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Single swim sessions in C. elegans induce key features of mammalian exercise

BACKGROUND: Exercise exerts remarkably powerful effects on metabolism and health, with anti-disease and anti-aging outcomes. Pharmacological manipulation of exercise benefit circuits might improve the health of the sedentary and the aging populations. Still, how exercised muscle signals to induce sy...

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Autores principales: Laranjeiro, Ricardo, Harinath, Girish, Burke, Daniel, Braeckman, Bart P., Driscoll, Monica
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5385602/
https://www.ncbi.nlm.nih.gov/pubmed/28395669
http://dx.doi.org/10.1186/s12915-017-0368-4
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author Laranjeiro, Ricardo
Harinath, Girish
Burke, Daniel
Braeckman, Bart P.
Driscoll, Monica
author_facet Laranjeiro, Ricardo
Harinath, Girish
Burke, Daniel
Braeckman, Bart P.
Driscoll, Monica
author_sort Laranjeiro, Ricardo
collection PubMed
description BACKGROUND: Exercise exerts remarkably powerful effects on metabolism and health, with anti-disease and anti-aging outcomes. Pharmacological manipulation of exercise benefit circuits might improve the health of the sedentary and the aging populations. Still, how exercised muscle signals to induce system-wide health improvement remains poorly understood. With a long-term interest in interventions that promote animal-wide health improvement, we sought to define exercise options for Caenorhabditis elegans. RESULTS: Here, we report on the impact of single swim sessions on C. elegans physiology. We used microcalorimetry to show that C. elegans swimming has a greater energy cost than crawling. Animals that swam continuously for 90 min specifically consumed muscle fat supplies and exhibited post-swim locomotory fatigue, with both muscle fat depletion and fatigue indicators recovering within 1 hour of exercise cessation. Quantitative polymerase chain reaction (qPCR) transcript analyses also suggested an increase in fat metabolism during the swim, followed by the downregulation of specific carbohydrate metabolism transcripts in the hours post-exercise. During a 90 min swim, muscle mitochondria matrix environments became more oxidized, as visualized by a localized mitochondrial reduction-oxidation-sensitive green fluorescent protein reporter. qPCR data supported specific transcriptional changes in oxidative stress defense genes during and immediately after a swim. Consistent with potential antioxidant defense induction, we found that a single swim session sufficed to confer protection against juglone-induced oxidative stress inflicted 4 hours post-exercise. CONCLUSIONS: In addition to showing that even a single swim exercise bout confers physiological changes that increase robustness, our data reveal that acute swimming-induced changes share common features with some acute exercise responses reported in humans. Overall, our data validate an easily implemented swim experience as C. elegans exercise, setting the foundation for exploiting the experimental advantages of this model to genetically or pharmacologically identify the exercise-associated molecules and signaling pathways that confer system-wide health benefits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0368-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-53856022017-04-11 Single swim sessions in C. elegans induce key features of mammalian exercise Laranjeiro, Ricardo Harinath, Girish Burke, Daniel Braeckman, Bart P. Driscoll, Monica BMC Biol Research Article BACKGROUND: Exercise exerts remarkably powerful effects on metabolism and health, with anti-disease and anti-aging outcomes. Pharmacological manipulation of exercise benefit circuits might improve the health of the sedentary and the aging populations. Still, how exercised muscle signals to induce system-wide health improvement remains poorly understood. With a long-term interest in interventions that promote animal-wide health improvement, we sought to define exercise options for Caenorhabditis elegans. RESULTS: Here, we report on the impact of single swim sessions on C. elegans physiology. We used microcalorimetry to show that C. elegans swimming has a greater energy cost than crawling. Animals that swam continuously for 90 min specifically consumed muscle fat supplies and exhibited post-swim locomotory fatigue, with both muscle fat depletion and fatigue indicators recovering within 1 hour of exercise cessation. Quantitative polymerase chain reaction (qPCR) transcript analyses also suggested an increase in fat metabolism during the swim, followed by the downregulation of specific carbohydrate metabolism transcripts in the hours post-exercise. During a 90 min swim, muscle mitochondria matrix environments became more oxidized, as visualized by a localized mitochondrial reduction-oxidation-sensitive green fluorescent protein reporter. qPCR data supported specific transcriptional changes in oxidative stress defense genes during and immediately after a swim. Consistent with potential antioxidant defense induction, we found that a single swim session sufficed to confer protection against juglone-induced oxidative stress inflicted 4 hours post-exercise. CONCLUSIONS: In addition to showing that even a single swim exercise bout confers physiological changes that increase robustness, our data reveal that acute swimming-induced changes share common features with some acute exercise responses reported in humans. Overall, our data validate an easily implemented swim experience as C. elegans exercise, setting the foundation for exploiting the experimental advantages of this model to genetically or pharmacologically identify the exercise-associated molecules and signaling pathways that confer system-wide health benefits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0368-4) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-10 /pmc/articles/PMC5385602/ /pubmed/28395669 http://dx.doi.org/10.1186/s12915-017-0368-4 Text en © Driscoll et al. 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Laranjeiro, Ricardo
Harinath, Girish
Burke, Daniel
Braeckman, Bart P.
Driscoll, Monica
Single swim sessions in C. elegans induce key features of mammalian exercise
title Single swim sessions in C. elegans induce key features of mammalian exercise
title_full Single swim sessions in C. elegans induce key features of mammalian exercise
title_fullStr Single swim sessions in C. elegans induce key features of mammalian exercise
title_full_unstemmed Single swim sessions in C. elegans induce key features of mammalian exercise
title_short Single swim sessions in C. elegans induce key features of mammalian exercise
title_sort single swim sessions in c. elegans induce key features of mammalian exercise
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5385602/
https://www.ncbi.nlm.nih.gov/pubmed/28395669
http://dx.doi.org/10.1186/s12915-017-0368-4
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