Gravin orchestrates protein kinase A and β2-adrenergic receptor signaling critical for synaptic plasticity and memory

J Neurosci. 2012 Dec 12;32(50):18137-49. doi: 10.1523/JNEUROSCI.3612-12.2012.

Abstract

A kinase-anchoring proteins (AKAPs) organize compartmentalized pools of protein kinase A (PKA) to enable localized signaling events within neurons. However, it is unclear which of the many expressed AKAPs in neurons target PKA to signaling complexes important for long-lasting forms of synaptic plasticity and memory storage. In the forebrain, the anchoring protein gravin recruits a signaling complex containing PKA, PKC, calmodulin, and PDE4D (phosphodiesterase 4D) to the β2-adrenergic receptor. Here, we show that mice lacking the α-isoform of gravin have deficits in PKA-dependent long-lasting forms of hippocampal synaptic plasticity including β2-adrenergic receptor-mediated plasticity, and selective impairments of long-term memory storage. Furthermore, both hippocampal β2-adrenergic receptor phosphorylation by PKA, and learning-induced activation of ERK in the CA1 region of the hippocampus are attenuated in mice lacking gravin-α. We conclude that gravin compartmentalizes a significant pool of PKA that regulates learning-induced β2-adrenergic receptor signaling and ERK activation in the hippocampus in vivo, thereby organizing molecular interactions between glutamatergic and noradrenergic signaling pathways for long-lasting synaptic plasticity, and memory storage.

Publication types

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

MeSH terms

  • A Kinase Anchor Proteins / metabolism*
  • Animals
  • Blotting, Western
  • Cell Cycle Proteins / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Electric Stimulation
  • Female
  • Hippocampus / physiology
  • Immunohistochemistry
  • Immunoprecipitation
  • In Situ Hybridization
  • Male
  • Maze Learning / physiology
  • Memory / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Neuronal Plasticity / physiology*
  • Real-Time Polymerase Chain Reaction
  • Receptors, Adrenergic, beta-2 / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*

Substances

  • A Kinase Anchor Proteins
  • Akap12 protein, mouse
  • Cell Cycle Proteins
  • Receptors, Adrenergic, beta-2
  • Cyclic AMP-Dependent Protein Kinases