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Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility

Gut peristalsis, recognized as a wave-like progression along the anterior-posterior gut axis, plays a pivotal role in the transportation, digestion, and absorption of ingested materials. The embryonic gut, which has not experienced ingested materials, undergoes peristalsis offering a powerful model...

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Autores principales: Shikaya, Yuuki, Inaba, Masafumi, Tadokoro, Ryosuke, Utsunomiya, Shota, Takahashi, Yoshiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245550/
https://www.ncbi.nlm.nih.gov/pubmed/37293264
http://dx.doi.org/10.3389/fphys.2023.1175951
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author Shikaya, Yuuki
Inaba, Masafumi
Tadokoro, Ryosuke
Utsunomiya, Shota
Takahashi, Yoshiko
author_facet Shikaya, Yuuki
Inaba, Masafumi
Tadokoro, Ryosuke
Utsunomiya, Shota
Takahashi, Yoshiko
author_sort Shikaya, Yuuki
collection PubMed
description Gut peristalsis, recognized as a wave-like progression along the anterior-posterior gut axis, plays a pivotal role in the transportation, digestion, and absorption of ingested materials. The embryonic gut, which has not experienced ingested materials, undergoes peristalsis offering a powerful model for studying the intrinsic mechanisms underlying the gut motility. It has previously been shown in chicken embryos that acute contractions of the cloaca (an anus-like structure) located at the posterior end of the hindgut are tightly coupled with the arrival of hindgut-derived waves. To further scrutinize the interactions between hindgut and cloaca, we here developed an optogenetic method that produced artificial waves in the hindgut. A variant form of channelrhodopsin-2 (ChR2(D156C)), permitting extremely large photocurrents, was expressed in the muscle component of the hindgut of chicken embryos using Tol2-mediated gene transfer and in ovo electroporation techniques. The D156C-expressing hindgut responded efficiently to local pulses of blue light: local contractions emerge at an ectopic site in the hindgut, which were followed by peristaltic waves that reached to the endpoint of the hindgut. Markedly, the arrival of the optogenetically induced waves caused concomitant contractions of the cloaca, revealing that the hindgut-cloaca coordination is mediated by signals triggered by peristaltic waves. Moreover, a cloaca undergoing pharmacologically provoked aberrant contractions could respond to pulsed blue light irradiation. Together, the optogenetic technology developed in this study for inducing gut peristalsis paves the way to study the gut movement and also to explore therapeutic methodology for peristaltic disorders.
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spelling pubmed-102455502023-06-08 Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility Shikaya, Yuuki Inaba, Masafumi Tadokoro, Ryosuke Utsunomiya, Shota Takahashi, Yoshiko Front Physiol Physiology Gut peristalsis, recognized as a wave-like progression along the anterior-posterior gut axis, plays a pivotal role in the transportation, digestion, and absorption of ingested materials. The embryonic gut, which has not experienced ingested materials, undergoes peristalsis offering a powerful model for studying the intrinsic mechanisms underlying the gut motility. It has previously been shown in chicken embryos that acute contractions of the cloaca (an anus-like structure) located at the posterior end of the hindgut are tightly coupled with the arrival of hindgut-derived waves. To further scrutinize the interactions between hindgut and cloaca, we here developed an optogenetic method that produced artificial waves in the hindgut. A variant form of channelrhodopsin-2 (ChR2(D156C)), permitting extremely large photocurrents, was expressed in the muscle component of the hindgut of chicken embryos using Tol2-mediated gene transfer and in ovo electroporation techniques. The D156C-expressing hindgut responded efficiently to local pulses of blue light: local contractions emerge at an ectopic site in the hindgut, which were followed by peristaltic waves that reached to the endpoint of the hindgut. Markedly, the arrival of the optogenetically induced waves caused concomitant contractions of the cloaca, revealing that the hindgut-cloaca coordination is mediated by signals triggered by peristaltic waves. Moreover, a cloaca undergoing pharmacologically provoked aberrant contractions could respond to pulsed blue light irradiation. Together, the optogenetic technology developed in this study for inducing gut peristalsis paves the way to study the gut movement and also to explore therapeutic methodology for peristaltic disorders. Frontiers Media S.A. 2023-05-15 /pmc/articles/PMC10245550/ /pubmed/37293264 http://dx.doi.org/10.3389/fphys.2023.1175951 Text en Copyright © 2023 Shikaya, Inaba, Tadokoro, Utsunomiya and Takahashi. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Shikaya, Yuuki
Inaba, Masafumi
Tadokoro, Ryosuke
Utsunomiya, Shota
Takahashi, Yoshiko
Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
title Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
title_full Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
title_fullStr Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
title_full_unstemmed Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
title_short Optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
title_sort optogenetic control of gut movements reveals peristaltic wave-mediated induction of cloacal contractions and reactivation of impaired gut motility
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245550/
https://www.ncbi.nlm.nih.gov/pubmed/37293264
http://dx.doi.org/10.3389/fphys.2023.1175951
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