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Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution

Nervous systems are endowed with rapid chemosensation and intercellular signaling by ligand-gated ion channels (LGICs). While a complex, bilaterally symmetrical nervous system is a major innovation of bilaterian animals, the employment of specific LGICs during early bilaterian evolution is poorly un...

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Autores principales: Martí-Solans, Josep, Børve, Aina, Bump, Paul, Hejnol, Andreas, Lynagh, Timothy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9949801/
https://www.ncbi.nlm.nih.gov/pubmed/36821351
http://dx.doi.org/10.7554/eLife.81613
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author Martí-Solans, Josep
Børve, Aina
Bump, Paul
Hejnol, Andreas
Lynagh, Timothy
author_facet Martí-Solans, Josep
Børve, Aina
Bump, Paul
Hejnol, Andreas
Lynagh, Timothy
author_sort Martí-Solans, Josep
collection PubMed
description Nervous systems are endowed with rapid chemosensation and intercellular signaling by ligand-gated ion channels (LGICs). While a complex, bilaterally symmetrical nervous system is a major innovation of bilaterian animals, the employment of specific LGICs during early bilaterian evolution is poorly understood. We therefore questioned bilaterian animals’ employment of acid-sensing ion channels (ASICs), LGICs that mediate fast excitatory responses to decreases in extracellular pH in vertebrate neurons. Our phylogenetic analysis identified an earlier emergence of ASICs from the overarching DEG/ENaC (degenerin/epithelial sodium channel) superfamily than previously thought and suggests that ASICs were a bilaterian innovation. Our broad examination of ASIC gene expression and biophysical function in each major bilaterian lineage of Xenacoelomorpha, Protostomia, and Deuterostomia suggests that the earliest bilaterian ASICs were probably expressed in the periphery, before being incorporated into the brain as it emerged independently in certain deuterostomes and xenacoelomorphs. The loss of certain peripheral cells from Ecdysozoa after they separated from other protostomes likely explains their loss of ASICs, and thus the absence of ASICs from model organisms Drosophila and Caenorhabditis elegans. Thus, our use of diverse bilaterians in the investigation of LGIC expression and function offers a unique hypothesis on the employment of LGICs in early bilaterian evolution.
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spelling pubmed-99498012023-02-24 Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution Martí-Solans, Josep Børve, Aina Bump, Paul Hejnol, Andreas Lynagh, Timothy eLife Evolutionary Biology Nervous systems are endowed with rapid chemosensation and intercellular signaling by ligand-gated ion channels (LGICs). While a complex, bilaterally symmetrical nervous system is a major innovation of bilaterian animals, the employment of specific LGICs during early bilaterian evolution is poorly understood. We therefore questioned bilaterian animals’ employment of acid-sensing ion channels (ASICs), LGICs that mediate fast excitatory responses to decreases in extracellular pH in vertebrate neurons. Our phylogenetic analysis identified an earlier emergence of ASICs from the overarching DEG/ENaC (degenerin/epithelial sodium channel) superfamily than previously thought and suggests that ASICs were a bilaterian innovation. Our broad examination of ASIC gene expression and biophysical function in each major bilaterian lineage of Xenacoelomorpha, Protostomia, and Deuterostomia suggests that the earliest bilaterian ASICs were probably expressed in the periphery, before being incorporated into the brain as it emerged independently in certain deuterostomes and xenacoelomorphs. The loss of certain peripheral cells from Ecdysozoa after they separated from other protostomes likely explains their loss of ASICs, and thus the absence of ASICs from model organisms Drosophila and Caenorhabditis elegans. Thus, our use of diverse bilaterians in the investigation of LGIC expression and function offers a unique hypothesis on the employment of LGICs in early bilaterian evolution. eLife Sciences Publications, Ltd 2023-02-23 /pmc/articles/PMC9949801/ /pubmed/36821351 http://dx.doi.org/10.7554/eLife.81613 Text en © 2023, Martí-Solans 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 Evolutionary Biology
Martí-Solans, Josep
Børve, Aina
Bump, Paul
Hejnol, Andreas
Lynagh, Timothy
Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
title Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
title_full Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
title_fullStr Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
title_full_unstemmed Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
title_short Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
title_sort peripheral and central employment of acid-sensing ion channels during early bilaterian evolution
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9949801/
https://www.ncbi.nlm.nih.gov/pubmed/36821351
http://dx.doi.org/10.7554/eLife.81613
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