Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.

Feeding, a vital behavior in animals, is modulated depending on internal and external factors. In the nematode Caenorhabditis elegans, the feeding organ called the pharynx ingests food by pumping driven by the pharyngeal muscles. Here we report that optical silencing of the body wall muscles, which...

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Main Authors: Megumi Takahashi, Shin Takagi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-12-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5760098?pdf=render
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spelling doaj-097c3d121d5e47deb973c288346fc96b2020-11-24T21:41:59ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042017-12-011312e100713410.1371/journal.pgen.1007134Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.Megumi TakahashiShin TakagiFeeding, a vital behavior in animals, is modulated depending on internal and external factors. In the nematode Caenorhabditis elegans, the feeding organ called the pharynx ingests food by pumping driven by the pharyngeal muscles. Here we report that optical silencing of the body wall muscles, which drive the locomotory movement of worms, affects pumping. In worms expressing the Arch proton pump or the ACR2 anion channel in the body wall muscle cells, the pumping rate decreases after activation of Arch or ACR2 with light illumination, and recovers gradually after terminating illumination. Pumping was similarly inhibited by illumination in locomotion-defective mutants carrying Arch, suggesting that perturbation of locomotory movement is not critical for pumping inhibition. Analysis of mutants and cell ablation experiments showed that the signals mediating the pumping inhibition response triggered by activation of Arch with weak light are transferred mainly through two pathways: one involving gap junction-dependent mechanisms through pharyngeal I1 neurons, which mediate fast signals, and the other involving dense-core vesicle-dependent mechanisms, which mediate slow signals. Activation of Arch with strong light inhibited pumping strongly in a manner that does not rely on either gap junction-dependent or dense-core vesicle-dependent mechanisms. Our study revealed a new aspect of the neural and neuroendocrine controls of pumping initiated from the body wall muscles.http://europepmc.org/articles/PMC5760098?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Megumi Takahashi
Shin Takagi
spellingShingle Megumi Takahashi
Shin Takagi
Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.
PLoS Genetics
author_facet Megumi Takahashi
Shin Takagi
author_sort Megumi Takahashi
title Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.
title_short Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.
title_full Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.
title_fullStr Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.
title_full_unstemmed Optical silencing of body wall muscles induces pumping inhibition in Caenorhabditis elegans.
title_sort optical silencing of body wall muscles induces pumping inhibition in caenorhabditis elegans.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2017-12-01
description Feeding, a vital behavior in animals, is modulated depending on internal and external factors. In the nematode Caenorhabditis elegans, the feeding organ called the pharynx ingests food by pumping driven by the pharyngeal muscles. Here we report that optical silencing of the body wall muscles, which drive the locomotory movement of worms, affects pumping. In worms expressing the Arch proton pump or the ACR2 anion channel in the body wall muscle cells, the pumping rate decreases after activation of Arch or ACR2 with light illumination, and recovers gradually after terminating illumination. Pumping was similarly inhibited by illumination in locomotion-defective mutants carrying Arch, suggesting that perturbation of locomotory movement is not critical for pumping inhibition. Analysis of mutants and cell ablation experiments showed that the signals mediating the pumping inhibition response triggered by activation of Arch with weak light are transferred mainly through two pathways: one involving gap junction-dependent mechanisms through pharyngeal I1 neurons, which mediate fast signals, and the other involving dense-core vesicle-dependent mechanisms, which mediate slow signals. Activation of Arch with strong light inhibited pumping strongly in a manner that does not rely on either gap junction-dependent or dense-core vesicle-dependent mechanisms. Our study revealed a new aspect of the neural and neuroendocrine controls of pumping initiated from the body wall muscles.
url http://europepmc.org/articles/PMC5760098?pdf=render
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