Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex

Mol Cell. 2012 Jul 27;47(2):253-66. doi: 10.1016/j.molcel.2012.05.016. Epub 2012 Jun 21.

Abstract

Translational control of mRNAs in dendrites is essential for certain forms of synaptic plasticity and learning and memory. CPEB is an RNA-binding protein that regulates local translation in dendrites. Here, we identify poly(A) polymerase Gld2, deadenylase PARN, and translation inhibitory factor neuroguidin (Ngd) as components of a dendritic CPEB-associated polyadenylation apparatus. Synaptic stimulation induces phosphorylation of CPEB, PARN expulsion from the ribonucleoprotein complex, and polyadenylation in dendrites. A screen for mRNAs whose polyadenylation is altered by Gld2 depletion identified >100 transcripts including one encoding NR2A, an NMDA receptor subunit. shRNA depletion studies demonstrate that Gld2 promotes and Ngd inhibits dendritic NR2A expression. Finally, shRNA-mediated depletion of Gld2 in vivo attenuates protein synthesis-dependent long-term potentiation (LTP) at hippocampal dentate gyrus synapses; conversely, Ngd depletion enhances LTP. These results identify a pivotal role for polyadenylation and the opposing effects of Gld2 and Ngd in hippocampal synaptic plasticity.

Publication types

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

MeSH terms

  • Animals
  • Cytoplasm / metabolism*
  • Dendrites / metabolism
  • Hippocampus / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuronal Plasticity*
  • Nuclear Proteins / metabolism
  • Polyadenylation
  • Polynucleotide Adenylyltransferase / metabolism
  • Protein Biosynthesis*
  • RNA-Binding Proteins / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Repressor Proteins / metabolism
  • Ribonucleoproteins / metabolism
  • Synaptic Transmission*
  • Transcription Factors / metabolism
  • mRNA Cleavage and Polyadenylation Factors / metabolism

Substances

  • CPEB protein, mouse
  • CPEB1 protein, human
  • CPEB1 protein, rat
  • NGDN protein, human
  • Nuclear Proteins
  • RNA-Binding Proteins
  • Repressor Proteins
  • Ribonucleoproteins
  • SYMPK protein, human
  • Transcription Factors
  • mRNA Cleavage and Polyadenylation Factors
  • neuroguidin protein, mouse
  • Gld2 protein, mouse
  • Polynucleotide Adenylyltransferase
  • TENT2 protein, human
  • Tent2 protein, rat

Associated data

  • GEO/GSE37695