Subunit-Specific NMDA Receptor Trafficking to Synapses

Barria, Andres; Malinow, Roberto

doi:10.1016/s0896-6273(02)00776-6

Cited by 516Neuroscience and Neuropharmacology ResearchAmino Acid Enzymes and MetabolismReceptor Mechanisms and Signaling

Subunit-Specific NMDA Receptor Trafficking to Synapses

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Barria, Andres, Malinow, Roberto·2002·Neuron

DOI 10.1016/s0896-6273(02)00776-6

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Abstract

To elucidate mechanisms controlling the number and subunit composition of synaptic NMDA-Rs in hippocampal slice neurons, the NR1, NR2A, and NR2B subunits were optically and electrophysiologically tagged. The NR2 subunit directs delivery of receptors to synapses with different rules controlling NR2A and NR2B. Synaptic incorporation of NR2B-containing receptors is not limited by synaptic transmission nor enhanced by increased subunit expression. NR2A-containing receptors whose expression normally increases with age replace synaptic NR2B-containing receptors. Replacement is enhanced by increased NR2A expression and requires synaptic activity. Surprisingly, spontaneously released transmitter acting on synaptic NMDA-Rs is sufficient for replacement and reduces NMDA-R responses. Thus, as with AMPA-Rs, synaptic trafficking of NMDA-Rs is tightly regulated and has subunit-specific rules with functionally important consequences.

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Reduced spontaneous activity of mice defective in the ε4 subunit of the NMDA receptor channel
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γ-Aminobutyric Acid Type B Receptor Splice Variant Proteins GBR1a and GBR1b Are Both Associated with GBR2 in Situ and Display Differential Regional and Subcellular Distribution
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Contrasting Localizations of MALS/LIN-7 PDZ Proteins in Brain and Molecular Compensation in Knockout Mice
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A slow NMDA channel: in search of a role
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Epigenetic Regulations of GABAergic Neurotransmission: Relevance for Neurological Disorders and Epigenetic Therapy
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
LTP and LTD
Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968 · see citing works
Glutamate receptor ion channels.
Mayer, M. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.05.004 · Cited by 163 · see citing works
Glutamate Receptor Ion Channels: Structure, Regulation, and Function
Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., & Dingledine, R. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002451 · Cited by 3,568 · see citing works
NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease
Paoletti, P., Bellone, C., & Zhou, Q. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3504 · Cited by 2,523 · see citing works
PDZ domain proteins of synapses
Kim, E., & Sheng, M. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1517 · Cited by 1,565 · see citing works
NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders
Lau, C. G., & Zukin, R. S. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2153 · Cited by 1,159 · see citing works
Receptor trafficking and synaptic plasticity
Collingridge, G. L., Isaac, J. T. R., & Wang, Y. T. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1556 · Cited by 1,046 · see citing works
Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice
Welch, J. M., Lu, J., Rodriguiz, R. M., Trotta, N. C., Peca, J., Ding, J.-D., Feliciano, C., Chen, M., Adams, J. P., Luo, J., et al. (2007) · Nature · doi:10.1038/nature06104 · Cited by 852 · see citing works
Postsynaptic signaling and plasticity mechanisms
Sheng, M., & Kim, M. J. (2002) · Science · doi:10.1126/science.1075333 · Cited by 731 · see citing works
NMDA Receptor Subunit Composition Controls Synaptic Plasticity by Regulating Binding to CaMKII
Barria, A., & Malinow, R. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.034 · Cited by 709 · see citing works
Self-citation
Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686 · see citing works
Subunit Composition of Synaptic AMPA Receptors Revealed by a Single-Cell Genetic Approach
Lu, W., Shi, Y., Jackson, A. C., Bjorgan, K., During, M. J., Sprengel, R., Seeburg, P. H., & Nicoll, R. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.027 · Cited by 660 · see citing works
Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity
Yashiro, K., & Philpot, B. D. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.046 · Cited by 649 · see citing works
Postsynaptic Density 95 controls AMPA Receptor Incorporation during Long-Term Potentiation and Experience-Driven Synaptic Plasticity
Ehrlich, I., & Malinow, R. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4733-03.2004 · Cited by 567 · see citing works
Self-citation
The Role of NMDA Receptors in Alzheimer’s Disease
Liu, J., Chang, L., Song, Y., Li, H., & Wu, Y. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00043 · Cited by 535 · see citing works
Glutamate Receptor Exocytosis and Spine Enlargement during Chemically Induced Long-Term Potentiation
Kopec, C. D., Li, B., Wei, W., Boehm, J., & Malinow, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3918-05.2006 · Cited by 486 · see citing works
Self-citation
CD47 Protects Synapses from Excess Microglia-Mediated Pruning during Development
Lehrman, E. K., Wilton, D. K., Litvina, E. Y., Welsh, C. A., Chang, S. T., Frouin, A., Walker, A. J., Heller, M. D., Umemori, H., Chen, C., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.017 · Cited by 464 · see citing works
Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2
Wayman, G. A., Impey, S., Marks, D., Saneyoshi, T., Grant, W. F., Derkach, V., & Soderling, T. R. (2006) · Neuron · doi:10.1016/j.neuron.2006.05.008 · Cited by 466 · see citing works
A role for synaptic plasticity in the adolescent development of executive function
Selemon, L. D. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.7 · Cited by 439 · see citing works
“With age and activity, NR2A subunits become incorporated into the postsynaptic membrane, replacing NR2B subunits.(116) The resulting increased NR2A/NR2B ratio translates into a higher threshold for induction of LTP and conversely a state that is more favorable for induction of LTD.”
Background
N-Methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease
FAN, M., & Raymond, L. A. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.11.003 · Cited by 410 · see citing works
Abnormal Glutamate Receptor Expression in the Medial Temporal Lobe in Schizophrenia and Mood Disorders
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Receptor Trafficking
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Authors: Barria, A., & Malinow, R.
Affiliations: Cold Spring Harbor Laboratory (US)
Corresponding author: Malinow, Roberto
ORCID: Malinow, Roberto
Venue: Neuron
Publisher: Elsevier BV
Published: 2002-07
Volume: 35
Issue: 2
Pages: 345-353
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/s0896-6273(02)00776-6
OpenAlex: W2030377743
Cited by: 515
References: 151
Citations by year: 2026: 5 · 2025: 14 · 2024: 16 · 2023: 12 · 2022: 14 · 2021: 14 · 2020: 17 · 2019: 22 · 2018: 12 · 2017: 15 · 2016: 26 · 2015: 27 · 2014: 28 · 2013: 23 · 2012: 23
FWCI: 10.46
Type: journal article
Language: en
Open access: bronze
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Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords: NMDA receptor, receptor trafficking, NR2A, NR2B, NR1, subunit composition, hippocampal neurons, spontaneous neurotransmission, receptor subunit expression, synaptic plasticity
MeSH terms: Animals, Animals, Newborn, Cell Compartmentation, Cells, Cultured, Dendrites, Dose-Response Relationship, Drug, Hippocampus, Indicators and Reagents, Luminescent Proteins, Membrane Potentials, Mutation, Synaptic Transmission, Organ Culture Techniques, Recombinant Fusion Proteins, Synapses, Receptors, N-Methyl-D-Aspartate, Pyramidal Cells, Excitatory Amino Acid Antagonists, Protein Transport, Sodium Channel Blockers, Green Fluorescent Proteins

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Subunit-Specific NMDA Receptor Trafficking to Synapses

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