SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor
Open accessAbstract
At excitatory synapses, the postsynaptic scaffolding protein postsynaptic density 95 (PSD-95) couples NMDA receptors (NMDARs) to the Ras GTPase-activating protein SynGAP. The close association of SynGAP and NMDARs suggests that SynGAP may have an important role in NMDAR-dependent activation of Ras signaling pathways, such as the MAP kinase pathway, and in synaptic plasticity. To explore this issue, we examined long-term potentiation (LTP), p42 MAPK (ERK2) signaling, and spatial learning in mice with a heterozygous null mutation of the SynGAP gene (SynGAP(-/+)). In SynGAP(-/+) mutant mice, the induction of LTP in the hippocampal CA1 region was strongly reduced in the absence of any detectable alteration in basal synaptic transmission and NMDAR-mediated synaptic currents. Although basal levels of activated ERK2 were elevated in hippocampal extracts from SynGAP(-/+) mice, NMDAR stimulation still induced a robust increase in ERK activation in slices from SynGAP(-/+) mice. Thus, although SynGAP may regulate the ERK pathway, its role in LTP most likely involves additional downstream targets. Consistent with this, the amount of potentiation induced by stimulation protocols that induce an ERK-independent form of LTP were also significantly reduced in slices from SynGAP(-/+) mice. An elevation of basal phospho-ERK2 levels and LTP deficits were also observed in SynGAP(-/+)/H-Ras(-)/- double mutants, suggesting that SynGAP may normally regulate Ras isoforms other than H-Ras. A comparison of SynGAP and PSD-95 mutants suggests that PSD-95 couples NMDARs to multiple downstream signaling pathways with very different roles in LTP and learning.
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Adult SynGAP heterozygous knockout mice are reported to have normal synaptic transmission and only modest defects in synaptic plasticity.
“Interestingly, adult SynGAP Heterozygous knockout mice (Hets), which model human SYNGAP1 haploinsufficiency and offer construct validity, are reported to have normal synaptic transmission and only modest defects in synaptic plasticity”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Komiyama et al., 2002
Adult SynGAP heterozygous knockout mice have profound cognitive abnormalities despite lack of pervasive functional synaptic defects.
“Despite the lack of pervasive functional synaptic defects in adulthood, these animals have profound cognitive abnormalities”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Komiyama et al., 2002
These results are consistent with signaling deficits previously reported in adult SynGAP mice.
“These results are consistent with signaling deficits previously reported in adult SynGAP mice (Carlisle et al., 2008; Komiyama et al., 2002).”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Komiyama et al., 2002
The accelerated maturation hypothesis explains why others have failed to detect changes in hippocampal synaptic strength in adult SynGAP heterozygous mice.
“Our proposed “accelerated maturation” hypothesis also explains why others have failed to detect changes in hippocampal synaptic strength in adult SynGAP Het mice (Kim et al., 2003; Komiyama et al., 2002).”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Komiyama et al., 2002
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- Authors
- Komiyama, N. H., Watabe, A. M., Carlisle, H. J., Porter, K., Charlesworth, P., Monti, J., Strathdee, D. J. C., O'Carroll, C. M., Martin, S. J., Morris, R. G. M., O'Dell, T. J., & Grant, S. G. N.
- Affiliations
- University of Edinburgh (GB)
- University of California, Los Angeles (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-11-15
- Volume
- 22
- Issue
- 22
- Pages
- 9721-9732
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6757832
- OpenAlex
- W2105350975
- Cited by
- 382
- References
- 37
- Citations by year
- 2026: 13 · 2025: 21 · 2024: 23 · 2023: 18 · 2022: 17 · 2021: 13 · 2020: 23 · 2019: 20 · 2018: 17 · 2017: 17 · 2016: 15 · 2015: 10 · 2014: 13 · 2013: 8 · 2012: 16
- FWCI
- 5.01
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- Funders
- Wellcome Trust
- National Institute of Mental Health
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- SynGAP, PSD-95, NMDA receptor, ERK signaling, long-term potentiation, synaptic plasticity, spatial learning, Ras GTPase-activating protein, H-Ras, hippocampal CA1, excitatory synapses
- MeSH terms
- Disks Large Homolog 4 Protein, Animals, Electric Stimulation, Fetal Viability, Heterozygote, Hippocampus, Learning, Membrane Proteins, Mice, Mutant Strains, Nerve Tissue Proteins, Synaptic Transmission, Neuronal Plasticity, Neurons, Synapses, Receptors, N-Methyl-D-Aspartate, Long-Term Potentiation, Gene Targeting, Patch-Clamp Techniques, ras Proteins, Excitatory Postsynaptic Potentials, Mitogen-Activated Protein Kinase 1, GTPase-Activating Proteins, MAP Kinase Signaling System, Macromolecular Substances, Intracellular Signaling Peptides and Proteins, Mice, Guanylate Kinases, In Vitro Techniques
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