Postsynaptic clustering and activation of Pyk2 by PSD-95

J Neurosci. 2010 Jan 13;30(2):449-63. doi: 10.1523/JNEUROSCI.4992-08.2010.

Abstract

The tyrosine kinase Pyk2 plays a unique role in intracellular signal transduction by linking Ca(2+) influx to tyrosine phosphorylation, but the molecular mechanism of Pyk2 activation is unknown. We report that Pyk2 oligomerization by antibodies in vitro or overexpression of PSD-95 in PC6-3 cells induces trans-autophosphorylation of Tyr402, the first step in Pyk2 activation. In neurons, Ca(2+) influx through NMDA-type glutamate receptors causes postsynaptic clustering and autophosphorylation of endogenous Pyk2 via Ca(2+)- and calmodulin-stimulated binding to PSD-95. Accordingly, Ca(2+) influx promotes oligomerization and thereby autoactivation of Pyk2 by stimulating its interaction with PSD-95. We show that this mechanism of Pyk2 activation is critical for long-term potentiation in the hippocampus CA1 region, which is thought to underlie learning and memory.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Antibodies / pharmacology
  • Brain / cytology*
  • Brain / metabolism
  • Calcium / metabolism
  • Calmodulin / pharmacology
  • Cell Line, Transformed
  • Disks Large Homolog 4 Protein
  • Enzyme Inhibitors / pharmacology
  • Excitatory Amino Acid Agonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Focal Adhesion Kinase 2 / immunology
  • Focal Adhesion Kinase 2 / metabolism*
  • Green Fluorescent Proteins / genetics
  • Immunoprecipitation / methods
  • In Vitro Techniques
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Ionomycin / pharmacology
  • Ionophores / pharmacology
  • Male
  • Membrane Proteins / metabolism*
  • N-Methylaspartate / pharmacology
  • Neurons / drug effects
  • Neurons / physiology
  • PDZ Domains / physiology
  • Patch-Clamp Techniques / methods
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Protein Binding / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Sodium Channel Blockers / pharmacology
  • Synapses / metabolism*
  • Tetradecanoylphorbol Acetate / analogs & derivatives
  • Tetradecanoylphorbol Acetate / pharmacology
  • Tetrodotoxin / pharmacology
  • Transfection / methods
  • Tyrosine / metabolism

Substances

  • Antibodies
  • Calmodulin
  • Disks Large Homolog 4 Protein
  • Dlg4 protein, rat
  • Enzyme Inhibitors
  • Excitatory Amino Acid Agonists
  • Intracellular Signaling Peptides and Proteins
  • Ionophores
  • Membrane Proteins
  • Receptors, N-Methyl-D-Aspartate
  • Sodium Channel Blockers
  • Green Fluorescent Proteins
  • Tyrosine
  • Tetrodotoxin
  • Ionomycin
  • 4-O-methyl-12-O-tetradecanoylphorbol 13-acetate
  • N-Methylaspartate
  • Focal Adhesion Kinase 2
  • Tetradecanoylphorbol Acetate
  • Calcium