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PICK1 regulates AMPA receptor endocytosis via direct interactions with AP2 α-appendage and dynamin

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Fiuza, Maria, Rostosky, Christine M., Parkinson, Gabrielle T., Bygrave, Alexei M., Halemani, Nagaraj, Baptista, Marcio, Milosevic, Ira, Hanley, Jonathan G.·2017·Journal of Cell Biology
DOI 10.1083/jcb.201701034PMC PMC5626541
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Abstract

Clathrin-mediated endocytosis (CME) is used to internalize a diverse range of cargo proteins from the cell surface, often in response to specific signals. In neurons, the rapid endocytosis of GluA2-containing AMPA receptors (AMPARs) in response to NMDA receptor (NMDAR) stimulation causes a reduction in synaptic strength and is the central mechanism for long-term depression, which underlies certain forms of learning. The mechanisms that link NMDAR activation to CME of AMPARs remain elusive. PICK1 is a BAR domain protein required for NMDAR-dependent reductions in surface GluA2; however, the molecular mechanisms involved are unclear. In this study, we show that PICK1 makes direct, NMDAR-dependent interactions with the core endocytic proteins AP2 and dynamin. PICK1–AP2 interactions are required for clustering AMPARs at endocytic zones in dendrites in response to NMDAR stimulation and for consequent AMPAR internalization. We further show that PICK1 stimulates dynamin polymerization. We propose that PICK1 is a cargo-specific endocytic accessory protein required for efficient, activity-dependent AMPAR endocytosis.

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  • PICK1 via its BAR-domain can either promote invagination of the plasma membrane or direct GluA2 to regions of invagination where clathrin-mediated endocytosis occurs.

    “Via its BAR-domain, PICK1 can either promote the invagination of the plasma membrane or direct GluA2 to regions of invagination where clathrin-mediated endocytosis occurs (Xia et al., 2000, Fiuza et al., 2017).”

    From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Fiuza et al., 2017

    The Introduction and Discussion (‘AMPAR clustering at CCPs’; page not provided) support PICK1-dependent targeting of GluA2-containing receptors to clathrin-coated endocytic sites, with AP2 binding at or adjacent to PICK1’s BAR domain. They do not establish that PICK1’s BAR domain itself promotes plasma-membrane invagination; the paper instead describes its interaction with dynamin and stimulation of dynamin polymerization. (LLM, conf=0.86)

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Authors
Fiuza, M., Rostosky, C. M., Parkinson, G. T., Bygrave, A. M., Halemani, N., Baptista, M., Milosevic, I., & Hanley, J. G.
Affiliations
  • Centre for Synaptic Plasticity and School of Biochemistry, University of Bristol, Bristol, England, UK 1
  • Universitätsmedizin Göttingen (DE)
  • University of Bristol (GB)
  • European Neuroscience Institute, University Medical Center Göttingen, Göttingen, Germany 2
Corresponding author
Hanley, Jonathan G.
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2017-08-30
Volume
216
Issue
10
Pages
3323-3338
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
DOI
10.1083/jcb.201701034
PMC
PMC5626541
OpenAlex
W2751422759
Cited by
71
References
6
Citations by year
2026: 6 · 2025: 5 · 2024: 7 · 2023: 5 · 2022: 8 · 2021: 9 · 2020: 15 · 2019: 4 · 2018: 11 · 2017: 1
FWCI
4.15
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of Cell Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Explore Bristol Research (submittedVersion, cc-by)
  • Bristol Research (University of Bristol) (submittedVersion, cc-by)
Funders
Deutsche Forschungsgemeinschaft (MI-1702/1)
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 › Molecular Biology › Receptor Mechanisms and Signaling
Keywords
PICK1, AMPA receptor endocytosis, clathrin-mediated endocytosis, AP-2, dynamin, NMDA receptor signaling, GluA2, BAR domain proteins, synaptic plasticity, long-term depression
MeSH terms
Animals, Carrier Proteins, Cytoskeletal Proteins, Endocytosis, Humans, Nuclear Proteins, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Receptors, AMPA, Adaptor Protein Complex 2, Dynamins, Rats, HEK293 Cells

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