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PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans

Male mating in Caenorhabditis elegans is a complex behavior with a strong mechanosensory component. C. elegans has several characterized mechanotransducer proteins, but few have been shown to contribute to mating. Here, we investigated the roles of PEZO-1, a piezo channel, and TRP-4, a mechanotransd...

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Autores principales: Brugman, Katherine I, Susoy, Vladislav, Whittaker, Allyson J, Palma, Wilber, Nava, Stephanie, Samuel, Aravinthan D T, Sternberg, Paul W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9802279/
https://www.ncbi.nlm.nih.gov/pubmed/36712331
http://dx.doi.org/10.1093/pnasnexus/pgac213
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author Brugman, Katherine I
Susoy, Vladislav
Whittaker, Allyson J
Palma, Wilber
Nava, Stephanie
Samuel, Aravinthan D T
Sternberg, Paul W
author_facet Brugman, Katherine I
Susoy, Vladislav
Whittaker, Allyson J
Palma, Wilber
Nava, Stephanie
Samuel, Aravinthan D T
Sternberg, Paul W
author_sort Brugman, Katherine I
collection PubMed
description Male mating in Caenorhabditis elegans is a complex behavior with a strong mechanosensory component. C. elegans has several characterized mechanotransducer proteins, but few have been shown to contribute to mating. Here, we investigated the roles of PEZO-1, a piezo channel, and TRP-4, a mechanotransducing TRPN channel, in male mating behavior. We show that pezo-1 is expressed in several male-specific neurons with known roles in mating. We show that, among other neurons, trp-4 is expressed in the Post-Cloacal sensilla neuron type A (PCA) sensory neuron, which monitors relative sliding between the male and the hermaphrodite and inhibits neurons involved in vulva detection. Mutations in both genes compromise many steps of mating, including initial response to the hermaphrodite, scanning, turning, and vulva detection. We performed pan-neuronal imaging during mating between freely moving mutant males and hermaphrodites. Both pezo-1 and trp-4 mutants showed spurious activation of the sensory neurons involved in vulva detection. In trp-4 mutants, this spurious activation might be caused by PCA failure to inhibit vulva-detecting neurons during scanning. Indeed, we show that without functional TRP-4, PCA fails to detect the relative sliding between the male and hermaphrodite. Cell-specific TRP-4 expression restores PCA's mechanosensory function. Our results demonstrate new roles for both PEZO-1 and TRP-4 mechanotransducers in C. elegans mating behavior.
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spelling pubmed-98022792023-01-26 PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans Brugman, Katherine I Susoy, Vladislav Whittaker, Allyson J Palma, Wilber Nava, Stephanie Samuel, Aravinthan D T Sternberg, Paul W PNAS Nexus Biological, Health, and Medical Sciences Male mating in Caenorhabditis elegans is a complex behavior with a strong mechanosensory component. C. elegans has several characterized mechanotransducer proteins, but few have been shown to contribute to mating. Here, we investigated the roles of PEZO-1, a piezo channel, and TRP-4, a mechanotransducing TRPN channel, in male mating behavior. We show that pezo-1 is expressed in several male-specific neurons with known roles in mating. We show that, among other neurons, trp-4 is expressed in the Post-Cloacal sensilla neuron type A (PCA) sensory neuron, which monitors relative sliding between the male and the hermaphrodite and inhibits neurons involved in vulva detection. Mutations in both genes compromise many steps of mating, including initial response to the hermaphrodite, scanning, turning, and vulva detection. We performed pan-neuronal imaging during mating between freely moving mutant males and hermaphrodites. Both pezo-1 and trp-4 mutants showed spurious activation of the sensory neurons involved in vulva detection. In trp-4 mutants, this spurious activation might be caused by PCA failure to inhibit vulva-detecting neurons during scanning. Indeed, we show that without functional TRP-4, PCA fails to detect the relative sliding between the male and hermaphrodite. Cell-specific TRP-4 expression restores PCA's mechanosensory function. Our results demonstrate new roles for both PEZO-1 and TRP-4 mechanotransducers in C. elegans mating behavior. Oxford University Press 2022-09-27 /pmc/articles/PMC9802279/ /pubmed/36712331 http://dx.doi.org/10.1093/pnasnexus/pgac213 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the National Academy of Sciences. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Biological, Health, and Medical Sciences
Brugman, Katherine I
Susoy, Vladislav
Whittaker, Allyson J
Palma, Wilber
Nava, Stephanie
Samuel, Aravinthan D T
Sternberg, Paul W
PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans
title PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans
title_full PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans
title_fullStr PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans
title_full_unstemmed PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans
title_short PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans
title_sort pezo-1 and trp-4 mechanosensors are involved in mating behavior in caenorhabditis elegans
topic Biological, Health, and Medical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9802279/
https://www.ncbi.nlm.nih.gov/pubmed/36712331
http://dx.doi.org/10.1093/pnasnexus/pgac213
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