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

Ricardo Laranjeiro, Girish Harinath, Daniel Burke, Bart Braeckman UGent and Monica Driscoll (2017) BMC BIOLOGY. 15(1).
abstract
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
Exercise, C. elegans, Muscle, Oxidative stress, Metabolism, EXTRACELLULAR-SUPEROXIDE DISMUTASE, HUMAN SKELETAL-MUSCLE, NEMATODE CAENORHABDITIS-ELEGANS, OXIDATIVE-STRESS-RESPONSE, ENDURANCE-TRAINED MALES, PHYSICAL-ACTIVITY, GENE-EXPRESSION, HEALTH-BENEFITS, LIFE-SPAN, LONGEVITY
journal title
BMC BIOLOGY
BMC Biol.
volume
15
issue
1
article number
30
pages
17 pages
Web of Science type
Article
Web of Science id
000401488800001
ISSN
1741-7007
DOI
10.1186/s12915-017-0368-4
language
English
UGent publication?
yes
classification
A1
copyright statement
Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
id
8517667
handle
http://hdl.handle.net/1854/LU-8517667
date created
2017-04-13 12:22:58
date last changed
2017-06-28 08:54:50
@article{8517667,
  abstract     = {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.},
  articleno    = {30},
  author       = {Laranjeiro, Ricardo and Harinath, Girish and Burke, Daniel and Braeckman, Bart and Driscoll, Monica},
  issn         = {1741-7007},
  journal      = {BMC BIOLOGY},
  keyword      = {Exercise,C. elegans,Muscle,Oxidative stress,Metabolism,EXTRACELLULAR-SUPEROXIDE DISMUTASE,HUMAN SKELETAL-MUSCLE,NEMATODE CAENORHABDITIS-ELEGANS,OXIDATIVE-STRESS-RESPONSE,ENDURANCE-TRAINED MALES,PHYSICAL-ACTIVITY,GENE-EXPRESSION,HEALTH-BENEFITS,LIFE-SPAN,LONGEVITY},
  language     = {eng},
  number       = {1},
  pages        = {17},
  title        = {Single swim sessions in C. elegans induce key features of mammalian exercise},
  url          = {http://dx.doi.org/10.1186/s12915-017-0368-4},
  volume       = {15},
  year         = {2017},
}

Chicago
Laranjeiro, Ricardo, Girish Harinath, Daniel Burke, Bart Braeckman, and Monica Driscoll. 2017. “Single Swim Sessions in C. Elegans Induce Key Features of Mammalian Exercise.” Bmc Biology 15 (1).
APA
Laranjeiro, R., Harinath, G., Burke, D., Braeckman, B., & Driscoll, M. (2017). Single swim sessions in C. elegans induce key features of mammalian exercise. BMC BIOLOGY, 15(1).
Vancouver
1.
Laranjeiro R, Harinath G, Burke D, Braeckman B, Driscoll M. Single swim sessions in C. elegans induce key features of mammalian exercise. BMC BIOLOGY. 2017;15(1).
MLA
Laranjeiro, Ricardo, Girish Harinath, Daniel Burke, et al. “Single Swim Sessions in C. Elegans Induce Key Features of Mammalian Exercise.” BMC BIOLOGY 15.1 (2017): n. pag. Print.