Beta-adrenergic receptor activation rescues theta frequency stimulation-induced LTP deficits in mice expressing C-terminally truncated NMDA receptor GluN2A subunits

Learn Mem. 2011 Jan 21;18(2):118-27. doi: 10.1101/lm.2045311. Print 2011 Feb.

Abstract

Through protein interactions mediated by their cytoplasmic C termini the GluN2A and GluN2B subunits of NMDA receptors (NMDARs) have a key role in the formation of NMDAR signaling complexes at excitatory synapses. Although these signaling complexes are thought to have a crucial role in NMDAR-dependent forms of synaptic plasticity such as long-term potentiation (LTP), the role of the C terminus of GluN2A in coupling NMDARs to LTP enhancing and/or suppressing signaling pathways is unclear. To address this issue we examined the induction of LTP in the hippocampal CA1 region in mice lacking the C terminus of endogenous GluN2A subunits (GluN2AΔC/ΔC). Our results show that truncation of GluN2A subunits produces robust, but highly frequency-dependent, deficits in LTP and a reduction in basal levels of extracellular signal regulated kinase 2 (ERK2) activation and phosphorylation of AMPA receptor GluA1 subunits at a protein kinase A site (serine 845). Consistent with the notion that these signaling deficits contribute to the deficits in LTP in GluN2AΔC/ΔC mice, activating ERK2 and increasing GluA1 S845 phosphorylation through activation of β-adrenergic receptors rescued the induction of LTP in these mutants. Together, our results indicate that the capacity of excitatory synapses to undergo plasticity in response to different patterns of activity is dependent on the coupling of specific signaling pathways to the intracellular domains of the NMDARs and that abnormal plasticity resulting from mutations in NMDARs can be reduced by activation of key neuromodulatory transmitter receptors that engage converging signaling pathways.

Publication types

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

MeSH terms

  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Biophysical Phenomena / genetics
  • Electric Stimulation / methods
  • Excitatory Amino Acid Agonists / pharmacology
  • Hippocampus / cytology
  • Hippocampus / drug effects
  • Hippocampus / physiology*
  • In Vitro Techniques
  • Isoproterenol / pharmacology
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / genetics*
  • Long-Term Potentiation / physiology
  • Mice
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mutation / genetics*
  • N-Methylaspartate / pharmacology
  • Patch-Clamp Techniques / methods
  • Peptide Fragments / metabolism
  • Phosphorylation / drug effects
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / physiology
  • Receptors, Adrenergic, beta / metabolism*
  • Receptors, N-Methyl-D-Aspartate / deficiency
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Serine / metabolism

Substances

  • Adrenergic beta-Agonists
  • Excitatory Amino Acid Agonists
  • Peptide Fragments
  • Receptors, Adrenergic, beta
  • Receptors, N-Methyl-D-Aspartate
  • Serine
  • N-Methylaspartate
  • Mitogen-Activated Protein Kinase 1
  • Isoproterenol
  • N-methyl D-aspartate receptor subtype 2A