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Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock

Biological clocks are fundamental to an organism’s health, controlling periodicity of behaviour and metabolism. Here, we identify two acid-sensing ion channels, with very different proton sensing properties, and describe their role in an ultradian clock, the defecation motor program (DMP) of the nem...

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Autores principales: Kaulich, Eva, Carroll, Trae, Ackley, Brian D, Tang, Yi-Quan, Hardege, Iris, Nehrke, Keith, Schafer, William R, Walker, Denise S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9374441/
https://www.ncbi.nlm.nih.gov/pubmed/35666106
http://dx.doi.org/10.7554/eLife.75837
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author Kaulich, Eva
Carroll, Trae
Ackley, Brian D
Tang, Yi-Quan
Hardege, Iris
Nehrke, Keith
Schafer, William R
Walker, Denise S
author_facet Kaulich, Eva
Carroll, Trae
Ackley, Brian D
Tang, Yi-Quan
Hardege, Iris
Nehrke, Keith
Schafer, William R
Walker, Denise S
author_sort Kaulich, Eva
collection PubMed
description Biological clocks are fundamental to an organism’s health, controlling periodicity of behaviour and metabolism. Here, we identify two acid-sensing ion channels, with very different proton sensing properties, and describe their role in an ultradian clock, the defecation motor program (DMP) of the nematode Caenorhabditis elegans. An ACD-5-containing channel, on the apical membrane of the intestinal epithelium, is essential for maintenance of luminal acidity, and thus the rhythmic oscillations in lumen pH. In contrast, the second channel, composed of FLR-1, ACD-3 and/or DEL-5, located on the basolateral membrane, controls the intracellular Ca(2+) wave and forms a core component of the master oscillator that controls the timing and rhythmicity of the DMP. flr-1 and acd-3/del-5 mutants show severe developmental and metabolic defects. We thus directly link the proton-sensing properties of these channels to their physiological roles in pH regulation and Ca(2+) signalling, the generation of an ultradian oscillator, and its metabolic consequences.
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spelling pubmed-93744412022-08-13 Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock Kaulich, Eva Carroll, Trae Ackley, Brian D Tang, Yi-Quan Hardege, Iris Nehrke, Keith Schafer, William R Walker, Denise S eLife Cell Biology Biological clocks are fundamental to an organism’s health, controlling periodicity of behaviour and metabolism. Here, we identify two acid-sensing ion channels, with very different proton sensing properties, and describe their role in an ultradian clock, the defecation motor program (DMP) of the nematode Caenorhabditis elegans. An ACD-5-containing channel, on the apical membrane of the intestinal epithelium, is essential for maintenance of luminal acidity, and thus the rhythmic oscillations in lumen pH. In contrast, the second channel, composed of FLR-1, ACD-3 and/or DEL-5, located on the basolateral membrane, controls the intracellular Ca(2+) wave and forms a core component of the master oscillator that controls the timing and rhythmicity of the DMP. flr-1 and acd-3/del-5 mutants show severe developmental and metabolic defects. We thus directly link the proton-sensing properties of these channels to their physiological roles in pH regulation and Ca(2+) signalling, the generation of an ultradian oscillator, and its metabolic consequences. eLife Sciences Publications, Ltd 2022-06-06 /pmc/articles/PMC9374441/ /pubmed/35666106 http://dx.doi.org/10.7554/eLife.75837 Text en © 2022, Kaulich et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Kaulich, Eva
Carroll, Trae
Ackley, Brian D
Tang, Yi-Quan
Hardege, Iris
Nehrke, Keith
Schafer, William R
Walker, Denise S
Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock
title Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock
title_full Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock
title_fullStr Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock
title_full_unstemmed Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock
title_short Distinct roles for two Caenorhabditis elegans acid-sensing ion channels in an ultradian clock
title_sort distinct roles for two caenorhabditis elegans acid-sensing ion channels in an ultradian clock
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9374441/
https://www.ncbi.nlm.nih.gov/pubmed/35666106
http://dx.doi.org/10.7554/eLife.75837
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