Chemico-genetic discovery of astrocytic control of inhibition in vivo
Perisynaptic astrocytic processes are an integral part of central nervous system synapses 1 , 2 ; however, the molecular mechanisms that govern astrocyte–synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic ap...
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| Vydáno v: | Nature (London) Ročník 588; číslo 7837; s. 296 - 302 |
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| Hlavní autoři: | , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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London
Nature Publishing Group UK
10.12.2020
Nature Publishing Group |
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| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| On-line přístup: | Získat plný text |
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| Abstract | Perisynaptic astrocytic processes are an integral part of central nervous system synapses
1
,
2
; however, the molecular mechanisms that govern astrocyte–synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte–neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function.
A cell-surface fragment complementation strategy is used to identify the proteome at the junction of astrocytes and synapses in vivo, and shows that NRCAM expressed in astrocytes has a key role in regulating inhibitory synapse function. |
|---|---|
| AbstractList | Perisynaptic astrocytic processes are an integral part of central nervous system synapses1,2; however, the molecular mechanisms that govern astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte-neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function.Perisynaptic astrocytic processes are an integral part of central nervous system synapses1,2; however, the molecular mechanisms that govern astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte-neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function. Perisynaptic astrocytic processes are an integral part of central nervous system synapses.sup.1,2; however, the molecular mechanisms that govern astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte-neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function. Perisynaptic astrocytic processes are an integral part of central nervous system synapses.sup.1,2; however, the molecular mechanisms that govern astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte-neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function. A cell-surface fragment complementation strategy is used to identify the proteome at the junction of astrocytes and synapses in vivo, and shows that NRCAM expressed in astrocytes has a key role in regulating inhibitory synapse function. Perisynaptic astrocytic processes are an integral part of central nervous system synapses 1 , 2 ; however, the molecular mechanisms that govern astrocyte–synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte–neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function. A cell-surface fragment complementation strategy is used to identify the proteome at the junction of astrocytes and synapses in vivo, and shows that NRCAM expressed in astrocytes has a key role in regulating inhibitory synapse function. Perisynaptic astrocytic processes are an integral part of central nervous system synapses ; however, the molecular mechanisms that govern astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte-neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function. Perisynaptic astrocytic processes are an integral part of central nervous system synapses1,2; however, the molecular mechanisms that govern astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we use an in vivo chemico-genetic approach that applies a cell-surface fragment complementation strategy, Split-TurboID, and identify a proteome that is enriched at astrocyte-neuron junctions in vivo, which includes neuronal cell adhesion molecule (NRCAM). We find that NRCAM is expressed in cortical astrocytes, localizes to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NRCAM interacts transcellularly with neuronal NRCAM coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NRCAM reduces numbers of inhibitory synapses without altering glutamatergic synaptic density. Moreover, loss of astrocytic NRCAM markedly decreases inhibitory synaptic function, with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons and reveal how astrocytes control GABAergic synapse formation and function. Perisynaptic astrocyte processes are an integral part of central nervous system synapses1,2; however, the molecular mechanisms governing astrocyte-synapse adhesions and how astrocyte contacts control synapse formation and function are largely unknown. Here we develop an in vivo chemico-genetic approach, Split-TurboID, that uses a cell surface fragment complementation strategy. We thus identify a proteome enriched at astrocyte-neuron junctions in vivo, including Neuronal Cell Adhesion Molecule (NrCAM). We find that NrCAM is expressed in cortical astrocytes, localized to perisynaptic contacts and is required to restrict neuropil infiltration by astrocytic processes. Furthermore, we show that astrocytic NrCAM transcellularly interacts with neuronal NrCAM that is coupled to gephyrin at inhibitory postsynapses. Depletion of astrocytic NrCAM significantly reduces inhibitory synapse numbers without altering glutamatergic synaptic density. Moreover, loss of astrocytic NrCAM dramatically reduces inhibitory synaptic function with minor effects on excitation. Thus, our results present a proteomic framework for how astrocytes interface with neurons, and reveal how astrocytes control GABAergic synapse formation and function. |
| Audience | Academic |
| Author | Wallace, John T. Purkey, Alicia M. Baldwin, Katherine T. Soderblom, Erik J. Eroglu, Cagla Maness, Patricia F. Soderling, Scott H. Takano, Tetsuya Uezu, Akiyoshi Courtland, Jamie L. Shimogori, Tomomi |
| AuthorAffiliation | 2. Department of Neurobiology, Duke University Medical School, Durham, NC, 27710, USA 5. Departments of Biochemistry and Biophysics and, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599, USA 1. The Department of Cell Biology, Duke University Medical School, Durham, NC 27710, USA 3. Duke Proteomics and Metabolomics Shared Resource and Duke Center for Genomic and Computational Biology, Duke University Medical School, Durham, NC, 27710, USA 4. Molecular Mechanisms of Brain Development, Center for Brain Science (CBS), RIKEN, Saitama 351-0198, Japan |
| AuthorAffiliation_xml | – name: 5. Departments of Biochemistry and Biophysics and, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599, USA – name: 1. The Department of Cell Biology, Duke University Medical School, Durham, NC 27710, USA – name: 3. Duke Proteomics and Metabolomics Shared Resource and Duke Center for Genomic and Computational Biology, Duke University Medical School, Durham, NC, 27710, USA – name: 4. Molecular Mechanisms of Brain Development, Center for Brain Science (CBS), RIKEN, Saitama 351-0198, Japan – name: 2. Department of Neurobiology, Duke University Medical School, Durham, NC, 27710, USA |
| Author_xml | – sequence: 1 givenname: Tetsuya surname: Takano fullname: Takano, Tetsuya email: tetsuya.takano@keio.jp organization: The Department of Cell Biology, Duke University Medical School – sequence: 2 givenname: John T. surname: Wallace fullname: Wallace, John T. organization: The Department of Cell Biology, Duke University Medical School – sequence: 3 givenname: Katherine T. orcidid: 0000-0002-4423-5712 surname: Baldwin fullname: Baldwin, Katherine T. organization: The Department of Cell Biology, Duke University Medical School – sequence: 4 givenname: Alicia M. surname: Purkey fullname: Purkey, Alicia M. organization: The Department of Cell Biology, Duke University Medical School – sequence: 5 givenname: Akiyoshi surname: Uezu fullname: Uezu, Akiyoshi organization: The Department of Cell Biology, Duke University Medical School – sequence: 6 givenname: Jamie L. orcidid: 0000-0001-6846-3552 surname: Courtland fullname: Courtland, Jamie L. organization: Department of Neurobiology, Duke University Medical School – sequence: 7 givenname: Erik J. surname: Soderblom fullname: Soderblom, Erik J. organization: The Department of Cell Biology, Duke University Medical School, Duke Proteomics and Metabolomics Shared Resource and Duke Center for Genomic and Computational Biology, Duke University Medical School – sequence: 8 givenname: Tomomi surname: Shimogori fullname: Shimogori, Tomomi organization: Molecular Mechanisms of Brain Development, Center for Brain Science (CBS), RIKEN – sequence: 9 givenname: Patricia F. surname: Maness fullname: Maness, Patricia F. organization: Department of Biochemistry, University of North Carolina School of Medicine, Department of Biophysics, University of North Carolina School of Medicine – sequence: 10 givenname: Cagla orcidid: 0000-0002-7204-0218 surname: Eroglu fullname: Eroglu, Cagla email: cagla.eroglu@duke.edu organization: The Department of Cell Biology, Duke University Medical School, Department of Neurobiology, Duke University Medical School – sequence: 11 givenname: Scott H. orcidid: 0000-0001-7808-197X surname: Soderling fullname: Soderling, Scott H. email: scott.soderling@duke.edu organization: The Department of Cell Biology, Duke University Medical School, Department of Neurobiology, Duke University Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33177716$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2020 COPYRIGHT 2020 Nature Publishing Group Copyright Nature Publishing Group Dec 10, 2020 |
| Copyright_xml | – notice: The Author(s), under exclusive licence to Springer Nature Limited 2020 – notice: COPYRIGHT 2020 Nature Publishing Group – notice: Copyright Nature Publishing Group Dec 10, 2020 |
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| DOI | 10.1038/s41586-020-2926-0 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 T.T., C.E. and S.H.S. designed the study. T.T., J.T.W., A.P., C.E. and S.H.S wrote the manuscript. T.T., J.T.W., A.U and E.J.S performed in vivo BioID-proteomics analysis. T.T., J.T.W., J.L.C., T.S and P. F. M. produced the constructs. T.T., J.T.W. and K. T. B. performed imaging analysis and the morphological analysis of the astrocytes. A.P performed electrophysiological analysis. T.T. and K. T. B. performed the biological experiments. All authors discussed the results and commented on the manuscript text. Author contributions |
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| Title | Chemico-genetic discovery of astrocytic control of inhibition in vivo |
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