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Cover ArticleArticles, Cellular/Molecular

GluN2B-Containing NMDA Receptors Regulate AMPA Receptor Traffic through Anchoring of the Synaptic Proteasome

Joana S. Ferreira, Jeannette Schmidt, Pedro Rio, Rodolfo Águas, Amanda Rooyakkers, Ka Wan Li, August B. Smit, Ann Marie Craig and Ana Luisa Carvalho
Journal of Neuroscience 3 June 2015, 35 (22) 8462-8479; DOI: https://doi.org/10.1523/JNEUROSCI.3567-14.2015
Joana S. Ferreira
1Center for Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal,
2Department of Life Sciences, University of Coimbra, 3004-517 Coimbra, Portugal,
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Jeannette Schmidt
1Center for Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal,
3Doctoral Program in Experimental Biology and Biomedicine, Center for Neuroscience and Cell Biology and Institute for Interdisciplinary Research, University of Coimbra, 3004-504 Coimbra, Portugal,
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Pedro Rio
1Center for Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal,
2Department of Life Sciences, University of Coimbra, 3004-517 Coimbra, Portugal,
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Rodolfo Águas
1Center for Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal,
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Amanda Rooyakkers
4Brain Research Centre and Department of Psychiatry, University of British Columbia, Vancouver V6T 2B5, Canada, and
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Ka Wan Li
5Center for Neurogenomics and Cognitive Research, Neuroscience Campus Amsterdam, VU University, Delaware Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands
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August B. Smit
5Center for Neurogenomics and Cognitive Research, Neuroscience Campus Amsterdam, VU University, Delaware Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands
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Ann Marie Craig
4Brain Research Centre and Department of Psychiatry, University of British Columbia, Vancouver V6T 2B5, Canada, and
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Ana Luisa Carvalho
1Center for Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal,
2Department of Life Sciences, University of Coimbra, 3004-517 Coimbra, Portugal,
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Abstract

NMDA receptors play a central role in shaping the strength of synaptic connections throughout development and in mediating synaptic plasticity mechanisms that underlie some forms of learning and memory formation in the CNS. In the hippocampus and the neocortex, GluN1 is combined primarily with GluN2A and GluN2B, which are differentially expressed during development and confer distinct molecular and physiological properties to NMDA receptors. The contribution of each subunit to the synaptic traffic of NMDA receptors and therefore to their role during development and in synaptic plasticity is still controversial. We report a critical role for the GluN2B subunit in regulating NMDA receptor synaptic targeting. In the absence of GluN2B, the synaptic levels of AMPA receptors are increased and accompanied by decreased constitutive endocytosis of GluA1-AMPA receptor. We used quantitative proteomic analysis to identify changes in the composition of postsynaptic densities from GluN2B−/− mouse primary neuronal cultures and found altered levels of several ubiquitin proteasome system components, in particular decreased levels of proteasome subunits. Enhancing the proteasome activity with a novel proteasome activator restored the synaptic levels of AMPA receptors in GluN2B−/− neurons and their endocytosis, revealing that GluN2B-mediated anchoring of the synaptic proteasome is responsible for fine tuning AMPA receptor synaptic levels under basal conditions.

  • AMPA receptors
  • GluN2B
  • iTRAQ
  • NMDA receptors
  • postsynaptic density
  • proteasome
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The Journal of Neuroscience: 35 (22)
Journal of Neuroscience
Vol. 35, Issue 22
3 Jun 2015
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GluN2B-Containing NMDA Receptors Regulate AMPA Receptor Traffic through Anchoring of the Synaptic Proteasome
Joana S. Ferreira, Jeannette Schmidt, Pedro Rio, Rodolfo Águas, Amanda Rooyakkers, Ka Wan Li, August B. Smit, Ann Marie Craig, Ana Luisa Carvalho
Journal of Neuroscience 3 June 2015, 35 (22) 8462-8479; DOI: 10.1523/JNEUROSCI.3567-14.2015

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GluN2B-Containing NMDA Receptors Regulate AMPA Receptor Traffic through Anchoring of the Synaptic Proteasome
Joana S. Ferreira, Jeannette Schmidt, Pedro Rio, Rodolfo Águas, Amanda Rooyakkers, Ka Wan Li, August B. Smit, Ann Marie Craig, Ana Luisa Carvalho
Journal of Neuroscience 3 June 2015, 35 (22) 8462-8479; DOI: 10.1523/JNEUROSCI.3567-14.2015
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Keywords

  • AMPA receptors
  • GluN2B
  • iTRAQ
  • NMDA receptors
  • postsynaptic density
  • proteasome

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