ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation

J Biol Chem. 2007 Sep 14;282(37):27527-27535. doi: 10.1074/jbc.M701077200. Epub 2007 Jul 16.

Abstract

beta-Adrenergic receptors critically modulate long-lasting synaptic plasticity and long-term memory in the mammalian hippocampus. Persistent long-term potentiation of synaptic strength requires protein synthesis and has been correlated with some forms of hippocampal long-term memory. However, the intracellular processes that initiate protein synthesis downstream of the beta-adrenergic receptor are unidentified. Here we report that activation of beta-adrenergic receptors recruits ERK and mammalian target of rapamycin signaling to facilitate long-term potentiation maintenance at the level of translation initiation. Treatment of mouse hippocampal slices with a beta-adrenergic receptor agonist results in activation of eukaryotic initiation factor 4E and the eukaryotic initiation factor 4E kinase Mnk1, along with inhibition of the translation repressor 4E-BP. This coordinated activation of translation machinery requires concomitant ERK and mammalian target of rapamycin signaling. Taken together, our data identify distinct signaling pathways that converge to regulate beta-adrenergic receptor-dependent protein synthesis during long-term synaptic potentiation in the hippocampus. We suggest that beta-adrenergic receptors play a crucial role in gating the induction of long-lasting synaptic plasticity at the level of translation initiation, a mechanism that may underlie the ability of these receptors to influence the formation of long-lasting memories.

Publication types

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

MeSH terms

  • Animals
  • Eukaryotic Initiation Factor-4E / metabolism
  • Eukaryotic Initiation Factors / physiology
  • Extracellular Signal-Regulated MAP Kinases / physiology*
  • Female
  • Long-Term Potentiation*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Protein Biosynthesis*
  • Protein Kinases / physiology*
  • Receptors, Adrenergic, beta / physiology*
  • Signal Transduction*
  • TOR Serine-Threonine Kinases

Substances

  • Eif4ebp2 protein, mouse
  • Eukaryotic Initiation Factor-4E
  • Eukaryotic Initiation Factors
  • Receptors, Adrenergic, beta
  • Protein Kinases
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases
  • Extracellular Signal-Regulated MAP Kinases