Hippocampal long-term synaptic depression and memory deficits induced in early amyloidopathy are prevented by enhancing G-protein-gated inwardly rectifying potassium channel activity

J Neurochem. 2020 May;153(3):362-376. doi: 10.1111/jnc.14946. Epub 2020 Jan 30.

Abstract

Hippocampal synaptic plasticity disruption by amyloid-β (Aβ) peptides + thought to be responsible for learning and memory impairments in Alzheimer's disease (AD) early stage. Failures in neuronal excitability maintenance seems to be an underlying mechanism. G-protein-gated inwardly rectifying potassium (GirK) channels control neural excitability by hyperpolarization in response to many G-protein-coupled receptors activation. Here, in early in vitro and in vivo amyloidosis mouse models, we study whether GirK channels take part of the hippocampal synaptic plasticity impairments generated by Aβ1-42 . In vitro electrophysiological recordings from slices showed that Aβ1-42 alters synaptic plasticity by switching high-frequency stimulation (HFS) induced long-term potentiation (LTP) to long-term depression (LTD), which led to in vivo hippocampal-dependent memory deficits. Remarkably, selective pharmacological activation of GirK channels with ML297 rescued both HFS-induced LTP and habituation memory from Aβ1-42 action. Moreover, when GirK channels were specifically blocked by Tertiapin-Q, their activation with ML297 failed to rescue LTP from the HFS-dependent LTD induced by Aβ1-42 . On the other hand, the molecular analysis of the recorded slices by western blot showed that the expression of GIRK1/2 subunits, which form the prototypical GirK channel in the hippocampus, was not significantly regulated by Aβ1-42 . However, immunohistochemical examination of our in vivo amyloidosis model showed Aβ1-42 to down-regulate hippocampal GIRK1 subunit expression. Together, our results describe an Aβ-mediated deleterious synaptic mechanism that modifies the induction threshold for hippocampal LTP/LTD and underlies memory alterations observed in amyloidosis models. In this scenario, GirK activation assures memory formation by preventing the transformation of HFS-induced LTP into LTD.

Keywords: GirK channels; LABORAS; amyloid-β1-42 peptide; brain slices; habituation; hippocampus; synaptic plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid beta-Peptides / toxicity
  • Amyloidosis / chemically induced
  • Amyloidosis / metabolism*
  • Animals
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology*
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / metabolism*
  • Hippocampus / drug effects
  • Hippocampus / metabolism*
  • Long-Term Synaptic Depression / drug effects
  • Long-Term Synaptic Depression / physiology*
  • Male
  • Memory Disorders / chemically induced
  • Memory Disorders / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Organ Culture Techniques
  • Peptide Fragments / toxicity
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Receptors, G-Protein-Coupled / metabolism

Substances

  • Amyloid beta-Peptides
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Peptide Fragments
  • Potassium Channels, Inwardly Rectifying
  • Receptors, G-Protein-Coupled
  • amyloid beta-protein (1-42)