A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans
While depolarization of the neuronal membrane is known to evoke the neurotransmitter release from synaptic vesicles, hyperpolarization is regarded as a resting state of chemical neurotransmission. Here, we report that hyperpolarizing neurons can actively signal neural information by employing undock...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2024-05, Vol.121 (21), p.e2406565121 |
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| creator | Nakayama, Airi Watanabe, Masakatsu Yamashiro, Riku Kuroyanagi, Hiroo Matsuyama, Hironori J Oshima, Atsunori Mori, Ikue Nakano, Shunji |
| description | While depolarization of the neuronal membrane is known to evoke the neurotransmitter release from synaptic vesicles, hyperpolarization is regarded as a resting state of chemical neurotransmission. Here, we report that hyperpolarizing neurons can actively signal neural information by employing undocked hemichannels. We show that UNC-7, a member of the innexin family in
functions as a hemichannel in thermosensory neurons and transmits temperature information from the thermosensory neurons to their postsynaptic interneurons. By monitoring neural activities in freely behaving animals, we find that hyperpolarizing thermosensory neurons inhibit the activity of the interneurons and that UNC-7 hemichannels regulate this process. UNC-7 is required to control thermotaxis behavior and functions independently of synaptic vesicle exocytosis. Our findings suggest that innexin hemichannels mediate neurotransmission from hyperpolarizing neurons in a manner that is distinct from the synaptic transmission, expanding the way of neural circuitry operations. |
| doi_str_mv | 10.1073/pnas.2406565121 |
| format | Article |
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functions as a hemichannel in thermosensory neurons and transmits temperature information from the thermosensory neurons to their postsynaptic interneurons. By monitoring neural activities in freely behaving animals, we find that hyperpolarizing thermosensory neurons inhibit the activity of the interneurons and that UNC-7 hemichannels regulate this process. UNC-7 is required to control thermotaxis behavior and functions independently of synaptic vesicle exocytosis. Our findings suggest that innexin hemichannels mediate neurotransmission from hyperpolarizing neurons in a manner that is distinct from the synaptic transmission, expanding the way of neural circuitry operations.</description><identifier>ISSN: 0027-8424</identifier><identifier>ISSN: 1091-6490</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2406565121</identifier><identifier>PMID: 38753507</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Caenorhabditis elegans ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Circuits ; Connexins - genetics ; Connexins - metabolism ; Depolarization ; Exocytosis ; Hyperpolarization ; Interneurons ; Interneurons - metabolism ; Membrane potential ; Membrane Proteins ; Neural networks ; Neurons ; Neurons - metabolism ; Neurotransmission ; Neurotransmitter release ; Synaptic transmission ; Synaptic Transmission - physiology ; Synaptic vesicles ; Synaptic Vesicles - metabolism ; Taxis Response - physiology ; Thermotaxis</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2024-05, Vol.121 (21), p.e2406565121</ispartof><rights>Copyright National Academy of Sciences May 21, 2024</rights><rights>Copyright © 2024 the Author(s). Published by PNAS. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c376t-242b6abfe38b6539698b1cfb458c7f5b934fe1d907f6665d9dfd8950a2e6d5343</cites><orcidid>0000-0002-9810-2106 ; 0000-0002-6565-9450 ; 0000-0002-5744-197X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11127054/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11127054/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38753507$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nakayama, Airi</creatorcontrib><creatorcontrib>Watanabe, Masakatsu</creatorcontrib><creatorcontrib>Yamashiro, Riku</creatorcontrib><creatorcontrib>Kuroyanagi, Hiroo</creatorcontrib><creatorcontrib>Matsuyama, Hironori J</creatorcontrib><creatorcontrib>Oshima, Atsunori</creatorcontrib><creatorcontrib>Mori, Ikue</creatorcontrib><creatorcontrib>Nakano, Shunji</creatorcontrib><title>A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>While depolarization of the neuronal membrane is known to evoke the neurotransmitter release from synaptic vesicles, hyperpolarization is regarded as a resting state of chemical neurotransmission. Here, we report that hyperpolarizing neurons can actively signal neural information by employing undocked hemichannels. We show that UNC-7, a member of the innexin family in
functions as a hemichannel in thermosensory neurons and transmits temperature information from the thermosensory neurons to their postsynaptic interneurons. By monitoring neural activities in freely behaving animals, we find that hyperpolarizing thermosensory neurons inhibit the activity of the interneurons and that UNC-7 hemichannels regulate this process. UNC-7 is required to control thermotaxis behavior and functions independently of synaptic vesicle exocytosis. Our findings suggest that innexin hemichannels mediate neurotransmission from hyperpolarizing neurons in a manner that is distinct from the synaptic transmission, expanding the way of neural circuitry operations.</description><subject>Animals</subject><subject>Biological Sciences</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Circuits</subject><subject>Connexins - genetics</subject><subject>Connexins - metabolism</subject><subject>Depolarization</subject><subject>Exocytosis</subject><subject>Hyperpolarization</subject><subject>Interneurons</subject><subject>Interneurons - metabolism</subject><subject>Membrane potential</subject><subject>Membrane Proteins</subject><subject>Neural networks</subject><subject>Neurons</subject><subject>Neurons - metabolism</subject><subject>Neurotransmission</subject><subject>Neurotransmitter release</subject><subject>Synaptic transmission</subject><subject>Synaptic Transmission - physiology</subject><subject>Synaptic vesicles</subject><subject>Synaptic Vesicles - metabolism</subject><subject>Taxis Response - physiology</subject><subject>Thermotaxis</subject><issn>0027-8424</issn><issn>1091-6490</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtv1TAQhS1ERS-FNTsUiQ2btONn4hWqrnhJlbqBteUkkxuXxA52UrX8ehxaCu1qNJpvzpzRIeQNhVMKFT-bvU2nTICSSlJGn5EdBU1LJTQ8JzsAVpW1YOKYvEzpCgC0rOEFOeZ1JbmEakduzovhdsY4h9FG98v5Q-FxjcEXEdu4uiUVq-9C-wO7wnmPN84XA06uHWzuxlQsoVii9Wlyy59NO2auD3Gyi8sqGd9b9CEOtunc4lKBIx4y_4oc9XZM-Pq-npDvnz5-238pLy4_f92fX5Qtr9RSMsEaZZseed0oybXSdUPbvhGybqteNpqLHmmnoeqVUrLTXd_VWoJlqDrJBT8hH-5057WZsGvRZ7ujmaObbLw1wTrzeOLdYA7h2lBKWQVyU3h_rxDDzxXTYiaXWhxH6zGsyXCQ-bQC2NB3T9CrsEaf_9soLRTVgmXq7I5qY0gpYv_ghoLZYjVbrOZfrHnj7f9PPPB_c-S_ARVpokA</recordid><startdate>20240521</startdate><enddate>20240521</enddate><creator>Nakayama, Airi</creator><creator>Watanabe, Masakatsu</creator><creator>Yamashiro, Riku</creator><creator>Kuroyanagi, Hiroo</creator><creator>Matsuyama, Hironori J</creator><creator>Oshima, Atsunori</creator><creator>Mori, Ikue</creator><creator>Nakano, Shunji</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><orcidid>https://orcid.org/0000-0002-9810-2106</orcidid><orcidid>https://orcid.org/0000-0002-6565-9450</orcidid><orcidid>https://orcid.org/0000-0002-5744-197X</orcidid></search><sort><creationdate>20240521</creationdate><title>A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans</title><author>Nakayama, Airi ; 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Here, we report that hyperpolarizing neurons can actively signal neural information by employing undocked hemichannels. We show that UNC-7, a member of the innexin family in
functions as a hemichannel in thermosensory neurons and transmits temperature information from the thermosensory neurons to their postsynaptic interneurons. By monitoring neural activities in freely behaving animals, we find that hyperpolarizing thermosensory neurons inhibit the activity of the interneurons and that UNC-7 hemichannels regulate this process. UNC-7 is required to control thermotaxis behavior and functions independently of synaptic vesicle exocytosis. Our findings suggest that innexin hemichannels mediate neurotransmission from hyperpolarizing neurons in a manner that is distinct from the synaptic transmission, expanding the way of neural circuitry operations.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>38753507</pmid><doi>10.1073/pnas.2406565121</doi><orcidid>https://orcid.org/0000-0002-9810-2106</orcidid><orcidid>https://orcid.org/0000-0002-6565-9450</orcidid><orcidid>https://orcid.org/0000-0002-5744-197X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological Sciences Caenorhabditis elegans Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Circuits Connexins - genetics Connexins - metabolism Depolarization Exocytosis Hyperpolarization Interneurons Interneurons - metabolism Membrane potential Membrane Proteins Neural networks Neurons Neurons - metabolism Neurotransmission Neurotransmitter release Synaptic transmission Synaptic Transmission - physiology Synaptic vesicles Synaptic Vesicles - metabolism Taxis Response - physiology Thermotaxis |
| title | A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans |
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