Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand

J Neurosci. 2004 Nov 10;24(45):10248-59. doi: 10.1523/JNEUROSCI.0546-04.2004.

Abstract

Interactions between NMDA receptors (NMDARs) and the PDZ [postsynaptic density-95 (PSD-95)/Discs large/zona occludens-1] domains of PSD-95/SAP90 (synapse-associated protein with a molecular weight of 90 kDa) family proteins play important roles in the synaptic targeting and signaling of NMDARs. However, little is known about the mechanisms that regulate these PDZ domain-mediated interactions. Here we show that casein kinase II (CK2) phosphorylates the serine residue (Ser1480) within the C-terminal PDZ ligand (IESDV) of the NR2B subunit of NMDAR in vitro and in vivo. Phosphorylation of Ser1480 disrupts the interaction of NR2B with the PDZ domains of PSD-95 and SAP102 and decreases surface NR2B expression in neurons. Interestingly, activity of the NMDAR and Ca2+/calmodulin-dependent protein kinase II regulates CK2 phosphorylation of Ser1480. Furthermore, CK2 colocalizes with NR1 and PSD-95 at synaptic sites. These results indicate that activity-dependent CK2 phosphorylation of the NR2B PDZ ligand regulates the interaction of NMDAR with PSD-95/SAP90 family proteins as well as surface NMDAR expression and may be a critical mechanism for modulating excitatory synaptic function and plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • Amino Acid Sequence
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / physiology
  • Casein Kinase II / physiology*
  • Cell Line
  • Colforsin / pharmacology
  • Cyclic AMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Disks Large Homolog 4 Protein
  • Enzyme Activation
  • Hippocampus / cytology
  • Hippocampus / metabolism
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Ligands
  • Membrane Proteins
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Nerve Tissue Proteins / metabolism*
  • Neuronal Plasticity / physiology*
  • Phosphorylation
  • Phosphoserine / metabolism
  • Protein Interaction Mapping
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism
  • Protein Processing, Post-Translational*
  • Protein Structure, Tertiary
  • Protein Subunits
  • Protein Transport / physiology*
  • Rats
  • Receptors, N-Methyl-D-Aspartate / chemistry
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Recombinant Fusion Proteins / metabolism
  • Structure-Activity Relationship
  • Synapses / metabolism*
  • Tetradecanoylphorbol Acetate / pharmacology

Substances

  • DLG4 protein, human
  • Disks Large Homolog 4 Protein
  • Dlg4 protein, rat
  • Intracellular Signaling Peptides and Proteins
  • Ligands
  • Membrane Proteins
  • NR2B NMDA receptor
  • Nerve Tissue Proteins
  • Protein Subunits
  • Receptors, N-Methyl-D-Aspartate
  • Recombinant Fusion Proteins
  • postsynaptic density proteins
  • Phosphoserine
  • Colforsin
  • 2-Amino-5-phosphonovalerate
  • Casein Kinase II
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Tetradecanoylphorbol Acetate