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. 2018 Jun 20;8(1):9420.
doi: 10.1038/s41598-018-27330-3.

A Novel Vibration-Induced Exercise Paradigm Improves Fitness and Lipid Metabolism of Caenorhabditis Elegans

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Free PMC article

A Novel Vibration-Induced Exercise Paradigm Improves Fitness and Lipid Metabolism of Caenorhabditis Elegans

Emelyne Teo et al. Sci Rep. .
Free PMC article

Abstract

Exercise has been known to reduce the risk of obesity and metabolic syndrome, but the mechanisms underlying many exercise benefits remain unclear. This is, in part, due to a lack of exercise paradigms in invertebrate model organisms that would allow rapid mechanistic studies to be conducted. Here we report a novel exercise paradigm in Caenorhabditis elegans (C. elegans) that can be implemented under standard laboratory conditions. Mechanical stimulus in the form of vibration was transduced to C. elegans grown on solid agar media using an acoustic actuator. One day post-exercise, the exercised animals showed greater physical fitness compared to the un-exercised controls. Despite having higher mitochondrial reactive oxygen species levels, no mitohormetic adaptations and lifespan extension were observed in the exercised animals. Nonetheless, exercised animals showed lower triacylglycerides (TAG) accumulation than the controls. Among the individual TAG species, the most significant changes were found in mono- and polyunsaturated fatty acid residues. Such alteration resulted in an overall lower double bond index and peroxidation index which measure susceptibility towards lipid peroxidation. These observations are consistent with findings from mammalian exercise literature, suggesting that exercise benefits are largely conserved across different animal models.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Overview of the exercise paradigm. (A) Block diagram of the nematode exercise system. Exercise was implemented at 25 °C. (B) Frequency optimization. Change in speed of animals was calculated by taking the ratio of speed before and immediately after a one min vibration to the initial speed of animal (n = 5 animals per data point). (C) Speed-time profile of animals during continuous vibration (**P < 0.01, ***P < 0.001; one-way ANOVA post-test Dunnett’s multiple comparisons to t = 0; n = 8 animals per data point). (D) Speed-time profile of animals during interval vibration mode (**P < 0.01, ***P < 0.001; one-way ANOVA post-test Dunnett’s multiple comparisons to t = 0; n = 8 animals per data point). (E) Schematic of the time sequence used in our final exercise paradigm. (F) Speed-time profile of animals during the final exercise paradigm (*P < 0.05, ***P < 0.001; one-way ANOVA post-test Dunnett’s multiple comparisons to t = 0; n = 8 animals per data point). (G) Total exercise effect estimation (***P < 0.001; n = 8 animals per group). Total distance travelled was calculated by taking the area under the curve of speed-time graphs during the training phase only. Speed of animals was monitored at the 1st and 30th minute of each interval (representing the start and end of each cycle). All experiments described in this panel were performed in JK1107 animals at day 6 post bleaching. Experiments were carried out in at least two other trials, with similar trends observed.
Figure 2
Figure 2
Exercise benefits observed in C. elegans one day post-training (day 7 post bleaching). (A) Exercised animals had higher spontaneous distance travel ability (*P < 0.05; n ≥ 20 animals per group). (B) No significant difference in peak speed of exploring was observed between exercised and control animals (n ≥ 20 animals per group). (C) Exercised animals spent significantly more time exploring the plate than the control animals (**P < 0.005; n ≥ 20 animals per group). (D) A significantly greater percentage of control animals remained close to the origin for the duration of the trial (non-exploring) compared to the exercised animals (*P < 0.05; n = 5 independent trials with at least 20 animals per group per trial). (E) Representative images showing a typical non-exploring control and an actively exploring exercised animal. (F) There was a higher percentage of actively swimming nematodes in the exercised group after being placed in M9 buffer for 2 h compared to controls (*P < 0.05; n = 10 independent trials with at least 20 animals per group per trial). All experiments described in this panel have been carried out in at least two other trials, with similar trends observed.
Figure 3
Figure 3
Lifespan curves of three different trials. A significantly greater lifespan extension effect was observed only in the first trial (Log rank test P < 0.05).
Figure 4
Figure 4
Vibration-induced exercise paradigm increased mitochondrial ROS without inducing toxicity. (A) Mitosox fluorescence intensity was significantly higher in the exercised animals compared to controls immediately after the exercise training on day 6 of age (*P < 0.05; n ≥ 25 animals per group). (B) Pumping rate, measured immediately after the exercise training on day 6 of age, was not significantly different between the exercised and control animals (n ≥ 15 animals per group). (C) Total no of eggs laid was not significantly different between the exercised and control animals (n = 8 animals per group). (D) No significant differences were observed for transcript levels of mitohormetic or mitochondrial-related genes skn-1, polg-1 and ctb-1 between the exercised and control animals one day post exercise (day 7 of age) (n = 3 biological replicates per group; each replicate contains approximately 500 animals collected on different trials). pmp-3 was used as endogenous control. All experiments described in Fig. 4A–C have been carried out in at least two other trials, with similar trends observed.
Figure 5
Figure 5
The vibration-induced exercise paradigm did not trigger mitochondrial adaptations in C. elegans. (A) No significant difference was observed for mitochondrial DNA copy number between the exercised and control animals (n ≥ 20 animals per group). Similar trend was observed in two other trials. (B) Representative images of mitochondrial morphology in sarcomeres of young (D7) and old (D12) exercised and control animals, using transgenic strain SJ4103[myo-3p::GFP(mit)] (n ≥ 10 animals per group). Similar trend was observed in two other trials. (C) Oxygen consumption rate (OCR) profiles of the exercised and control animals measured by Seahorse analyser. AUC1: Area under curve (AUC) of the OCR-time graph of the first six time points; AUC2: AUC of the 7th to 12th time point; AUC3: AUC of the 13th to 18th time point. (D) No significant differences were observed for Basal Respiration (BR), Maximal Respiration (MR) or Spare Respiratory Capacity (SRC) between the exercised and control animals (n = 6 repeats per group; each repeat contains 10 animals). BR = AUC3 – AUC1; MR = AUC2 – AUC3; SRC = AUC2 – AUC1. Experiments in this panel were done one day post-training on day 7 of age.
Figure 6
Figure 6
Sudan Black staining of animals. (A) Representative images of animals stained with Sudan Black from three independent trials with n ≥ 20 animals per group (scale bar = 50 um). (B) Relative Sudan Black staining intensity quantified using ImageJ (One-way ANOVA Sidak’s multiple comparisons post-test analysis ***P < 0.001; n ≥ 20 animals per group). Similar trend was observed in two other trials.
Figure 7
Figure 7
Exercise modulated lipid metabolism in C. elegans. (A) Representative images of control and exercised animals stained with Sudan Black (n ≥ 25 animals per group; scale bar = 200 um). Similar trend was observed in two other trials. (B) Total TAG level was normalized to controls and was significantly lower in the exercised animals than the controls (***P < 0.001; n = 3 repeats per group; each repeat contains approximately 2000 animals collected from different trials). (CG) TAG species profile of the exercised animals normalized to controls (Two-way ANOVA for strain P < 0.001; post-test Sidak’s multiple comparisons analysis *P < 0.05, **P < 0.005, ***P < 0.001; n = 3 repeats per group; each repeat contains approximately 2000 animals collected from different trials). (G) TAG Double Bond Index (DBI) was significantly lower in the exercised animals than the controls (*P < 0.05; n = 3 repeats per group; each repeat contains approximately 2000 animals collected from different trials). (H) TAG Peroxidation Index (PI) was significantly lower in the exercised animals than the controls (*P < 0.05; n = 3 repeats per group; each repeat contains approximately 2000 animals collected from different trials). SFA: Saturated Fatty Acids; MUFA: Mono-unsaturated Fatty Acids, PUFA: Poly-unsaturated Fatty Acids; DB: Double Bond. Experiments in this panel were done immediately after the exercise paradigm on day 6 of age.

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