Inhibition of G9a/GLP Complex Promotes Long-Term Potentiation and Synaptic Tagging/Capture in Hippocampal CA1 Pyramidal Neurons

Cereb Cortex. 2017 Jun 1;27(6):3161-3171. doi: 10.1093/cercor/bhw170.

Abstract

Epigenetic regulations play an important role in regulating the learning and memory processes. G9a/G9a-like protein (GLP) lysine dimethyltransferase complex controls a prominent histone H3 lysine9 dimethylation (H3K9me2) that results in transcriptional silencing of the chromatin. Here, we report that the inhibition of G9a/GLP complex by either of the substrate competitive inhibitors UNC 0638 or BIX 01294 reinforces protein synthesis-independent long-term potentiation (early-LTP) to protein synthesis-dependent long-term potentiation (late-LTP). The reinforcement effect was observed if the inhibitors were present during the induction of early-LTP and in addition when G9a/GLP complex inhibition was carried out by priming of synapses within an interval of 30 min before or after the induction of early-LTP. Surprisingly, the reinforced LTP by G9a/GLP complex inhibition was able to associate with a weak plasticity event from nearby independent synaptic populations, resulting in synaptic tagging/capture (STC). We have identified brain-derived neurotrophic factor (BDNF) as a critical plasticity protein that maintains G9a/GLP complex inhibition-mediated LTP facilitation and its STC. Our study reveals an epigenetic mechanism for promoting plasticity and associativity by G9a/GLP complex inhibition, and it may engender a promising epigenetic target for enhancing memory in neural networks.

Keywords: BDNF; G9a/GLP; long-term potentiation; metaplasticity; synaptic tagging; synaptic tagging and capture.

MeSH terms

  • Animals
  • Azepines / pharmacology
  • Brain-Derived Neurotrophic Factor / metabolism
  • CA1 Region, Hippocampal / cytology*
  • Chromatin Immunoprecipitation
  • Electric Stimulation
  • Enzyme Inhibitors / pharmacology
  • Histone-Lysine N-Methyltransferase / genetics
  • Histone-Lysine N-Methyltransferase / metabolism*
  • In Vitro Techniques
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology*
  • Male
  • Models, Biological
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / physiology*
  • Quinazolines / pharmacology
  • Rats
  • Rats, Wistar
  • Synapses / drug effects
  • Synapses / physiology*

Substances

  • Azepines
  • BIX 01294
  • Brain-Derived Neurotrophic Factor
  • Enzyme Inhibitors
  • Quinazolines
  • UNC 0638
  • Ehmt2 protein, rat
  • Histone-Lysine N-Methyltransferase