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

(2017) BMC BIOLOGY. 15(1).
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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.
Keywords
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

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Citation

Please use this url to cite or link to this publication:

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.
@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},
}

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