Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases

Even though microbial photosensitive proteins have been used for optogenetics, their use should be optimized to precisely control cell and tissue functions in vivo. We exploited GtCCR4 and KnChR, cation channelrhodopsins from algae, BeGC1, a guanylyl cyclase rhodopsin from a fungus, and photoactivat...

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Main Authors: Hanako Hagio, Wataru Koyama, Shiori Hosaka, Aysenur Deniz Song, Janchiv Narantsatsral, Koji Matsuda, Takashi Shimizu, Shoko Hososhima, Satoshi P Tsunoda, Hideki Kandori, Masahiko Hibi
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/83975
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author Hanako Hagio
Wataru Koyama
Shiori Hosaka
Aysenur Deniz Song
Janchiv Narantsatsral
Koji Matsuda
Takashi Shimizu
Shoko Hososhima
Satoshi P Tsunoda
Hideki Kandori
Masahiko Hibi
author_facet Hanako Hagio
Wataru Koyama
Shiori Hosaka
Aysenur Deniz Song
Janchiv Narantsatsral
Koji Matsuda
Takashi Shimizu
Shoko Hososhima
Satoshi P Tsunoda
Hideki Kandori
Masahiko Hibi
author_sort Hanako Hagio
collection DOAJ
description Even though microbial photosensitive proteins have been used for optogenetics, their use should be optimized to precisely control cell and tissue functions in vivo. We exploited GtCCR4 and KnChR, cation channelrhodopsins from algae, BeGC1, a guanylyl cyclase rhodopsin from a fungus, and photoactivated adenylyl cyclases (PACs) from cyanobacteria (OaPAC) or bacteria (bPAC), to control cell functions in zebrafish. Optical activation of GtCCR4 and KnChR in the hindbrain reticulospinal V2a neurons, which are involved in locomotion, induced swimming behavior at relatively short latencies, whereas activation of BeGC1 or PACs achieved it at long latencies. Activation of GtCCR4 and KnChR in cardiomyocytes induced cardiac arrest, whereas activation of bPAC gradually induced bradycardia. KnChR activation led to an increase in intracellular Ca2+ in the heart, suggesting that depolarization caused cardiac arrest. These data suggest that these optogenetic tools can be used to reveal the function and regulation of zebrafish neurons and cardiomyocytes.
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spelling doaj.art-c36260fca69f49f4aaeca2fe96ce128e2023-08-17T13:19:23ZengeLife Sciences Publications LtdeLife2050-084X2023-08-011210.7554/eLife.83975Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclasesHanako Hagio0https://orcid.org/0000-0003-2197-4595Wataru Koyama1https://orcid.org/0009-0005-6851-5961Shiori Hosaka2Aysenur Deniz Song3https://orcid.org/0000-0003-0998-9225Janchiv Narantsatsral4Koji Matsuda5Takashi Shimizu6https://orcid.org/0000-0002-8750-6797Shoko Hososhima7Satoshi P Tsunoda8Hideki Kandori9https://orcid.org/0000-0002-4922-1344Masahiko Hibi10https://orcid.org/0000-0002-9142-4444Graduate School of Science, Nagoya University, Japan, Nagoya, Japan; Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan; Institute for Advanced Research, Nagoya University, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanDepartment of Life Science and Applied Chemistry, Nagoya Institute of Technology, Nagoya, JapanDepartment of Life Science and Applied Chemistry, Nagoya Institute of Technology, Nagoya, JapanDepartment of Life Science and Applied Chemistry, Nagoya Institute of Technology, Nagoya, JapanGraduate School of Science, Nagoya University, Japan, Nagoya, JapanEven though microbial photosensitive proteins have been used for optogenetics, their use should be optimized to precisely control cell and tissue functions in vivo. We exploited GtCCR4 and KnChR, cation channelrhodopsins from algae, BeGC1, a guanylyl cyclase rhodopsin from a fungus, and photoactivated adenylyl cyclases (PACs) from cyanobacteria (OaPAC) or bacteria (bPAC), to control cell functions in zebrafish. Optical activation of GtCCR4 and KnChR in the hindbrain reticulospinal V2a neurons, which are involved in locomotion, induced swimming behavior at relatively short latencies, whereas activation of BeGC1 or PACs achieved it at long latencies. Activation of GtCCR4 and KnChR in cardiomyocytes induced cardiac arrest, whereas activation of bPAC gradually induced bradycardia. KnChR activation led to an increase in intracellular Ca2+ in the heart, suggesting that depolarization caused cardiac arrest. These data suggest that these optogenetic tools can be used to reveal the function and regulation of zebrafish neurons and cardiomyocytes.https://elifesciences.org/articles/83975optogeneticsrhodopsinguanylyl cyclaseadenylyl cyclaselocomotioncardiac contraction
spellingShingle Hanako Hagio
Wataru Koyama
Shiori Hosaka
Aysenur Deniz Song
Janchiv Narantsatsral
Koji Matsuda
Takashi Shimizu
Shoko Hososhima
Satoshi P Tsunoda
Hideki Kandori
Masahiko Hibi
Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
eLife
optogenetics
rhodopsin
guanylyl cyclase
adenylyl cyclase
locomotion
cardiac contraction
title Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
title_full Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
title_fullStr Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
title_full_unstemmed Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
title_short Optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
title_sort optogenetic manipulation of neuronal and cardiomyocyte functions in zebrafish using microbial rhodopsins and adenylyl cyclases
topic optogenetics
rhodopsin
guanylyl cyclase
adenylyl cyclase
locomotion
cardiac contraction
url https://elifesciences.org/articles/83975
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