Endurance exercise and selective breeding for longevity extend Drosophila healthspan by overlapping mechanisms

Sujkowski, Alyson; Bazzell, Brian; Carpenter, Kylie; Arking, Robert; Wessells, Robert

doi:10.18632/aging.100789

Cited by 58 publications

(99 citation statements)

References 89 publications

(106 reference statements)

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“…In mammalian exercise systems, carbohydrate sources have been shown to be preserved during the recovery period [68]. Interestingly, downregulation of carbohydrate metabolism has also been reported in Drosophila following endurance exercise [6], pointing to a conserved exercise-dependent metabolic response in invertebrate and vertebrate models. Glucose and lipid contributions to the energy expended during physical exercise vary widely depending on the exercise duration and intensity.…”

Section: Discussionmentioning

confidence: 99%

“…Importantly, powerful exercise training paradigms based on climbing activity have been described in Drosophila [4, 5]. Exercise adaptations in flies include improvements in mobility and cardiac performance, increased mitochondrial activity and quality, and increased lipolysis [4–6]. Although these studies support that exercise benefits are conserved from invertebrates to humans, the area of invertebrate exercise genetics remains strikingly underdeveloped.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2017

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BackgroundExercise 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.ResultsHere, 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.ConclusionsIn 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 materialThe 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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2017

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“…Endurance training improves the healthy function of multiple organ systems including skeletal muscle, heart and brain (Bostrom et al, 2013). These functional improvements are associated with conserved shifts in metabolism (Booth et al, 2015) and changes in gene expression in both vertebrate models (Coffey and Hawley, 2007) and Drosophila (Sujkowski et al, 2015). …”

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confidence: 99%

“…We have previously described an endurance training paradigm for Drosophila that uses reiterated induction of negative geotaxis to allow controlled, daily training of fruit fly cohorts (Tinkerhess et al, 2012a). Following a three-week period of ramped endurance exercise activity, wild-type male flies display increased climbing speed (Piazza et al, 2009), endurance (Tinkerhess et al, 2012b), cardiac performance (Piazza et al, 2009; Sujkowski et al, 2012), flight (Sujkowski et al, 2015), and mitochondrial enzyme activity (Piazza et al, 2009). Furthermore, endurance training increases mitochondrial number and reduces accumulated oxidative stress in fly cardiac muscle (Laker et al, 2014).…”

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confidence: 99%

“…Exercise also induces consumption of accumulated fat stores in flies with excess lipid (Sujkowski et al, 2012). Finally, exercised male Drosophila exhibit healthspan-associated changes in gene expression, including upregulation of stress defense genes (Sujkowski et al, 2015). Taken together, these observations support the idea that endurance training in Drosophila induces similar effects as training in humans (Gaman et al, 2011) and vertebrate models (Fluck, 2006), and reinforce the concept of exercise training as a conserved hormetic intervention.…”

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confidence: 99%

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Octopamine Drives Endurance Exercise Adaptations in Drosophila

et al. 2017

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Summary Endurance exercise is an effective therapeutic intervention with substantial pro-healthspan effects. Male Drosophila respond to a ramped daily program of exercise by inducing conserved physiological responses similar to those seen in mice and humans. Female flies respond to an exercise stimulus, but do not experience the adaptive training response seen in males. Here, we use female flies as a model to demonstrate that differences in exercise response are mediated by differences in neuronal activity. The activity of octopaminergic neurons is specifically required to induce the conserved cellular and physiological changes seen following endurance training. Furthermore, either intermittent, scheduled activation of octopaminergic neurons, or octopamine feeding, is able to fully substitute for exercise, conferring a suite of pro-healthspan benefits to sedentary Drosophila. These experiments indicate that octopamine is a critical mediator of adaptation to endurance exercise in Drosophila.

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Endurance exercise and selective breeding for longevity extend Drosophila healthspan by overlapping mechanisms

Cited by 58 publications

References 89 publications

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

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

Octopamine Drives Endurance Exercise Adaptations in Drosophila

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