Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity

Neuron. 2008 Dec 10;60(5):788-802. doi: 10.1016/j.neuron.2008.10.014.

Abstract

Long-term potentiation (LTP) is accompanied by dendritic spine growth and changes in the composition of the postsynaptic density (PSD). We find that activity-dependent growth of apical spines of CA1 pyramidal neurons is accompanied by destabilization of the PSD that results in transient loss and rapid replacement of PSD-95 and SHANK2. Signaling through PSD-95 is required for activity-dependent spine growth and trafficking of SHANK2. N-terminal PDZ and C-terminal guanylate kinase domains of PSD-95 are required for both processes, indicating that PSD-95 coordinates multiple signals to regulate morphological plasticity. Activity-dependent trafficking of PSD-95 is triggered by phosphorylation at serine 73, a conserved calcium/calmodulin-dependent protein kinase II (CaMKII) consensus phosphorylation site, which negatively regulates spine growth and potentiation of synaptic currents. We propose that PSD-95 and CaMKII act at multiple steps during plasticity induction to initially trigger and later terminate spine growth by trafficking growth-promoting PSD proteins out of the active spine.

Publication types

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

MeSH terms

  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine / analogs & derivatives
  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine / pharmacology
  • Animals
  • Animals, Newborn
  • Dendritic Spines / drug effects
  • Dendritic Spines / physiology*
  • Disks Large Homolog 4 Protein
  • Electric Stimulation / methods
  • Enzyme Inhibitors / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Glutamates / pharmacology
  • Green Fluorescent Proteins / biosynthesis
  • Green Fluorescent Proteins / genetics
  • Hippocampus / cytology
  • Indoles / pharmacology
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Long-Term Potentiation / physiology
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Nerve Tissue Proteins / metabolism
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Neurons / cytology*
  • Neurons / drug effects
  • Organ Culture Techniques
  • Patch-Clamp Techniques / methods
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Piperazines / pharmacology
  • Point Mutation
  • Protein Structure, Tertiary
  • Protein Transport / drug effects
  • Rats
  • Rats, Sprague-Dawley
  • Serine / metabolism*
  • Time Factors

Substances

  • 4-methoxy-7-nitroindolinyl-glutamate
  • Disks Large Homolog 4 Protein
  • Dlg4 protein, rat
  • Enzyme Inhibitors
  • Excitatory Amino Acid Antagonists
  • Glutamates
  • Indoles
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Piperazines
  • Shank2 protein, rat
  • Green Fluorescent Proteins
  • Serine
  • KN 62
  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine
  • 3-(2-carboxypiperazin-4-yl)propyl-1-phosphonic acid