Canonical versus non-canonical transsynaptic signaling of neuroligin 3 tunes development of sociality in mice
Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclea...
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| Published in | Nature communications Vol. 12; no. 1; pp. 1848 - 15 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
23.03.2021
Nature Publishing Group Nature Portfolio |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2041-1723 2041-1723 |
| DOI | 10.1038/s41467-021-22059-6 |
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| Abstract | Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the
Nlgn3
R451C autism model. At neuronal level, the autism-related
Nlgn3
R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality.
Mutations of Neuroligin 3 (NLGN3) have been associated with autism spectrum disorder (ASD). Here, the authors identify a previously undescribed interaction between NLGN3 and a splice variant of protein tyrosine phosphatase δ (PTP δ) and its role in development of social behaviour in mice. |
|---|---|
| AbstractList | Mutations of Neuroligin 3 (NLGN3) have been associated with autism spectrum disorder (ASD). Here, the authors identify a previously undescribed interaction between NLGN3 and a splice variant of protein tyrosine phosphatase δ (PTP δ) and its role in development of social behaviour in mice. Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the Nlgn3 R451C autism model. At neuronal level, the autism-related Nlgn3 R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality. Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the Nlgn3 R451C autism model. At neuronal level, the autism-related Nlgn3 R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality.Mutations of Neuroligin 3 (NLGN3) have been associated with autism spectrum disorder (ASD). Here, the authors identify a previously undescribed interaction between NLGN3 and a splice variant of protein tyrosine phosphatase δ (PTP δ) and its role in development of social behaviour in mice. Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the Nlgn3 R451C autism model. At neuronal level, the autism-related Nlgn3 R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality. Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the Nlgn3 R451C autism model. At neuronal level, the autism-related Nlgn3 R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality. Mutations of Neuroligin 3 (NLGN3) have been associated with autism spectrum disorder (ASD). Here, the authors identify a previously undescribed interaction between NLGN3 and a splice variant of protein tyrosine phosphatase δ (PTP δ) and its role in development of social behaviour in mice. Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the Nlgn3 R451C autism model. At neuronal level, the autism-related Nlgn3 R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality.Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum disorder (ASD) development of sociality can be impaired. However, the molecular mechanism underlying NLGN3-mediated social development is unclear. Here, we identify non-canonical interactions between NLGN3 and protein tyrosine phosphatase δ (PTPδ) splice variants, competing with NRXN binding. NLGN3-PTPδ complex structure revealed a splicing-dependent interaction mode and competition mechanism between PTPδ and NRXNs. Mice carrying a NLGN3 mutation that selectively impairs NLGN3-NRXN interaction show increased sociability, whereas mice where the NLGN3-PTPδ interaction is impaired exhibit impaired social behavior and enhanced motor learning, with imbalance in excitatory/inhibitory synaptic protein expressions, as reported in the Nlgn3 R451C autism model. At neuronal level, the autism-related Nlgn3 R451C mutation causes selective impairment in the non-canonical pathway. Our findings suggest that canonical and non-canonical NLGN3 pathways compete and regulate the development of sociality. |
| ArticleNumber | 1848 |
| Author | Fukata, Yuko Nakashima, Shogo Shiroshima, Tomoko Maenaka, Katsumi Shimada, Takashi Tabuchi, Katsuhiko Fukata, Masaki Matsumoto, Jumpei Kim, Juhyon Nishijo, Hisao Yoshida, Tomoyuki Uemura, Takeshi Maeda, Asami Mishina, Masayoshi Okabe, Shigeo Mori, Hisashi Yamagata, Atsushi Imai, Ayako Tanaka, Shinji Azechi, Kenji Osaka, Fumina Izumi, Hironori Fukai, Shuya Takao, Keizo Iwasawa-Okamoto, Shiho Saitoh, Takashi |
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surname: Nakashima fullname: Nakashima, Shogo organization: Department of System Emotional Science, Faculty of Medicine, University of Toyama – sequence: 7 givenname: Tomoko surname: Shiroshima fullname: Shiroshima, Tomoko organization: Department of Anatomy, Kitasato University School of Medicine – sequence: 8 givenname: Asami surname: Maeda fullname: Maeda, Asami organization: Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine – sequence: 9 givenname: Shiho surname: Iwasawa-Okamoto fullname: Iwasawa-Okamoto, Shiho organization: Department of Molecular Neuroscience, Faculty of Medicine, University of Toyama – sequence: 10 givenname: Kenji surname: Azechi fullname: Azechi, Kenji organization: Department of Molecular Neuroscience, Faculty of Medicine, University of Toyama – sequence: 11 givenname: Fumina surname: Osaka fullname: Osaka, Fumina organization: Center for Research and Education on Drug Discovery, Faculty of Pharmaceutical Sciences, 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Center, University of Toyama – sequence: 20 givenname: Shinji surname: Tanaka fullname: Tanaka, Shinji organization: Department of Cellular Neurobiology, Graduate School of Medicine, The University of Tokyo – sequence: 21 givenname: Shigeo orcidid: 0000-0003-1216-8890 surname: Okabe fullname: Okabe, Shigeo organization: Department of Cellular Neurobiology, Graduate School of Medicine, The University of Tokyo – sequence: 22 givenname: Katsuhiko orcidid: 0000-0002-1673-4637 surname: Tabuchi fullname: Tabuchi, Katsuhiko organization: JST PRESTO, Department of Molecular and Cellular Physiology, Institute of Medicine, Academic Assembly, Shinshu University, Institute for Biomedical Sciences, Interdisciplinary Cluster for Cutting Edge Research, Shinshu University – sequence: 23 givenname: Takeshi orcidid: 0000-0001-6000-4618 surname: Uemura fullname: Uemura, Takeshi organization: Institute for Biomedical Sciences, Interdisciplinary Cluster for Cutting Edge Research, Shinshu University, Division of Gene Research, Research Center for Supports to Advanced Science, Shinshu University – sequence: 24 givenname: Masayoshi surname: Mishina fullname: Mishina, Masayoshi organization: Brain Science Laboratory, Research Organization of Science and Technology, Ritsumeikan University – sequence: 25 givenname: Hisashi orcidid: 0000-0001-9743-2456 surname: Mori fullname: Mori, Hisashi organization: Department of Molecular Neuroscience, Faculty of Medicine, University of Toyama, Research Center for Idling Brain Science, University of Toyama – sequence: 26 givenname: Shuya orcidid: 0000-0002-1241-1443 surname: Fukai fullname: Fukai, Shuya email: fukai@kuchem.kyoto-u.ac.jp organization: Department of Chemistry, Graduate School of Science, Kyoto University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33758193$$D View this record in MEDLINE/PubMed |
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| Snippet | Neuroligin 3 (NLGN3) and neurexins (NRXNs) constitute a canonical transsynaptic cell-adhesion pair, which has been implicated in autism. In autism spectrum... Mutations of Neuroligin 3 (NLGN3) have been associated with autism spectrum disorder (ASD). Here, the authors identify a previously undescribed interaction... |
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| SubjectTerms | 13 13/106 631/378/2591 631/378/3919 631/80/304 64 64/60 82/83 Alternative splicing Amino Acid Sequence Animals Autism Autism Spectrum Disorder - genetics Autism Spectrum Disorder - metabolism Behavior Rating Scale Calcium-Binding Proteins - chemistry Calcium-Binding Proteins - genetics Calcium-Binding Proteins - metabolism Cell adhesion Cell Adhesion Molecules, Neuronal - chemistry Cell Adhesion Molecules, Neuronal - genetics Cell Adhesion Molecules, Neuronal - metabolism Disease Models, Animal Female HEK293 Cells Humanities and Social Sciences Humans Male Membrane Proteins - chemistry Membrane Proteins - genetics Membrane Proteins - metabolism Mice Mice, Knockout Mice, Transgenic Motor skill learning multidisciplinary Mutation Nerve Tissue Proteins - chemistry Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Neural Cell Adhesion Molecules - chemistry Neural Cell Adhesion Molecules - genetics Neural Cell Adhesion Molecules - metabolism Neurons - metabolism Phosphatase Protein Domains Protein Splicing Protein-tyrosine-phosphatase Proteins Receptor-Like Protein Tyrosine Phosphatases, Class 2 - chemistry Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics Receptor-Like Protein Tyrosine Phosphatases, Class 2 - metabolism Recombinant Proteins Science Science (multidisciplinary) Signal Transduction - genetics Signal Transduction - physiology Social Behavior Splicing Synapses - genetics Tyrosine |
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| Title | Canonical versus non-canonical transsynaptic signaling of neuroligin 3 tunes development of sociality in mice |
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