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AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation
Open accessAbstract
The exocytosis of AMPA receptors is a key step in long-term potentiation (LTP), yet the timing and location of exocytosis and the signaling pathways involved in exocytosis during synaptic plasticity are not fully understood. Here we combine two-photon uncaging with two-photon imaging of a fluorescent label of surface AMPA receptors to monitor individual AMPA receptor exocytosis events near spines undergoing LTP. AMPA receptors that reached the stimulated spine came from a combination of preexisting surface receptors (70–90%) and newly exocytosed receptors (10–30%). We observed exocytosis in both the dendrite and spine under basal conditions. The rate of AMPA receptor exocytosis increased ∼5-fold during LTP induction and decayed to the basal level within ∼1 min, both in the stimulated spine and in the dendrite within ∼3 μm of the stimulated spine. AMPA receptors inserted in the spine were trapped in the spine in an activity-dependent manner. The activity-dependent exocytosis required the Ras-ERK pathway, but not CaMKII. Thus, diffusive Ras-ERK signaling presumably serves as an important means for signaling from synapses to dendritic shafts to recruit AMPA receptors into synapses during LTP.
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“while Rho signaling leads to local AMPA receptor integration in the dendrite (Patterson et al., 2010)”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Patterson et al., 2010
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“Numerous studies have shown that blocking postsynaptic exocytosis by a variety of means blocks LTP/sLTP (195, 249, 250, 332–338).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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“Fourth, in most cases the AMPARs are inserted via exocytosis into the dendritic shaft, some distance from the synapse (220, 249, 250, 337).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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“These synapses contain AMPARs, but LTP-inducing stimuli cause a rapid addition of AMPARs to the synapse (246–250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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“By tagging AMPARs with a pH-sensitive tag (SEP-GluA1), the insertion of AMPARs into the surface membrane can be directly visualized during LTP-inducing protocols (249, 250, 335, 337, 338, 340).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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“Sixth, whereas the recovery from bleaching spine SEP-GluA1 following glutamate uncaging shows a modest dependence on CaMKII, single SEP-GluA1 exocytotic events during glutamate uncaging appear to be independent of CaMKII (250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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“Fifth, a comparison of the synaptic accumulation of SEP-GluA1 by glutamate uncaging, with and without prior bleaching of surface receptors, indicates that much of the accumulation is due to lateral diffusion and not exocytotic insertion of receptors (250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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“but, as discussed, CaMKII appears not to be required for AMPAR exocytotic events (250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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Metadata
- Authors
- Patterson, M. A., Szatmari, E. M., & Yasuda, R.
- Affiliations
- Duke Medical Center (US)
- Department of Neurobiology and
- Howard Hughes Medical Institute (US)
- Corresponding author
- Yasuda, Ryohei
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-08-23
- Volume
- 107
- Issue
- 36
- Pages
- 15951-15956
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2936631
- OpenAlex
- W2014868528
- Cited by
- 259
- References
- 37
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 12 · 2023: 16 · 2022: 11 · 2021: 19 · 2020: 20 · 2019: 11 · 2018: 22 · 2017: 17 · 2016: 14 · 2015: 14 · 2014: 21 · 2013: 22 · 2012: 21
- FWCI
- 7.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Alzheimer's Association
- National Institute of Mental Health (R01MH080047)
- National Institute on Drug Abuse (R01DA027807)
- National Institute of Neurological Disorders and Stroke (R01NS068410)
- 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 › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- long-term potentiation, dendritic spines, Ras/ERK signaling, CaMKII, synaptic plasticity, two-photon uncaging, two-photon imaging
- MeSH terms
- Animals, Exocytosis, Fluorescent Dyes, Kinetics, Long-Term Potentiation, Receptors, AMPA, ras Proteins, Extracellular Signal-Regulated MAP Kinases, Rats
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