A microRNA negative feedback loop downregulates vesicle transport and inhibits fear memory

Elife. 2016 Dec 21:5:e22467. doi: 10.7554/eLife.22467.

Abstract

The SNARE-mediated vesicular transport pathway plays major roles in synaptic remodeling associated with formation of long-term memories, but the mechanisms that regulate this pathway during memory acquisition are not fully understood. Here we identify miRNAs that are up-regulated in the rodent hippocampus upon contextual fear-conditioning and identify the vesicular transport and synaptogenesis pathways as the major targets of the fear-induced miRNAs. We demonstrate that miR-153, a member of this group, inhibits the expression of key components of the vesicular transport machinery, and down-regulates Glutamate receptor A1 trafficking and neurotransmitter release. MiR-153 expression is specifically induced during LTP induction in hippocampal slices and its knockdown in the hippocampus of adult mice results in enhanced fear memory. Our results suggest that miR-153, and possibly other fear-induced miRNAs, act as components of a negative feedback loop that blocks neuronal hyperactivity at least partly through the inhibition of the vesicular transport pathway.

Keywords: cell biology; hippocampus; learning; memory; miRNA; mouse; negative feed back loop; rat; synaptic plasticity.

Publication types

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

MeSH terms

  • Animals
  • Fear*
  • Feedback, Physiological*
  • Hippocampus / physiology*
  • Memory*
  • Mice
  • MicroRNAs / metabolism*
  • Neurons / physiology*
  • Neurotransmitter Agents / metabolism
  • Receptors, Glutamate / metabolism
  • Synaptic Vesicles / metabolism*

Substances

  • MIRN153 microRNA, mouse
  • MicroRNAs
  • Neurotransmitter Agents
  • Receptors, Glutamate