Synaptic plasticity through activation of GluA3-containing AMPA-receptors

  1. Maria C Renner
  2. Eva HH Albers
  3. Nicolas Gutierrez-Castellanos
  4. Niels R Reinders
  5. Aile N van Huijstee
  6. Hui Xiong
  7. Tessa R Lodder
  8. Helmut W Kessels  Is a corresponding author
  1. The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Netherlands

Abstract

Excitatory synaptic transmission is mediated by AMPA-type glutamate receptors (AMPARs). In CA1 pyramidal neurons of the hippocampus two types of AMPARs predominate: those that contain subunits GluA1 and GluA2 (GluA1/2), and those that contain GluA2 and GluA3 (GluA2/3). Whereas subunits GluA1 and GluA2 have been extensively studied, the contribution of GluA3 to synapse physiology has remained unclear. Here we show in mice that GluA2/3s are in a low-conductance state under basal conditions, and although present at synapses they contribute little to synaptic currents. When intracellular cyclic AMP (cAMP) levels rise, GluA2/3 channels shift to a high-conductance state, leading to synaptic potentiation. This cAMP-driven synaptic potentiation requires the activation of both protein kinase A (PKA) and the GTPase Ras, and is induced upon the activation of β-adrenergic receptors. Together, these experiments reveal a novel type of plasticity at CA1 hippocampal synapses that is expressed by the activation of GluA3-containing AMPARs.

Article and author information

Author details

  1. Maria C Renner

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Eva HH Albers

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Nicolas Gutierrez-Castellanos

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Niels R Reinders

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Aile N van Huijstee

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Hui Xiong

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Tessa R Lodder

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Helmut W Kessels

    Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
    For correspondence
    h.kessels@nin.knaw.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1122-745X

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (821.02.016)

  • Helmut W Kessels

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (864.11.014)

  • Helmut W Kessels

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Indira M Raman, Northwestern University, United States

Ethics

Animal experimentation: All experiments were conducted in line with the European guidelines for the care and use of laboratory animals (Council Directive 86/6009/EEC). The experimental protocol was approved by the Animal Experiment Committee of the Royal Netherlands Academy of Arts and Sciences (KNAW).

Version history

  1. Received: January 25, 2017
  2. Accepted: July 31, 2017
  3. Accepted Manuscript published: August 1, 2017 (version 1)
  4. Version of Record published: August 31, 2017 (version 2)

Copyright

© 2017, Renner et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Maria C Renner
  2. Eva HH Albers
  3. Nicolas Gutierrez-Castellanos
  4. Niels R Reinders
  5. Aile N van Huijstee
  6. Hui Xiong
  7. Tessa R Lodder
  8. Helmut W Kessels
(2017)
Synaptic plasticity through activation of GluA3-containing AMPA-receptors
eLife 6:e25462.
https://doi.org/10.7554/eLife.25462

Share this article

https://doi.org/10.7554/eLife.25462

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