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Autism-Associated Neuroligin-3 Mutations Commonly Disrupt Tonic Endocannabinoid Signaling

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Földy, Csaba, Malenka, Robert C., Südhof, Thomas C.·2013·Neuron

DOI 10.1016/j.neuron.2013.02.036PMC PMC3663050

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Abstract

Neuroligins are postsynaptic cell-adhesion molecules that interact with presynaptic neurexins. Rare mutations in neuroligins and neurexins predispose to autism, including a neuroligin-3 amino acid substitution (R451C) and a neuroligin-3 deletion. Previous analyses showed that neuroligin-3 R451C-knockin mice exhibit robust synaptic phenotypes but failed to uncover major changes in neuroligin-3 knockout mice, questioning the notion that a common synaptic mechanism mediates autism pathogenesis in patients with these mutations. Here, we used paired recordings in mice carrying these mutations to measure synaptic transmission at GABAergic synapses formed by hippocampal parvalbumin- and cholecystokinin-expressing basket cells onto pyramidal neurons. We demonstrate that in addition to unique gain-of-function effects produced by the neuroligin-3 R451C-knockin but not the neuroligin-3 knockout mutation, both mutations dramatically impaired tonic but not phasic endocannabinoid signaling. Our data thus suggest that neuroligin-3 is specifically required for tonic endocannabinoid signaling, raising the possibility that alterations in endocannabinoid signaling may contribute to autism pathophysiology.

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Authors: Földy, C., Malenka, R. C., & Südhof, T. C.
Affiliations: Stanford Medicine (US)
Howard Hughes Medical Institute (US)
Corresponding author: Földy, Csaba
Südhof, Thomas C.
ORCID: Földy, Csaba
Malenka, Robert C.
Südhof, Thomas C.
Venue: Neuron
Publisher: Elsevier BV
Published: 2013-05
Volume: 78
Issue: 3
Pages: 498-509
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2013.02.036
PMC: PMC3663050
OpenAlex: W2142679888
Cited by: 287
References: 55
Citations by year: 2026: 7 · 2025: 16 · 2024: 12 · 2023: 21 · 2022: 25 · 2021: 23 · 2020: 30 · 2019: 19 · 2018: 20 · 2017: 27 · 2016: 24 · 2015: 32 · 2014: 23 · 2013: 8
FWCI: 14.07
Type: journal article
Language: en
Update notices: erratum (2013-07-10)
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 372 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
Simons Foundation
National Institute of Mental Health (P50MH086403)
National Institute on Drug Abuse (R01DA030379, K99DA034029)
National Institute of Neurological Disorders and Stroke (NS069375, P30NS069375)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
Keywords: neuroligin-3, autism spectrum disorder, GABAergic synapses, basket cells, parvalbumin, cholecystokinin, synaptic transmission, gain-of-function, neurexin, autism pathogenesis
MeSH terms: Animals, Cells, Cultured, Cholecystokinin, Hippocampus, Membrane Proteins, Mice, Transgenic, Mutation, Nerve Tissue Proteins, Synaptic Transmission, Neurons, Parvalbumins, Synapses, Signal Transduction, Cell Adhesion Molecules, Neuronal, Mice, Gene Knock-In Techniques, GABAergic Neurons, Endocannabinoids

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Autism-Associated Neuroligin-3 Mutations Commonly Disrupt Tonic Endocannabinoid Signaling

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