Structurally defined signaling in neuro‐glia units in the enteric nervous system
Coordination of gastrointestinal function relies on joint efforts of enteric neurons and glia, whose crosstalk is vital for the integration of their activity. To investigate the signaling mechanisms and to delineate the spatial aspects of enteric neuron‐to‐glia communication within enteric ganglia w...
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| Veröffentlicht in: | Glia 2019-06, Vol.67 (6), p.1167-1178 |
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| creator | Boesmans, Werend Hao, Marlene M. Fung, Candice Li, Zhiling Van den Haute, Chris Tack, Jan Pachnis, Vassilis Vanden Berghe, Pieter |
| description | Coordination of gastrointestinal function relies on joint efforts of enteric neurons and glia, whose crosstalk is vital for the integration of their activity. To investigate the signaling mechanisms and to delineate the spatial aspects of enteric neuron‐to‐glia communication within enteric ganglia we developed a method to stimulate single enteric neurons while monitoring the activity of neighboring enteric glial cells. We combined cytosolic calcium uncaging of individual enteric neurons with calcium imaging of enteric glial cells expressing a genetically encoded calcium indicator and demonstrate that enteric neurons signal to enteric glial cells through pannexins using paracrine purinergic pathways. Sparse labeling of enteric neurons and high‐resolution analysis of the structural relation between neuronal cell bodies, varicose release sites and enteric glia uncovered that this form of neuron‐to‐glia communication is contained between the cell body of an enteric neuron and its surrounding enteric glial cells. Our results reveal the spatial and functional foundation of neuro‐glia units as an operational cellular assembly in the enteric nervous system.
Main Points
Enteric neurons release purines to communicate with enteric glial cells in their direct vicinity.
Nerve cell bodies are closely associated with glial cells to form functional neuro‐glia units within ganglia of the enteric nervous system. |
| doi_str_mv | 10.1002/glia.23596 |
| format | Article |
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Main Points
Enteric neurons release purines to communicate with enteric glial cells in their direct vicinity.
Nerve cell bodies are closely associated with glial cells to form functional neuro‐glia units within ganglia of the enteric nervous system.</description><identifier>ISSN: 0894-1491</identifier><identifier>EISSN: 1098-1136</identifier><identifier>DOI: 10.1002/glia.23596</identifier><identifier>PMID: 30730592</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Animals ; Ca2+ imaging ; Ca2+ uncaging ; Calcium ; Calcium imaging ; Cell body ; Cell Communication - physiology ; Cells, Cultured ; Coding ; Crosstalk ; enteric glial cell ; Enteric nervous system ; Enteric Nervous System - chemistry ; Enteric Nervous System - cytology ; Enteric Nervous System - physiology ; enteric neuron ; Female ; Ganglia ; gastrointestinal tract ; Genetic code ; Glial cells ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Nervous system ; Neuroglia - chemistry ; Neuroglia - physiology ; Neuronal-glial interactions ; Neurons ; Neurons - chemistry ; Neurons - physiology ; Paracrine signalling ; Phosphates ; purinergic signaling ; Signal Transduction - physiology ; synaptic</subject><ispartof>Glia, 2019-06, Vol.67 (6), p.1167-1178</ispartof><rights>2019 The Authors. published by Wiley Periodicals, Inc.</rights><rights>2019 The Authors. Glia published by Wiley Periodicals, Inc.</rights><rights>2019. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5146-9d9e04249a63887629367142f3f8d38caa9a5b4c925b831fc1dd7b242a515efc3</citedby><cites>FETCH-LOGICAL-c5146-9d9e04249a63887629367142f3f8d38caa9a5b4c925b831fc1dd7b242a515efc3</cites><orcidid>0000-0002-9701-8252 ; 0000-0002-4277-3664 ; 0000-0001-9733-7686 ; 0000-0002-2426-0451 ; 0000-0002-3206-6704 ; 0000-0002-0009-2094 ; 0000-0002-3888-971X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fglia.23596$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fglia.23596$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30730592$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Boesmans, Werend</creatorcontrib><creatorcontrib>Hao, Marlene M.</creatorcontrib><creatorcontrib>Fung, Candice</creatorcontrib><creatorcontrib>Li, Zhiling</creatorcontrib><creatorcontrib>Van den Haute, Chris</creatorcontrib><creatorcontrib>Tack, Jan</creatorcontrib><creatorcontrib>Pachnis, Vassilis</creatorcontrib><creatorcontrib>Vanden Berghe, Pieter</creatorcontrib><title>Structurally defined signaling in neuro‐glia units in the enteric nervous system</title><title>Glia</title><addtitle>Glia</addtitle><description>Coordination of gastrointestinal function relies on joint efforts of enteric neurons and glia, whose crosstalk is vital for the integration of their activity. To investigate the signaling mechanisms and to delineate the spatial aspects of enteric neuron‐to‐glia communication within enteric ganglia we developed a method to stimulate single enteric neurons while monitoring the activity of neighboring enteric glial cells. We combined cytosolic calcium uncaging of individual enteric neurons with calcium imaging of enteric glial cells expressing a genetically encoded calcium indicator and demonstrate that enteric neurons signal to enteric glial cells through pannexins using paracrine purinergic pathways. Sparse labeling of enteric neurons and high‐resolution analysis of the structural relation between neuronal cell bodies, varicose release sites and enteric glia uncovered that this form of neuron‐to‐glia communication is contained between the cell body of an enteric neuron and its surrounding enteric glial cells. Our results reveal the spatial and functional foundation of neuro‐glia units as an operational cellular assembly in the enteric nervous system.
Main Points
Enteric neurons release purines to communicate with enteric glial cells in their direct vicinity.
Nerve cell bodies are closely associated with glial cells to form functional neuro‐glia units within ganglia of the enteric nervous system.</description><subject>Animals</subject><subject>Ca2+ imaging</subject><subject>Ca2+ uncaging</subject><subject>Calcium</subject><subject>Calcium imaging</subject><subject>Cell body</subject><subject>Cell Communication - physiology</subject><subject>Cells, Cultured</subject><subject>Coding</subject><subject>Crosstalk</subject><subject>enteric glial cell</subject><subject>Enteric nervous system</subject><subject>Enteric Nervous System - chemistry</subject><subject>Enteric Nervous System - cytology</subject><subject>Enteric Nervous System - physiology</subject><subject>enteric neuron</subject><subject>Female</subject><subject>Ganglia</subject><subject>gastrointestinal tract</subject><subject>Genetic code</subject><subject>Glial cells</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Nervous system</subject><subject>Neuroglia - chemistry</subject><subject>Neuroglia - physiology</subject><subject>Neuronal-glial interactions</subject><subject>Neurons</subject><subject>Neurons - chemistry</subject><subject>Neurons - physiology</subject><subject>Paracrine signalling</subject><subject>Phosphates</subject><subject>purinergic signaling</subject><subject>Signal Transduction - physiology</subject><subject>synaptic</subject><issn>0894-1491</issn><issn>1098-1136</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp9kctKxDAUhoMoOo5ufAApuBGhmkuTJhtBxMvAgOBlHdI0nYl0Uk1aZXY-gs_ok5iZjqIuXIWT8_Gf_5wfgD0EjxGE-GRSW3WMCRVsDQwQFDxFiLB1MIBcZCnKBNoC2yE8QohikW-CLQJzAqnAA3B71_pOt51XdT1PSlNZZ8ok2IlTtXWTxLrEmc43H2_vizFJ52wbFr_t1CTGtcZbHQn_0nQhCfPQmtkO2KhUHczu6h2Ch8uL-_PrdHxzNTo_G6eaooylohQGZjgTihHOc4YFYTnKcEUqXhKulRKKFpkWmBacoEqjsswLnGFFETWVJkNw2us-dcXMlDq6iVvIJ29nys9lo6z83XF2KifNi2RUkJywKHC4EvDNc2dCK2c2aFPXypm4jsQYCgYpifAQHPxBH5vOxxstKc6i75xH6qintG9C8Kb6NoOgXEQlFzeUy6givP_T_jf6lU0EUA-82trM_5GSV-PRWS_6CaPboGg</recordid><startdate>201906</startdate><enddate>201906</enddate><creator>Boesmans, Werend</creator><creator>Hao, Marlene M.</creator><creator>Fung, Candice</creator><creator>Li, Zhiling</creator><creator>Van den Haute, Chris</creator><creator>Tack, Jan</creator><creator>Pachnis, Vassilis</creator><creator>Vanden Berghe, Pieter</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9701-8252</orcidid><orcidid>https://orcid.org/0000-0002-4277-3664</orcidid><orcidid>https://orcid.org/0000-0001-9733-7686</orcidid><orcidid>https://orcid.org/0000-0002-2426-0451</orcidid><orcidid>https://orcid.org/0000-0002-3206-6704</orcidid><orcidid>https://orcid.org/0000-0002-0009-2094</orcidid><orcidid>https://orcid.org/0000-0002-3888-971X</orcidid></search><sort><creationdate>201906</creationdate><title>Structurally defined signaling in neuro‐glia units in the enteric nervous system</title><author>Boesmans, Werend ; 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To investigate the signaling mechanisms and to delineate the spatial aspects of enteric neuron‐to‐glia communication within enteric ganglia we developed a method to stimulate single enteric neurons while monitoring the activity of neighboring enteric glial cells. We combined cytosolic calcium uncaging of individual enteric neurons with calcium imaging of enteric glial cells expressing a genetically encoded calcium indicator and demonstrate that enteric neurons signal to enteric glial cells through pannexins using paracrine purinergic pathways. Sparse labeling of enteric neurons and high‐resolution analysis of the structural relation between neuronal cell bodies, varicose release sites and enteric glia uncovered that this form of neuron‐to‐glia communication is contained between the cell body of an enteric neuron and its surrounding enteric glial cells. Our results reveal the spatial and functional foundation of neuro‐glia units as an operational cellular assembly in the enteric nervous system.
Main Points
Enteric neurons release purines to communicate with enteric glial cells in their direct vicinity.
Nerve cell bodies are closely associated with glial cells to form functional neuro‐glia units within ganglia of the enteric nervous system.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>30730592</pmid><doi>10.1002/glia.23596</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-9701-8252</orcidid><orcidid>https://orcid.org/0000-0002-4277-3664</orcidid><orcidid>https://orcid.org/0000-0001-9733-7686</orcidid><orcidid>https://orcid.org/0000-0002-2426-0451</orcidid><orcidid>https://orcid.org/0000-0002-3206-6704</orcidid><orcidid>https://orcid.org/0000-0002-0009-2094</orcidid><orcidid>https://orcid.org/0000-0002-3888-971X</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Glia, 2019-06, Vol.67 (6), p.1167-1178 |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Animals Ca2+ imaging Ca2+ uncaging Calcium Calcium imaging Cell body Cell Communication - physiology Cells, Cultured Coding Crosstalk enteric glial cell Enteric nervous system Enteric Nervous System - chemistry Enteric Nervous System - cytology Enteric Nervous System - physiology enteric neuron Female Ganglia gastrointestinal tract Genetic code Glial cells Male Mice Mice, Inbred C57BL Mice, Transgenic Nervous system Neuroglia - chemistry Neuroglia - physiology Neuronal-glial interactions Neurons Neurons - chemistry Neurons - physiology Paracrine signalling Phosphates purinergic signaling Signal Transduction - physiology synaptic |
| title | Structurally defined signaling in neuro‐glia units in the enteric nervous system |
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