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cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans

Living organisms including bacteria, plants and animals sense ambient temperature so that they can avoid noxious temperature or adapt to new environmental temperature. A nematode C. elegans can sense innocuous temperature, and navigate themselves towards memorize past cultivation temperature (T(c))...

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Autores principales: Aok, Ichiro, Shiota, Makoto, Tsukada, Yuki, Nakano, Shunji, Mori, Ikue
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9725164/
https://www.ncbi.nlm.nih.gov/pubmed/36472979
http://dx.doi.org/10.1371/journal.pone.0278343
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author Aok, Ichiro
Shiota, Makoto
Tsukada, Yuki
Nakano, Shunji
Mori, Ikue
author_facet Aok, Ichiro
Shiota, Makoto
Tsukada, Yuki
Nakano, Shunji
Mori, Ikue
author_sort Aok, Ichiro
collection PubMed
description Living organisms including bacteria, plants and animals sense ambient temperature so that they can avoid noxious temperature or adapt to new environmental temperature. A nematode C. elegans can sense innocuous temperature, and navigate themselves towards memorize past cultivation temperature (T(c)) of their preference. For this thermotaxis, AFD thermosensory neuron is pivotal, which stereotypically responds to warming by increasing intracellular Ca(2+) level in a manner dependent on the remembered past T(c). We aimed to reveal how AFD encodes the information of temperature into neural activities. cGMP synthesis in AFD is crucial for thermosensation in AFD and thermotaxis behavior. Here we characterized the dynamic change of cGMP level in AFD by imaging animals expressing a fluorescence resonance energy transfer (FRET)-based cGMP probe specifically in AFD and found that cGMP dynamically responded to both warming and cooling in a manner dependent on past T(c). Moreover, we characterized mutant animals that lack guanylyl cyclases (GCYs) or phosphodiesterases (PDEs), which synthesize and hydrolyze cGMP, respectively, and uncovered how GCYs and PDEs contribute to cGMP and Ca(2+) dynamics in AFD and to thermotaxis behavior.
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spelling pubmed-97251642022-12-07 cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans Aok, Ichiro Shiota, Makoto Tsukada, Yuki Nakano, Shunji Mori, Ikue PLoS One Research Article Living organisms including bacteria, plants and animals sense ambient temperature so that they can avoid noxious temperature or adapt to new environmental temperature. A nematode C. elegans can sense innocuous temperature, and navigate themselves towards memorize past cultivation temperature (T(c)) of their preference. For this thermotaxis, AFD thermosensory neuron is pivotal, which stereotypically responds to warming by increasing intracellular Ca(2+) level in a manner dependent on the remembered past T(c). We aimed to reveal how AFD encodes the information of temperature into neural activities. cGMP synthesis in AFD is crucial for thermosensation in AFD and thermotaxis behavior. Here we characterized the dynamic change of cGMP level in AFD by imaging animals expressing a fluorescence resonance energy transfer (FRET)-based cGMP probe specifically in AFD and found that cGMP dynamically responded to both warming and cooling in a manner dependent on past T(c). Moreover, we characterized mutant animals that lack guanylyl cyclases (GCYs) or phosphodiesterases (PDEs), which synthesize and hydrolyze cGMP, respectively, and uncovered how GCYs and PDEs contribute to cGMP and Ca(2+) dynamics in AFD and to thermotaxis behavior. Public Library of Science 2022-12-06 /pmc/articles/PMC9725164/ /pubmed/36472979 http://dx.doi.org/10.1371/journal.pone.0278343 Text en © 2022 Aok et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Aok, Ichiro
Shiota, Makoto
Tsukada, Yuki
Nakano, Shunji
Mori, Ikue
cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
title cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
title_full cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
title_fullStr cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
title_full_unstemmed cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
title_short cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
title_sort cgmp dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in c. elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9725164/
https://www.ncbi.nlm.nih.gov/pubmed/36472979
http://dx.doi.org/10.1371/journal.pone.0278343
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