An autism‐associated point mutation in the neuroligin cytoplasmic tail selectively impairs AMPA receptor‐mediated synaptic transmission in hippocampus
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Neuroligins are evolutionarily conserved postsynaptic cell-adhesion molecules that function, at least in part, by forming trans-synaptic complexes with presynaptic neurexins. Different neuroligin isoforms perform diverse functions and exhibit distinct intracellular localizations, but contain similar cytoplasmic sequences whose role remains largely unknown. Here, we analysed the effect of a single amino-acid substitution (R704C) that targets a conserved arginine residue in the cytoplasmic sequence of all neuroligins, and that was associated with autism in neuroligin-4. We introduced the R704C mutation into mouse neuroligin-3 by homologous recombination, and examined its effect on synapses in vitro and in vivo. Electrophysiological and morphological studies revealed that the neuroligin-3 R704C mutation did not significantly alter synapse formation, but dramatically impaired synapse function. Specifically, the R704C mutation caused a major and selective decrease in AMPA receptor-mediated synaptic transmission in pyramidal neurons of the hippocampus, without similarly changing NMDA or GABA receptor-mediated synaptic transmission, and without detectably altering presynaptic neurotransmitter release. Our results suggest that the cytoplasmic tail of neuroligin-3 has a central role in synaptic transmission by modulating the recruitment of AMPA receptors to postsynaptic sites at excitatory synapses.
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Knock-in mice with the ASD-associated missense mutation Nlgn3(R704C) show decreased AMPA receptor-mediated synaptic transmission in the hippocampus, but no alteration in NMDA or GABA-receptor mediated neurotransmission.
“Knock-in mice with another ASD-associated missense mutation, Nlgn3(R704C) displayed a decrease in AMPA receptor-mediated synaptic transmission in the hippocampus, but no alteration in NMDA or GABA (γ-aminobutyric acid)-receptor mediated neurotransmission39.”
From Activity-dependent neuronal signalling and autism spectrum disorder (2013) · cites this paper as [39]
Several neuroligin mutations found in individuals with ASD have been modelled in mice, and these mice show alterations in excitatory or inhibitory neurotransmission.
“Several of the neuroligin mutations found in individuals with ASD have been modelled in mice, and these mice have been shown to have alterations in excitatory or inhibitory neurotransmission.”
From Activity-dependent neuronal signalling and autism spectrum disorder (2013) · cites this paper as [39]
Nlgn3R704C KI mice show decreased AMPA but not NMDA or GABA receptor-mediated hippocampal neurotransmission, possibly due to increased internalization of AMPA receptors.
“Another mouse model mimicking an ASD-related mutation [393], the Nlgn3R704C KI shows decreased α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionic acid (AMPA), but not N-Methyl-D-aspartic acid (NMDA) or GABA, receptor-mediated hippocampal neurotransmission [100], possibly due to increased internalization of AMPA receptors [62].”
From Autism spectrum disorder: neuropathology and animal models (2017) · cites this paper as [100]
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- Authors
- Etherton, M. R., Tabuchi, K., Sharma, M., Ko, J., & Südhof, T. C.
- Affiliations
- Stanford University (US)
- National Institute for Physiological Sciences (JP)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Südhof, Thomas C
- Venue
- The EMBO Journal
- Published
- 2011-06-03
- Volume
- 30
- Issue
- 14
- Pages
- 2908-2919
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC3160244
- OpenAlex
- W2112440629
- Cited by
- 140
- References
- 54
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 6 · 2023: 3 · 2022: 9 · 2021: 5 · 2020: 6 · 2019: 6 · 2018: 14 · 2017: 11 · 2016: 10 · 2015: 17 · 2014: 12 · 2013: 21 · 2012: 7
- FWCI
- 5.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Simons Foundation
- National Institute of Mental Health (MH052804, R37MH052804)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Keywords
- neuroligin-3, neuroligin 4, autism spectrum disorder, cytoplasmic tail, AMPA receptors, synaptic transmission, hippocampus, pyramidal neurons, neurexin, excitatory synapses
- MeSH terms
- Amino Acid Sequence, Animals, Autistic Disorder, Carrier Proteins, Cells, Cultured, Chlorocebus aethiops, Cytoplasm, Electrophysiology, Female, Hippocampus, Humans, Male, Membrane Proteins, Molecular Sequence Data, Nerve Tissue Proteins, Synaptic Transmission, Neurons, Recombination, Genetic, Synapses, Cell Adhesion Molecules, Neuronal, Point Mutation, Sequence Homology, Amino Acid, Receptors, AMPA, Mice, Knockout, COS Cells, Amino Acid Substitution, Mice
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