium/calmodulin-dependent kinase II

J Neurosci. 2002 Mar 15;22(6):2153-64. doi: 10.1523/JNEUROSCI.22-06-02153.2002.

Abstract

In contrast to the rapid regulation of AMPA receptors, previous evidence has supported the idea that the synaptic density of NMDA-type glutamate receptors is fairly static, modulated only over a long time scale in a homeostatic manner. We report here that selective activation of protein kinase C (PKC) with phorbol esters induces a rapid dispersal of NMDA receptors from synaptic to extrasynaptic plasma membrane in cultured rat hippocampal neurons. PKC activation induced a simultaneous translocation of calcium/calmodulin-dependent kinase II (CaMKII) to synapses but no change in spine number, presynaptic terminal number, or the distribution of AMPA receptors or the synaptic scaffolding protein PSD-95. PKC-induced accumulation of CaMKII was dependent on filamentous actin, whereas dispersal of NMDA receptors occurred by a different mechanism independent of actin or CaMKII. Consistent with the decrease in synaptic density of NMDA receptors, phorbol ester pretreatment reduced excitotoxicity. These results reveal a surprisingly dynamic nature to the molecular composition and functional properties of glutamatergic postsynaptic specializations.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism*
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Cytoskeleton / metabolism
  • Dendrites / metabolism
  • Dendrites / ultrastructure
  • Disks Large Homolog 4 Protein
  • Enzyme Activation / drug effects
  • Gene Expression
  • Green Fluorescent Proteins
  • Intracellular Signaling Peptides and Proteins
  • Luminescent Proteins / genetics
  • Membrane Proteins
  • Nerve Tissue Proteins / metabolism
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism
  • Phorbol Esters / pharmacology
  • Protein Kinase C / metabolism*
  • Protein Transport / drug effects
  • Protein Transport / physiology
  • Rats
  • Receptors, AMPA / metabolism
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Synapses / metabolism*
  • Time Factors

Substances

  • Disks Large Homolog 4 Protein
  • Dlg4 protein, rat
  • Intracellular Signaling Peptides and Proteins
  • Luminescent Proteins
  • Membrane Proteins
  • NR1 NMDA receptor
  • Nerve Tissue Proteins
  • Phorbol Esters
  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • Recombinant Fusion Proteins
  • postsynaptic density proteins
  • Green Fluorescent Proteins
  • Protein Kinase C
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases