Multiple Mechanisms for the Potentiation of AMPA Receptor-Mediated Transmission by α-Ca2+/Calmodulin-Dependent Protein Kinase II

Poncer, Jean Christophe; Esteban, José A.; Malinow, Roberto

doi:10.1523/jneurosci.22-11-04406.2002

Cited by 177Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsTreatment of Major Depression

Multiple Mechanisms for the Potentiation of AMPA Receptor-Mediated Transmission by α-Ca2+/Calmodulin-Dependent Protein Kinase II

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Poncer, Jean Christophe, Esteban, José A., Malinow, Roberto·2002·The Journal of Neuroscience

DOI 10.1523/jneurosci.22-11-04406.2002PMC PMC6758819

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Abstract

Some forms of activity-dependent synaptic potentiation require the activation of postsynaptic Ca(2+)/calmodulin-dependent protein kinase II (CaMKII). Activation of CaMKII has been shown to phosphorylate the glutamate receptor 1 subunit of the AMPA receptor (AMPAR), thereby affecting some of the properties of the receptor. Here, a recombinant, constitutively active form of alphaCaMKII tagged with the fluorescent marker green fluorescent protein (GFP) [alphaCaMKII(1-290)-enhanced GFP (EGFP)] was expressed in CA1 pyramidal neurons from hippocampal slices. The changes in glutamatergic transmission onto these cells were analyzed. AMPA but not NMDA receptor-mediated EPSCs were specifically potentiated in infected compared with nearby noninfected neurons. This potentiation was associated with a reduction in the proportion of synapses devoid of AMPARs. In addition, expression of alphaCaMKII(1-290)-EGFP increased the quantal size of AMPAR-mediated responses. This effect reflected, at least in part, an increased unitary conductance of the channels underlying the EPSCs. These results reveal that several key features of long-term potentiation of hippocampal glutamatergic synapses are reproduced by the sole activity of alphaCaMKII.

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Expression of active CaMKII or direct delivery into the cell via the recording electrode has repeatedly revealed a roughly two- to threefold enhancement in the AMPAR EPSC but little change in the NMDAR EPSC.
“Expression of active CaMKII (121, 130–132, 209, 210, 212) or direct delivery into the cell via the recording electrode (199) has repeatedly revealed a roughly two- to threefold enhancement in the AMPAR EPSC but little change in the NMDAR EPSC (130–132).”
From Synaptic memory and CaMKII (2023) · cites this paper as [131]
The Results (Fig. 2; page not specified in our copy) report that expression of active αCaMKII increased AMPAR EPSCs to 3.73 ± 0.9 times control, with no significant change in NMDAR EPSCs. This supports the selective enhancement, but the reported mean is above the claimed roughly two- to threefold range. The recording-electrode delivery method is cited separately in the citing sentence, not attributed to this paper. (LLM, conf=0.87)
Experimental — accuracy not yet measured
The number of NMDARs does not change during LTP, since constitutively active CaMKII does not affect the NMDAR EPSC and LTP is expressed primarily on the AMPAR.
“The number of NMDARs does not change, since constitutively active CaMKII does not affect the NMDAR EPSC (130–132) and LTP is expressed primarily on the AMPAR (19).”
From Synaptic memory and CaMKII (2023) · cites this paper as [131]
The Results (Figure 2) report that constitutively active αCaMKII increased AMPAR EPSCs without a significant change in NMDAR EPSCs. The paper does not establish from that measurement that the number of NMDARs remains unchanged during LTP. The separate statement about LTP being expressed primarily on AMPARs is cited to another source in the printed sentence. (LLM, conf=0.85)
Experimental — accuracy not yet measured
NMDAR-dependent LTP is the result of increased AMPAR density in the post-synaptic membrane and/or single channel conductance of the AMPAR.
“The major form of LTP identified in the brain, NMDAR-dependent LTP, is the result of increased AMPAR density in the post-synaptic membrane and/or single channel conductance of the AMPAR (Huganir and Nicoll, 2013, Herring and Nicoll, 2016, Poncer et al., 2002, Benke et al., 1998).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Poncer et al., 2002
The introductory passage and Discussion describe increased synaptic AMPAR number and channel conductance as mechanisms associated with LTP in CA1 hippocampal neurons. The paper does not establish that these mechanisms explain NMDAR-dependent LTP throughout the brain; its own experiments test whether activated CaMKII mimics LTP-related effects in CA1 neurons. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Overexpression of constitutively active CaMKII has little effect on synaptic NMDAR responses.
“overexpression of constitutively active CaMKII has little effect on synaptic NMDAR responses (130–132).”
From Synaptic memory and CaMKII (2023) · cites this paper as [131]
Overexpression of PSD-95 potentiates AMPAR EPSCs and occludes LTP, and the S73D mutant causes similar potentiation.
“since overexpression of PSD-95 on its own potentiates AMPAR EPSCs and occludes LTP (131, 297, 298) and the S73D mutant causes a similar potentiation.”
From Synaptic memory and CaMKII (2023) · cites this paper as [131]
The Results (Figure 2) attribute increased AMPAR EPSCs to expression of activated αCaMKII, not PSD-95. Searches for PSD-95 overexpression, LTP occlusion, and the S73D mutant found no passage addressing those claims in our copy. (LLM, conf=0.76)
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Multiple Mechanisms for the Potentiation of AMPA Receptor- Mediated Transmission by -Ca2 /Calmodulin-Dependent Protein Kinase II
Gálvez-Santisteban, M., Rodriguez-Fraticelli, A., Vergarajaúregui, S., Bañón-Rodríguez, I., Bernascone, I., & Martín‐Belmonte, F. (2002) · DIGITAL.CSIC (Spanish National Research Council (CSIC)) · doi:10.13039/100004412
Multiple Mechanisms for the Potentiation of AMPA Receptor- Mediated Transmission by -Ca2/Calmodulin-Dependent Protein
Ii, K., Poncer, J. C., Esteban, J. A., & Malinow, R. (2015)
Self-citation
Mechanisms of Potentiation by Calcium-Calmodulin Kinase II of Postsynaptic Sensitivity in Rat Hippocampal CA1 Neurons
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Recruitment of Calcium-Permeable AMPA Receptors during Synaptic Potentiation Is Regulated by CaM-Kinase I
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Ca <sup>2+</sup> /calmodulin-kinase II enhances channel conductance of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors
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Authors: Poncer, J. C., Esteban, J. A., & Malinow, R.
Affiliations: Inserm (FR)
Cold Spring Harbor Laboratory (US)
ORCID: Poncer, Jean Christophe
Malinow, Roberto
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2002-06-01
Volume: 22
Issue: 11
Pages: 4406-4411
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.22-11-04406.2002
PMC: PMC6758819
OpenAlex: W1756593109
Cited by: 177
References: 46
Citations by year: 2026: 2 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 4 · 2019: 1 · 2018: 7 · 2017: 3 · 2016: 3 · 2015: 9 · 2014: 10 · 2013: 8 · 2012: 7
FWCI: 5.13
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
Funders: G. Harold and Leila Y. Mathers Foundation
National Institutes of Health
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
Keywords: CaMKIIα, AMPA receptors, synaptic potentiation, long-term potentiation, CA1 pyramidal neurons, hippocampus, glutamatergic synapses, quantal size, single-channel conductance, activity-dependent synaptic plasticity, NMDA receptor
MeSH terms: Animals, Female, Hippocampus, Luminescent Proteins, Male, Synaptic Transmission, Neuronal Plasticity, Recombinant Fusion Proteins, Sindbis Virus, Gene Expression, Long-Term Potentiation, Calcium-Calmodulin-Dependent Protein Kinases, Pyramidal Cells, Receptors, AMPA, Patch-Clamp Techniques, Transgenes, Excitatory Postsynaptic Potentials, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2, In Vitro Techniques

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Multiple Mechanisms for the Potentiation of AMPA Receptor-Mediated Transmission by α-Ca2+/Calmodulin-Dependent Protein Kinase II

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