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Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders
Open accessAbstract
There is a long-standing paradox that NMDA (N-methyl-D-aspartate) receptors (NMDARs) can both promote neuronal health and kill neurons. Recent studies show that NMDAR-induced responses depend on the receptor location: stimulation of synaptic NMDARs, acting primarily through nuclear Ca(2+) signalling, leads to the build-up of a neuroprotective 'shield', whereas stimulation of extrasynaptic NMDARs promotes cell death. These differences result from the activation of distinct genomic programmes and from opposing actions on intracellular signalling pathways. Perturbations in the balance between synaptic and extrasynaptic NMDAR activity contribute to neuronal dysfunction in acute ischaemia and Huntington's disease, and could be a common theme in the aetiology of neurodegenerative diseases. Neuroprotective therapies should aim to both enhance the effect of synaptic activity and disrupt extrasynaptic NMDAR-dependent death signalling.
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“research suggests that synaptic NMDAR transmission promotes cell survival and that extra-synaptic NMDARs promote cell death through p38MAPK inhibition and activation, respectively [25].”
From Ketamine in neuropsychiatric disorders: an update (2024) · cites this paper as [25]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Augmented release of glutamate from astrocytes has been shown to be decrease brain-derived neurotrophic factor and increase excitotoxicity (Hardingham and Bading, 2010).”
From Inflammation in Fear- and Anxiety-Based Disorders: PTSD, GAD, and Beyond (2017) · cites this paper as Hardingham and Bading, 2010
Experimental — accuracy not yet measuredIn the citing paper
“PI3K/AKT and RAS/ERK signaling pathways also control processes associated with neural excitotoxicity and cell survival [191].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [191]
In the citing paper
“While redox state modulates NMDAR function, activation of synaptic NMDARs strengthens neuronal antioxidant defense mechanisms (Hardingham and Bading, 2010).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Hardingham and Bading, 2010
In the citing paper
“Interestingly, synaptic NMDAR activation boosts GSH, thioredoxin, and peroxiredoxin systems via calcium-mediated signaling involving activation of CREB and inhibition of FOXO (Hardingham and Bading, 2010; Papadia et al., 2008).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Hardingham and Bading, 2010
In the citing paper
“Moreover, GABAergic interneuron-specific deletion of Grin1 has been show to lead to increased ROS levels which are exacerbated by post-weaning social isolation, in association with down-regulation of peroxisome proliferative activated receptor-γ, coactivator 1α (PPARGC1A, also known as PGC-1α), a regulator of mitochondrial energy metabolism and antioxidant defences 78 .”
From Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis (2016) · cites this paper as [78]
In the citing paper
“Both immunohistochemical and electrophysiological studies have confirmed the existence of extra-synaptic NMDARs, which are not located in the post-synaptic density 68, and are primarily comprised of GluN2B-containing heterotetramers 28, 29.”
From Mechanisms of ketamine action as an antidepressant (2018) · cites this paper as [68]
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- Soriano, F. X., Leveille, F., Papadia, S., Bell, K. F. & Hardingham, G. E. Neuronal activity controls the antagonistic balance between PGC-1α and SMRT in regulating antioxidant defences. Antioxid. Redox Signal. (in the press).
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Metadata
- Authors
- Hardingham, G. E., & Bading, H.
- Affiliations
- University of Edinburgh (GB)
- Heidelberg University (DE)
- Corresponding author
- Hardingham, Giles E.
- Bading, Hilmar
- Venue
- Nature Reviews Neuroscience
- Published
- 2010-09-15
- Volume
- 11
- Issue
- 10
- Pages
- 682-696
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- PMC
- PMC2948541
- OpenAlex
- W1966556202
- Cited by
- 1,644
- References
- 167
- Citations by year
- 2026: 83 · 2025: 109 · 2024: 100 · 2023: 111 · 2022: 93 · 2021: 125 · 2020: 112 · 2019: 92 · 2018: 98 · 2017: 99 · 2016: 117 · 2015: 103 · 2014: 128 · 2013: 111 · 2012: 87
- FWCI
- 7.95
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Alexander von Humboldt-Stiftung
- Wellcome Trust (94018, 087491, 088156)
- Deutsche Forschungsgemeinschaft
- Medical Research Council
- Biotechnology and Biological Sciences Research Council
- 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
- Health Sciences › Medicine › Pharmacology (medical) › Treatment of Major Depression
- Keywords
- NMDA receptor, synaptic NMDA receptors, extrasynaptic NMDA receptors, neuroprotection, neuronal cell death, intracellular signaling, ischemia, Huntington's disease, neurodegenerative diseases, neuroprotective therapy
- MeSH terms
- Animals, Humans, Synapses, Signal Transduction, Gene Expression, Receptors, N-Methyl-D-Aspartate, Cell Death, Oxidative Stress, Neuroprotective Agents, Neurodegenerative Diseases
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