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An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans

BACKGROUND: Optogenetics allows the experimental manipulation of excitable cells by a light stimulus without the need for technically challenging and invasive procedures. The high degree of spatial, temporal, and intensity control that can be achieved with a light stimulus, combined with cell type-s...

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Autores principales: Koopman, M., Janssen, L., Nollen, E. A. A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8386059/
https://www.ncbi.nlm.nih.gov/pubmed/34429103
http://dx.doi.org/10.1186/s12915-021-01085-2
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author Koopman, M.
Janssen, L.
Nollen, E. A. A.
author_facet Koopman, M.
Janssen, L.
Nollen, E. A. A.
author_sort Koopman, M.
collection PubMed
description BACKGROUND: Optogenetics allows the experimental manipulation of excitable cells by a light stimulus without the need for technically challenging and invasive procedures. The high degree of spatial, temporal, and intensity control that can be achieved with a light stimulus, combined with cell type-specific expression of light-sensitive ion channels, enables highly specific and precise stimulation of excitable cells. Optogenetic tools have therefore revolutionized the study of neuronal circuits in a number of models, including Caenorhabditis elegans. Despite the existence of several optogenetic systems that allow spatial and temporal photoactivation of light-sensitive actuators in C. elegans, their high costs and low flexibility have limited wide access to optogenetics. Here, we developed an inexpensive, easy-to-build, modular, and adjustable optogenetics device for use on different microscopes and worm trackers, which we called the OptoArm. RESULTS: The OptoArm allows for single- and multiple-worm illumination and is adaptable in terms of light intensity, lighting profiles, and light color. We demonstrate OptoArm’s power in a population-based multi-parameter study on the contributions of motor circuit cells to age-related motility decline. We found that individual components of the neuromuscular system display different rates of age-dependent deterioration. The functional decline of cholinergic neurons mirrors motor decline, while GABAergic neurons and muscle cells are relatively age-resilient, suggesting that rate-limiting cells exist and determine neuronal circuit ageing. CONCLUSION: We have assembled an economical, reliable, and highly adaptable optogenetics system which can be deployed to address diverse biological questions. We provide a detailed description of the construction as well as technical and biological validation of our set-up. Importantly, use of the OptoArm is not limited to C. elegans and may benefit studies in multiple model organisms, making optogenetics more accessible to the broader research community. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01085-2.
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spelling pubmed-83860592021-08-26 An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans Koopman, M. Janssen, L. Nollen, E. A. A. BMC Biol Methodology Article BACKGROUND: Optogenetics allows the experimental manipulation of excitable cells by a light stimulus without the need for technically challenging and invasive procedures. The high degree of spatial, temporal, and intensity control that can be achieved with a light stimulus, combined with cell type-specific expression of light-sensitive ion channels, enables highly specific and precise stimulation of excitable cells. Optogenetic tools have therefore revolutionized the study of neuronal circuits in a number of models, including Caenorhabditis elegans. Despite the existence of several optogenetic systems that allow spatial and temporal photoactivation of light-sensitive actuators in C. elegans, their high costs and low flexibility have limited wide access to optogenetics. Here, we developed an inexpensive, easy-to-build, modular, and adjustable optogenetics device for use on different microscopes and worm trackers, which we called the OptoArm. RESULTS: The OptoArm allows for single- and multiple-worm illumination and is adaptable in terms of light intensity, lighting profiles, and light color. We demonstrate OptoArm’s power in a population-based multi-parameter study on the contributions of motor circuit cells to age-related motility decline. We found that individual components of the neuromuscular system display different rates of age-dependent deterioration. The functional decline of cholinergic neurons mirrors motor decline, while GABAergic neurons and muscle cells are relatively age-resilient, suggesting that rate-limiting cells exist and determine neuronal circuit ageing. CONCLUSION: We have assembled an economical, reliable, and highly adaptable optogenetics system which can be deployed to address diverse biological questions. We provide a detailed description of the construction as well as technical and biological validation of our set-up. Importantly, use of the OptoArm is not limited to C. elegans and may benefit studies in multiple model organisms, making optogenetics more accessible to the broader research community. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01085-2. BioMed Central 2021-08-24 /pmc/articles/PMC8386059/ /pubmed/34429103 http://dx.doi.org/10.1186/s12915-021-01085-2 Text en © The Author(s) 2021, corrected publication 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Methodology Article
Koopman, M.
Janssen, L.
Nollen, E. A. A.
An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans
title An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans
title_full An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans
title_fullStr An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans
title_full_unstemmed An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans
title_short An economical and highly adaptable optogenetics system for individual and population-level manipulation of Caenorhabditis elegans
title_sort economical and highly adaptable optogenetics system for individual and population-level manipulation of caenorhabditis elegans
topic Methodology Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8386059/
https://www.ncbi.nlm.nih.gov/pubmed/34429103
http://dx.doi.org/10.1186/s12915-021-01085-2
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