Syngap+/- CA1 Pyramidal Neurons Exhibit Upregulated Translation of Long MRNAs Associated with LTP

eNeuro. 2025 May 19;12(5):ENEURO.0086-25.2025. doi: 10.1523/ENEURO.0086-25.2025. Print 2025 May.

Abstract

In the Syngap+/- model of SYNGAP1-related intellectual disability (SRID), excessive neuronal protein synthesis is linked to deficits in synaptic plasticity. Here, we use Translating Ribosome Affinity Purification and RNA-seq (TRAP-seq) to identify mistranslating mRNAs in Syngap+/- CA1 pyramidal neurons that exhibit occluded long-term potentiation (LTP). We find the translation environment is significantly altered in a manner that is distinct from the Fmr1-/y model of fragile X syndrome (FXS), another monogenic model of autism and intellectual disability. The Syngap+/- translatome is enriched for regulators of DNA repair and mimics changes induced with chemical LTP (cLTP) in WT. This includes a striking upregulation in the translation of mRNAs with a longer-length (>2 kb) coding sequence (CDS). In contrast, long CDS transcripts are downregulated with induction of Gp1 metabotropic glutamate receptor-induced long-term depression (mGluR-LTD) in WT, and in the Fmr1-/y model that exhibits occluded mGluR-LTD. Together, our results show the Syngap+/- and Fmr1-/y models mimic the translation environments of LTP and LTD, respectively, consistent with the saturation of plasticity states in each model. Moreover, we show that translation of >2 kb mRNAs is a defining feature of LTP that is oppositely regulated during LTD, revealing a novel mRNA signature of plasticity.

Keywords: Fragile X; LTD; LTP; Syngap; translation.

MeSH terms

  • Animals
  • CA1 Region, Hippocampal* / metabolism
  • Fragile X Messenger Ribonucleoprotein 1 / genetics
  • Long-Term Potentiation* / genetics
  • Long-Term Potentiation* / physiology
  • Long-Term Synaptic Depression / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Protein Biosynthesis* / physiology
  • Pyramidal Cells* / metabolism
  • RNA, Messenger* / genetics
  • RNA, Messenger* / metabolism
  • Up-Regulation
  • ras GTPase-Activating Proteins* / genetics
  • ras GTPase-Activating Proteins* / metabolism

Substances

  • RNA, Messenger
  • ras GTPase-Activating Proteins
  • Fragile X Messenger Ribonucleoprotein 1
  • Syngap1 protein, mouse