A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors

Bhattacharyya, Samarjit; Biou, Virginie; Xu, Weifeng; Schlüter, Oliver; Malenka, Robert C

doi:10.1038/nn.2249

Cited by 185Neuroscience and Neuropharmacology ResearchCellular transport and secretionGenetics and Neurodevelopmental Disorders

A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors

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Bhattacharyya, Samarjit, Biou, Virginie, Xu, Weifeng, Schlüter, Oliver, Malenka, Robert C·2009·Nature Neuroscience

DOI 10.1038/nn.2249PMC PMC2694745

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Abstract

The endocytosis of AMPA receptors (AMPARs) underlies several forms of synaptic plasticity, including NMDA receptor (NMDAR)-dependent long-term depression (LTD), but the molecular mechanisms responsible for this trafficking remain unknown. We found that PSD-95, a major postsynaptic density protein, is important for NMDAR-triggered endocytosis of synaptic AMPARs in rat neuron cultures because of its binding to A kinase-anchoring protein 150 (AKAP150), a scaffold for specific protein kinases and phosphatases. Knockdown of PSD-95 with shRNA blocked NMDAR-triggered, but not constitutive or mGluR-triggered, endocytosis of AMPARs. Deletion of PSD-95's Src homology 3 and guanylate kinase-like domains, as well as a point mutation (L460P), both of which inhibit binding of PSD-95 to AKAP150, also blocked NMDAR-triggered AMPAR endocytosis. Furthermore, expression of a mutant AKAP150 that does not bind calcineurin inhibited this NMDAR-triggered trafficking event. Our results suggest that PSD-95's interaction with AKAP150 is critical for NMDAR-triggered AMPAR endocytosis and LTD, possibly because these scaffolds position calcineurin in the appropriate subsynaptic domain.

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The findings are in agreement with previous studies in culture preparations that implicated AKAP79/150-CaN anchoring in regulation of AMPAR activity and endocytosis underlying LTD.
“Our findings are also in agreement with previous studies in culture preparations that implicated AKAP79/150-CaN anchoring in regulation of AMPAR activity and endocytosis underlying LTD”
From AKAP150-Anchored Calcineurin Regulates Synaptic Plasticity by Limiting Synaptic Incorporation of Ca2+-Permeable AMPA Receptors (2012) · cites this paper as Bhattacharyya et al., 2009
A previous overexpression study in cultured rat neurons found that an AKAP150 mutant with a larger deletion surrounding the CaN anchoring site moved from spines with 100 μM NMDA treatment.
“a previous overexpression study in cultured rat neurons found that an AKAP150 mutant with a larger deletion surrounding the CaN anchoring site moved from spines with 100 μM NMDA treatment”
From AKAP150-Anchored Calcineurin Regulates Synaptic Plasticity by Limiting Synaptic Incorporation of Ca2+-Permeable AMPA Receptors (2012) · cites this paper as Bhattacharyya et al., 2009

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“Consistent with this idea, a previous overexpression study in cultured rat neurons found that an AKAP150 mutant with a larger deletion surrounding the CaN anchoring site moved from spines with 100 M NMDA treatment (Bhattacharyya et al., 2009).”
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Authors: Bhattacharyya, S., Biou, V., Xu, W., Schlüter, O., & Malenka, R. C.
Affiliations: Stanford Medicine (US)
European Neuroscience Institute Göttingen (DE)
Corresponding author: Malenka, Robert C
ORCID: Bhattacharyya, Samarjit
Xu, Weifeng
Schlüter, Oliver
Malenka, Robert C
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2009-01-25
Volume: 12
Issue: 2
Pages: 172-181
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn.2249
PMC: PMC2694745
OpenAlex: W2082119586
Cited by: 185
References: 49
Citations by year: 2026: 3 · 2025: 3 · 2024: 9 · 2023: 9 · 2022: 9 · 2021: 8 · 2020: 8 · 2019: 4 · 2018: 9 · 2017: 8 · 2016: 8 · 2015: 12 · 2014: 14 · 2013: 16 · 2012: 21
FWCI: 9.01
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute of Mental Health (R37MH063394, R01MH063394, K99MH080310, MH080310, MH63394)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: PSD-95, AKAP150, AMPA receptor endocytosis, NMDA receptor, long-term depression, synaptic plasticity, calcineurin, postsynaptic density, protein kinase anchoring, metabotropic glutamate receptors, Src homology 3 domain
MeSH terms: Disks Large Homolog 4 Protein, Animals, Cells, Cultured, Endocytosis, Hippocampus, Membrane Proteins, Neuronal Plasticity, Neurons, Synapses, Receptors, N-Methyl-D-Aspartate, Mutagenesis, Rats, Sprague-Dawley, Protein Structure, Tertiary, Receptors, AMPA, src Homology Domains, Calcineurin, Protein Transport, Long-Term Synaptic Depression, Intracellular Signaling Peptides and Proteins, Rats, A Kinase Anchor Proteins

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A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors

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