Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD
Open accessAbstract
The alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) subtype of glutamate receptors is subject to functionally distinct constitutive and regulated clathrin-dependent endocytosis, contributing to various forms of synaptic plasticity. In HEK293 cells transiently expressing GluR1 or GluR2 mutants containing domain deletions or point mutations in their intracellular carboxyl termini (CT), we found that deletion of the first 10 amino acids (834-843) selectively reduced the rate of constitutive AMPA receptor endocytosis, whereas truncation of the last 15 amino acids of the GluR2 CT, or point mutation of the tyrosine residues in this region, only eliminated the regulated (insulin-stimulated) endocytosis. Moreover, in hippocampal slices, both insulin treatment and low-frequency stimulation (LFS) specifically stimulated tyrosine phosphorylation of the GluR2 subunits of native AMPA receptors, and the enhanced phosphorylation appears necessary for both insulin- and LFS-induced long-term depression of AMPA receptor-mediated excitatory postsynaptic currents. Thus, our results demonstrate that constitutive and regulated AMPA receptor endocytosis requires different sequences within GluR CTs and tyrosine phosphorylation of GluR2 CT is required for the regulated AMPA receptor endocytosis and hence the expression of certain forms of synaptic plasticity.
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Treatment with the 3Y peptide completely blocks LTD and activity-dependent GluA2 endocytosis, while having no effect on basal synaptic transmission.
“Multiple studies have shown both in slice physiology experiments and in vivo that treatment with a short peptide mimicking the tyrosine-rich region of GluA2 (called the 3Y peptide) completely blocks LTD as well as activity-dependent GluA2 endocytosis (Fox et al., 2007, Ahmadian et al., 2004), while having no effect on basal synaptic transmission.”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Ahmadian et al., 2004
The hippocampal-slice results (Figure 7) report that GluR2 3Y significantly reduced LFS-induced LTD, while the slice recordings (Figure 6) report no effect on basal synaptic transmission. The cultured-neuron experiments (Figure 8) show blockade of insulin-stimulated AMPA receptor endocytosis, not endocytosis directly measured after activity-induced LTD. This paper therefore does not establish complete blockade of activity-dependent endocytosis or provide in vivo evidence. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe 'slot hypothesis' offers some explanation for the prominent role of GluA1 in LTP and of GluA2 in LTD, via the rapid activity-dependent mobilization of GluA1-containing receptors onto the cell surface during LTP, and the removal of GluA2 containing receptors from the cell-surface during LTD through interactions with AP2 and/or through interactions involving the GluA2 Y-rich motif.
“Thus the “slot hypothesis” offers some explanation for the prominent role of GluA1 in LTP and of GluA2 in LTD, via the rapid activity-dependent mobilization of GluA1-containing receptors onto the cell surface during LTP, and the removal of GluA2 containing receptors from the cell-surface during LTD through interactions with AP2 and/or through interactions involving the GluA2 Y-rich motif (Ahmadian”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Ahmadian et al., 2004
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- Authors
- Ahmadian, G., Ju, W., Liu, L., Wyszynski, M., Lee, S. H., Dunah, A. W., Taghibiglou, C., Wang, Y., Lu, J., Wong, T. P., Sheng, M., & Wang, Y. T.
- Affiliations
- National Institute of Genetic Engineering and Biotechnology (IR)
- University of British Columbia (CA)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Wang, Yu Tian
- ORCID
- Venue
- The EMBO Journal
- Published
- 2004-02-19
- Volume
- 23
- Issue
- 5
- Pages
- 1040-1050
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC380981
- OpenAlex
- W2141680511
- Cited by
- 296
- References
- 28
- Citations by year
- 2026: 8 · 2025: 2 · 2024: 9 · 2023: 3 · 2022: 7 · 2021: 13 · 2020: 15 · 2019: 14 · 2018: 18 · 2017: 9 · 2016: 14 · 2015: 11 · 2014: 16 · 2013: 25 · 2012: 18
- FWCI
- 5.55
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Heart and Stroke Foundation of Canada
- National Institutes of Health
- Canadian Institutes of Health Research
- National Institute of Neurological Disorders and Stroke (NS 35050, R01NS035050)
- 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
- AMPA receptors, GluR2, tyrosine phosphorylation, receptor internalization, insulin signaling, long-term depression, clathrin-mediated endocytosis, carboxyl terminus, low-frequency stimulation, synaptic plasticity, excitatory postsynaptic currents, hippocampus
- MeSH terms
- Aging, Amino Acid Sequence, Animals, Cells, Cultured, Endocytosis, Hippocampus, Humans, Insulin, Molecular Sequence Data, Mutation, Synaptic Transmission, Neurons, Phosphorylation, Time Factors, Sequence Alignment, Rats, Sprague-Dawley, Receptors, AMPA, Phosphotyrosine, Protein Subunits, Long-Term Synaptic Depression, Rats, In Vitro Techniques
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