Pathogenic mechanism of an autism-associated neuroligin mutation involves altered AMPA-receptor trafficking
Open accessAbstract
Neuroligins are postsynaptic cell-adhesion molecules that bind to presynaptic neurexins. Although the general synaptic role of neuroligins is undisputed, their specific functions at a synapse remain unclear, even controversial. Moreover, many neuroligin gene mutations were associated with autism, but the pathophysiological relevance of these mutations is often unknown, and their mechanisms of action uninvestigated. Here, we examine the synaptic effects of an autism-associated neuroligin-4 substitution (called R704C), which mutates a cytoplasmic arginine residue that is conserved in all neuroligins. We show that the R704C mutation, when introduced into neuroligin-3, enhances the interaction between neuroligin-3 and AMPA receptors, increases AMPA-receptor internalization and decreases postsynaptic AMPA-receptor levels. When introduced into neuroligin-4, conversely, the R704C mutation unexpectedly elevated AMPA-receptor-mediated synaptic responses. These results suggest a general functional link between neuroligins and AMPA receptors, indicate that both neuroligin-3 and -4 act at excitatory synapses but perform surprisingly distinct functions, and demonstrate that the R704C mutation significantly impairs the normal function of neuroligin-4, thereby validating its pathogenicity.
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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 [62]
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- Authors
- Chanda, S., Aoto, J., Lee, S.-J., Wernig, M., & Südhof, T. C.
- Affiliations
- Howard Hughes Medical Institute (US)
- Stanford Medicine (US)
- Corresponding author
- Südhof, T C
- Venue
- Molecular Psychiatry
- Published
- 2015-03-17
- Volume
- 21
- Issue
- 2
- Pages
- 169-177
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC4573762
- OpenAlex
- W2082967233
- Cited by
- 60
- References
- 31
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2023: 5 · 2022: 6 · 2021: 3 · 2020: 8 · 2019: 4 · 2018: 5 · 2017: 10 · 2016: 7 · 2015: 5
- FWCI
- 4.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- New York Stem Cell Foundation
- National Institutes of Health
- National Institute of Mental Health (MH-092931, R01MH092931, MH103531-01, R00MH103531, R37MH052804, K99MH103531)
- 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
- neuroligins, neuroligin 4, neuroligin-3, autism spectrum disorder, AMPA receptor trafficking, receptor internalization, postsynaptic receptors, excitatory synapses, neurexin, adhesion molecules, synaptic function
- MeSH terms
- Animals, Autistic Disorder, Hippocampus, Membrane Proteins, Mice, Inbred Strains, Mutation, Nerve Tissue Proteins, Synaptic Transmission, Neurons, Olfactory Bulb, Synapses, Cell Adhesion Molecules, Neuronal, Receptors, AMPA, alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid, Cell Culture Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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