Cited by 985Neuroscience and Neuropharmacology ResearchNeuroinflammation and Neurodegeneration MechanismsReceptor Mechanisms and Signaling

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Differential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-α

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Stellwagen, David, Beattie, Eric C., Seo, Jae Y., Malenka, Robert C.·2005·The Journal of Neuroscience

DOI 10.1523/jneurosci.4486-04.2005PMC PMC6725093

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Abstract

The proinflammatory cytokine tumor necrosis factor-α (TNFα) causes a rapid exocytosis of AMPA receptors in hippocampal pyramidal cells and is constitutively required for the maintenance of normal surface expression of AMPA receptors. Here we demonstrate that TNFα acts on neuronal TNFR1 receptors to preferentially exocytose glutamate receptor 2-lacking AMPA receptors through a phosphatidylinositol 3 kinase-dependent process. This increases excitatory synaptic strength while changing the molecular stoichiometry of synaptic AMPA receptors. Conversely, TNFα causes an endocytosis of GABA A receptors, resulting in fewer surface GABA A receptors and a decrease in inhibitory synaptic strength. These results suggest that TNFα can regulate neuronal circuit homeostasis in a manner that may exacerbate excitotoxic damage resulting from neuronal insults.

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The Glutamate Receptor Ion Channels
Dingledine, R., Borges, K., Bowie, D., & Traynelis, S. F. (1999) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01394-2 · Cited by 3,554 · cited 9×
“These new synaptic AMPARs are likely replaced over time by GluR2-containing receptors, because HPP-spermine had no effect on mEPSCs recorded from control neurons despite the finding that constitutive TNF release is necessary to maintain normal levels of surface AMPARs.”
BackgroundInfluential
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · cited 2×
“Trafficking of these receptors is thought to underlie, at least in part, both rapid forms of synaptic plasticity and slower homeostatic changes in transmission (Malinow and Malenka, 2002; Turrigiano and Nelson, 2004).”
BackgroundSelf-citation
Homeostatic plasticity in the developing nervous system
Turrigiano, G. G., & Nelson, S. B. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1327 · Cited by 2,485 · cited 9×
“…circuit activity is pharmacologically reduced, excitatory synapses are strengthened and inhibitory synapses weakened (Turrigiano and Nelson, 2004), at least in part through changes in the synaptic surface expression of AMPARs and GABAA receptors (Kilman et al., 2002; Turrigiano and Nelson, 2004).”
BackgroundResultInfluential
Signal transduction by tumor necrosis factor and its relatives.
Baud, V., & Karin, M. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02064-5 · Cited by 1,741 · cited 3×
“TNFR1 initiates signaling through an array of downstream pathways, most known for their roles in gene expression and apoptosis (Pan et al., 1997; Baud and Karin, 2001).”
Background
Control of Synaptic Strength by Glial TNFα
Beattie, E. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., Beattie, M. S., & Malenka, R. C. (2002) · Science · doi:10.1126/science.1067859 · Cited by 1,344 · cited 7×
“Recently, the proinflammatory cytokine tumor necrosis factor- (TNF ) was found to be a novel, gliareleased factor that increases the surface expression of AMPARs (Beattie et al., 2002).”
BackgroundMethodResultInfluentialSelf-citation
CXCR4-activated astrocyte glutamate release via TNFα: amplification by microglia triggers neurotoxicity
Bezzi, P., Domercq, M., Brambilla, L., Galli, R., Schols, D., De Clercq, E., Vescovi, A., Bagetta, G., Kollias, G., Meldolesi, J., et al. (2001) · Nature Neuroscience · doi:10.1038/89490 · Cited by 1,102 · cited 2×
“In contrast, consistent with our previous results (Beattie et al., 2002), a recombinant soluble form of the TNF receptor TNFR1 (sTNFR), which binds endogenous TNF (Bezzi et al., 2001), decreased surface GluR1 staining (10 g/ ml; 72 5%; n 59) (Fig.”
BackgroundResult
Reinsertion or Degradation of AMPA Receptors Determined by Activity-Dependent Endocytic Sorting
Ehlers, M. D. (2000) · Neuron · doi:10.1016/s0896-6273(00)00129-x · Cited by 1,096 · cited 2×
“It is possible that the antibodies to GluR1 might somehow sterically inhibit antibody staining of surface GluR2, and, therefore, we used an alternative technique, biotinylation of surface AMPARs (Ehlers, 2000; Kim and von Zastrow, 2003), to reexamine whether GluR2 surface expression was increased by TNF .”
Method
Glial activation: a driving force for pathological pain
Watkins, L. R., Milligan, E. D., & Maier, S. F. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01854-3 · Cited by 1,091 · cited 1×
“Similarly, the effects of TNF could contribute to the modification of circuit behavior that underlies the hyperalgesia after peripheral nerve damage, a neuropathological state that involves glia-released cytokines, including TNF (Watkins et al., 2001; Milligan et al., 2003).”
Background
Activation of Synaptic NMDA Receptors Induces Membrane Insertion of New AMPA Receptors and LTP in Cultured Hippocampal Neurons
Lu, W.-Y., Man, H., Ju, W. H., Trimble, W. S., MacDonald, J. F., & Wang, Y. T. (2001) · Neuron · doi:10.1016/s0896-6273(01)00194-5 · Cited by 935 · cited 1×
“However, glycine treatment caused an increase in surface expression of both GluR1 and GluR2 (Lu et al., 2001; Man et al., 2003), although we observed a large increase in surface GluR1 with TNF but no significant change in surface GluR2.”
Background
Tumor Necrosis Factor-α: A Mediator of Focal Ischemic Brain Injury
Barone, F. C., Arvin, B., White, R. F., Miller, A., Webb, C. L., Willette, R. N., Lysko, P. G., & Feuerstein, G. Z. (1997) · Stroke · doi:10.1161/01.str.28.6.1233 · Cited by 863 · cited 2×
“…Nagatsu et al., 2000; Perry et al., 2001), and preventing its signaling in vivo can, for example, prevent or reduce neuron loss after cerebral ischemia (Dawson et al., 1996; Barone et al., 1997; Meistrell et al., 1997) and head injury (for review, see Barone et al., 1997; Shohami et al., 1999).”

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Authors: Stellwagen, D., Beattie, E. C., Seo, J. Y., & Malenka, R. C.
Affiliations: Stanford Medicine (US)
California Pacific Medical Center (US)
Corresponding author: Malenka, Robert C.
ORCID: Stellwagen, David
Malenka, Robert C.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2005-03-23
Volume: 25
Issue: 12
Pages: 3219-3228
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.4486-04.2005
PMC: PMC6725093
OpenAlex: W2134209166
Cited by: 985
References: 74
Citations by year: 2026: 44 · 2025: 35 · 2024: 59 · 2023: 54 · 2022: 60 · 2021: 64 · 2020: 61 · 2019: 48 · 2018: 49 · 2017: 41 · 2016: 43 · 2015: 57 · 2014: 45 · 2013: 53 · 2012: 61
FWCI: 11.57
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 184 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (MH63394)
National Institute of Mental Health (F32MH065752, R37MH063394, R01MH063394, MH065752, MH63394)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords: TNF-α, AMPA receptor trafficking, receptor internalization, TNFR1, phosphatidylinositol 3-kinase, excitotoxicity, hippocampal pyramidal neurons, inflammatory cytokines, synaptic homeostasis
MeSH terms: Animals, Animals, Newborn, Antibodies, Cells, Cultured, Dose-Response Relationship, Radiation, Drug Interactions, Electric Stimulation, Enzyme Inhibitors, Hippocampus, Immunohistochemistry, Neural Inhibition, Synaptic Transmission, Neurons, Tumor Necrosis Factor-alpha, Blotting, Western, Gene Expression, Receptors, GABA, Receptors, AMPA, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Biotinylation, Protein Transport, Receptors, Tumor Necrosis Factor, Type I, Rats, In Vitro Techniques

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Differential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-α

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