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

View Article: PubMed Central - PubMed

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.

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.

No MeSH data available.


Related in: MedlinePlus

Transcriptional changes in C. elegans suggest increased fat metabolism during swim exercise. a Diagram of fat metabolism highlighting the steps that we chose for our expression analysis. C. elegans proteins are shown in red. For simplicity, several metabolic steps are omitted. b Heat map summarizing quantitative polymerase chain reaction results in N2 animals at different time points post-exercise for fat metabolic genes (n = 5 independent trials). Expression data is presented as log2 fold change of exercise samples relative to control samples in a color gradient from red (downregulation) to dark green (upregulation). White represents no change in expression levels. Paired two-tailed Student’s t tests were used to compare relative expressions of control versus exercise samples at each time point. See Additional file 6 for detailed results for each gene. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC5385602&req=5

Fig5: Transcriptional changes in C. elegans suggest increased fat metabolism during swim exercise. a Diagram of fat metabolism highlighting the steps that we chose for our expression analysis. C. elegans proteins are shown in red. For simplicity, several metabolic steps are omitted. b Heat map summarizing quantitative polymerase chain reaction results in N2 animals at different time points post-exercise for fat metabolic genes (n = 5 independent trials). Expression data is presented as log2 fold change of exercise samples relative to control samples in a color gradient from red (downregulation) to dark green (upregulation). White represents no change in expression levels. Paired two-tailed Student’s t tests were used to compare relative expressions of control versus exercise samples at each time point. See Additional file 6 for detailed results for each gene. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001

Mentions: Fat metabolism is a complex network of enzymatic reactions that can lead to outcomes as diverse as lipid storage, fatty acid breakdown, lipid incorporation into cell membranes, or cell signaling, depending on the metabolic state and requirements of the organism. A large proportion of lipids in C. elegans, such as triglycerides, are stored in lipid droplets across different tissues. For fatty acids to be used as a source of energy, lipases have to break down triglycerides into glycerol and fatty acids. Fatty acids are then available for activation (conversion into acyl-coenzyme A(CoA)) followed by beta-oxidation, which generates acetyl-CoA that can enter the tricarboxylic acid cycle. We focused our analysis of lipid metabolism gene expression on fatty acid breakdown and lipid storage (Fig. 5a).Fig. 5


Single swim sessions in C. elegans induce key features of mammalian exercise
Transcriptional changes in C. elegans suggest increased fat metabolism during swim exercise. a Diagram of fat metabolism highlighting the steps that we chose for our expression analysis. C. elegans proteins are shown in red. For simplicity, several metabolic steps are omitted. b Heat map summarizing quantitative polymerase chain reaction results in N2 animals at different time points post-exercise for fat metabolic genes (n = 5 independent trials). Expression data is presented as log2 fold change of exercise samples relative to control samples in a color gradient from red (downregulation) to dark green (upregulation). White represents no change in expression levels. Paired two-tailed Student’s t tests were used to compare relative expressions of control versus exercise samples at each time point. See Additional file 6 for detailed results for each gene. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5385602&req=5

Fig5: Transcriptional changes in C. elegans suggest increased fat metabolism during swim exercise. a Diagram of fat metabolism highlighting the steps that we chose for our expression analysis. C. elegans proteins are shown in red. For simplicity, several metabolic steps are omitted. b Heat map summarizing quantitative polymerase chain reaction results in N2 animals at different time points post-exercise for fat metabolic genes (n = 5 independent trials). Expression data is presented as log2 fold change of exercise samples relative to control samples in a color gradient from red (downregulation) to dark green (upregulation). White represents no change in expression levels. Paired two-tailed Student’s t tests were used to compare relative expressions of control versus exercise samples at each time point. See Additional file 6 for detailed results for each gene. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001
Mentions: Fat metabolism is a complex network of enzymatic reactions that can lead to outcomes as diverse as lipid storage, fatty acid breakdown, lipid incorporation into cell membranes, or cell signaling, depending on the metabolic state and requirements of the organism. A large proportion of lipids in C. elegans, such as triglycerides, are stored in lipid droplets across different tissues. For fatty acids to be used as a source of energy, lipases have to break down triglycerides into glycerol and fatty acids. Fatty acids are then available for activation (conversion into acyl-coenzyme A(CoA)) followed by beta-oxidation, which generates acetyl-CoA that can enter the tricarboxylic acid cycle. We focused our analysis of lipid metabolism gene expression on fatty acid breakdown and lipid storage (Fig. 5a).Fig. 5

View Article: PubMed Central - PubMed

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&nbsp;min specifically consumed muscle fat supplies and exhibited post-swim locomotory fatigue, with both muscle fat depletion and fatigue indicators recovering within 1&nbsp;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&nbsp;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&nbsp;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.

No MeSH data available.


Related in: MedlinePlus