Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans
A hub-and-spoke circuit of neurons connected by gap junctions controls aggregation behavior and related behavioral responses to oxygen, pheromones, and food in Caenorhabditis elegans. The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-02, Vol.114 (7), p.E1263-E1272 |
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| creator | Jang, Heeun Levy, Sagi Flavell, Steven W. Mende, Fanny Latham, Richard Zimmer, Manuel Bargmann, Cornelia I. |
| description | A hub-and-spoke circuit of neurons connected by gap junctions controls aggregation behavior and related behavioral responses to oxygen, pheromones, and food in Caenorhabditis elegans. The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene unc-9 is required in RMG hub neurons to drive aggregation and related behaviors, indicating that UNC-9–containing gap junctions mediate RMG signaling. To dissect the circuit in detail, we developed methods to inhibit unc-9–based gap junctions with dominant-negative unc-1 transgenes. unc-1(dn) alters a stomatin-like protein that regulates unc-9 electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of unc-1(dn) in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, unc-1(dn) has effects opposite to those of tetanus toxin light chain, separating the roles of ADL electrical and chemical synapses. These results reveal roles of gap junctions in a complex behavior at cellular resolution and provide a tool for similar exploration of other gap junction circuits. |
| doi_str_mv | 10.1073/pnas.1621274114 |
| format | Article |
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The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene unc-9 is required in RMG hub neurons to drive aggregation and related behaviors, indicating that UNC-9–containing gap junctions mediate RMG signaling. To dissect the circuit in detail, we developed methods to inhibit unc-9–based gap junctions with dominant-negative unc-1 transgenes. unc-1(dn) alters a stomatin-like protein that regulates unc-9 electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of unc-1(dn) in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, unc-1(dn) has effects opposite to those of tetanus toxin light chain, separating the roles of ADL electrical and chemical synapses. These results reveal roles of gap junctions in a complex behavior at cellular resolution and provide a tool for similar exploration of other gap junction circuits.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1621274114</identifier><identifier>PMID: 28143932</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animal behavior ; Animals ; Animals, Genetically Modified ; Biological Sciences ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Electrical Synapses - genetics ; Electrical Synapses - metabolism ; Gap Junctions - genetics ; Gap Junctions - metabolism ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Molecules ; Motor Activity - genetics ; Nematodes ; Neurons ; Pheromones ; Pheromones - metabolism ; PNAS Plus ; Proteins ; Sensory Receptor Cells - metabolism ; Signal Transduction - genetics ; Social Behavior</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-02, Vol.114 (7), p.E1263-E1272</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Feb 14, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c476t-fe9ff6dc527e6843bede375b7308a2da6cfec63c0ed6f909975560aca84007da3</citedby><cites>FETCH-LOGICAL-c476t-fe9ff6dc527e6843bede375b7308a2da6cfec63c0ed6f909975560aca84007da3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26479436$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26479436$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53769,53771,57995,58228</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28143932$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jang, Heeun</creatorcontrib><creatorcontrib>Levy, Sagi</creatorcontrib><creatorcontrib>Flavell, Steven W.</creatorcontrib><creatorcontrib>Mende, Fanny</creatorcontrib><creatorcontrib>Latham, Richard</creatorcontrib><creatorcontrib>Zimmer, Manuel</creatorcontrib><creatorcontrib>Bargmann, Cornelia I.</creatorcontrib><title>Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>A hub-and-spoke circuit of neurons connected by gap junctions controls aggregation behavior and related behavioral responses to oxygen, pheromones, and food in Caenorhabditis elegans. The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene unc-9 is required in RMG hub neurons to drive aggregation and related behaviors, indicating that UNC-9–containing gap junctions mediate RMG signaling. To dissect the circuit in detail, we developed methods to inhibit unc-9–based gap junctions with dominant-negative unc-1 transgenes. unc-1(dn) alters a stomatin-like protein that regulates unc-9 electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of unc-1(dn) in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, unc-1(dn) has effects opposite to those of tetanus toxin light chain, separating the roles of ADL electrical and chemical synapses. These results reveal roles of gap junctions in a complex behavior at cellular resolution and provide a tool for similar exploration of other gap junction circuits.</description><subject>Animal behavior</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Biological Sciences</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Electrical Synapses - genetics</subject><subject>Electrical Synapses - metabolism</subject><subject>Gap Junctions - genetics</subject><subject>Gap Junctions - metabolism</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Molecules</subject><subject>Motor Activity - genetics</subject><subject>Nematodes</subject><subject>Neurons</subject><subject>Pheromones</subject><subject>Pheromones - metabolism</subject><subject>PNAS Plus</subject><subject>Proteins</subject><subject>Sensory Receptor Cells - metabolism</subject><subject>Signal Transduction - genetics</subject><subject>Social Behavior</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqN0TtvFDEUBWALgcgSqKlAlmhoJrl-jB8NElqeUiQaqC2v586uV7P2Ynsi8e-ZsCEBKioX5_OVfQ8hzxlcMNDi8ph8vWCKM64lY_IBWTGwrFPSwkOyAuC6M5LLM_Kk1j0A2N7AY3LGDZPCCr4iw7tYK4YWc6J5pAnnkpOf6NYf6X5OpyDEEubYKm0732jB7Tz5hrTmEBe6wZ2_jrnQmOjaY8pl5zdDbLFSnHDrU31KHo1-qvjs9jwn3z68_7r-1F19-fh5_faqC1Kr1o1ox1ENoecalZFigwMK3W-0AOP54FUYMSgRAAc1WrBW970CH7yRAHrw4py8Oc09zpsDDgFTK35yxxIPvvxw2Uf3d5Lizm3ztesFB2vsMuD17YCSv89YmzvEGnCafMI8V8eMYVpprfh_UCWUVZarhb76h-7zXJYt_1LWaMMBFnV5UqHkWguOd-9m4G7Kdjdlu_uylxsv__zunf_d7gJenMC-tlzucyW1lUKJn8vzsbk</recordid><startdate>20170214</startdate><enddate>20170214</enddate><creator>Jang, Heeun</creator><creator>Levy, Sagi</creator><creator>Flavell, Steven W.</creator><creator>Mende, Fanny</creator><creator>Latham, Richard</creator><creator>Zimmer, Manuel</creator><creator>Bargmann, Cornelia I.</creator><general>National Academy of Sciences</general><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170214</creationdate><title>Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans</title><author>Jang, Heeun ; 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The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene unc-9 is required in RMG hub neurons to drive aggregation and related behaviors, indicating that UNC-9–containing gap junctions mediate RMG signaling. To dissect the circuit in detail, we developed methods to inhibit unc-9–based gap junctions with dominant-negative unc-1 transgenes. unc-1(dn) alters a stomatin-like protein that regulates unc-9 electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of unc-1(dn) in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, unc-1(dn) has effects opposite to those of tetanus toxin light chain, separating the roles of ADL electrical and chemical synapses. These results reveal roles of gap junctions in a complex behavior at cellular resolution and provide a tool for similar exploration of other gap junction circuits.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28143932</pmid><doi>10.1073/pnas.1621274114</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animal behavior Animals Animals, Genetically Modified Biological Sciences Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Electrical Synapses - genetics Electrical Synapses - metabolism Gap Junctions - genetics Gap Junctions - metabolism Membrane Proteins - genetics Membrane Proteins - metabolism Molecules Motor Activity - genetics Nematodes Neurons Pheromones Pheromones - metabolism PNAS Plus Proteins Sensory Receptor Cells - metabolism Signal Transduction - genetics Social Behavior |
| title | Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans |
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