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Cortisol acting through the glucocorticoid receptor is not responsible for exercise-enhanced growth but does affect the white skeletal muscle transcriptome in zebrafish (Danio rerio)

ABSTRACT: Forced sustained swimming exercise at optimal speed enhances growth in many fish species, particularly through hypertrophy of the white skeletal muscle. The exact mechanism of this effect has not been resolved yet. To explore the mechanism, we first subjected wild-type zebrafish to an exercise protocol validated for exercise-enhanced growth, and showed that exercised zebrafish, which indeed showed enhanced growth, had higher cortisol levels than the non-exercised controls. A central role was therefore hypothesized for the steroid hormone cortisol acting through the Glucocorticoid receptor (Gr). Second, we subjected wild-type zebrafish and zebrafish with a mutant Gr to exercise at optimal, suboptimal and super-optimal speeds and compared them with non-exercised controls. Exercised zebrafish showed growth enhancement at all speeds, with highest growth at optimal speeds. In the Gr mutant fish, exercise resulted in growth enhancement similar to wild-type zebrafish, indicating that cortisol cannot be considered as a main determinant of exercise-enhanced growth. Finally, the transcriptome of white skeletal muscle tissue was analysed by RNA sequencing. The results of this analysis showed that in the muscle tissue of Gr mutant fish a lower number of genes is regulated by exercise than in wild-type fish (183 versus 351). A cluster of 36 genes was regulated by exercise in both wild-type and mutant fish. In this cluster, genes involved in transcriptional regulation and protein ubiquitination were overrepresented. Since growth was enhanced similarly in both wild-type fish and mutants, these processes may play an important role in exercise-enhanced growth.

ORGANISM(S): Danio rerio

PROVIDER: GSE120253 | GEO | 2019/02/05

REPOSITORIES: GEO

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Project description:The adult skeletal muscle is a plastic tissue with a remarkable ability to adapt to different levels of activity by altering its excitability, its contractile and metabolic phenotype and its mass. Knowledge on the mechanisms responsible for muscle mass comes primarily from models of muscle inactivity or denervation or from genetic models of muscle diseases. Given that the underlying exercise-induced transcriptional mechanisms regulating muscle mass are not fully understood, here we investigated the cellular and molecular adaptive mechanisms taking place in fast skeletal muscle of adult zebrafish in response to swimming. Fish were trained at low swimming speed (0.1 m/s; non-exercised) or at their optimal swimming speed (0.4 m/s; exercised). A significant increase in fibre cross-sectional area (1,290 M-BM-1 88 vs. 1,665 M-BM-1 106 M-NM-<m2) and vascularization (298 M-BM-1 23 vs. 458 M-BM-1 38 capillaries/mm2) was found in exercised over non-exercised fish. Gene expression profiling evidenced the transcriptional activation of a series of complex networks of extracellular and intracellular signaling molecules and pathways involved in the regulation of muscle mass, myogenesis and angiogenesis, many (e.g. BMP, TGFM-oM-^AM-", FGF, Notch, Wnt, MEF2, Shh, EphrinB2) not previously associated with exercise-induced contractile activity, and that recapitulate in part the transcriptional events occurring during skeletal muscle regeneration. These results demonstrate that fibre hypertrophy is responsible for the growth-promoting effects of exercise accompanied by a switch to a more oxidative capacity of white muscle fibres to fuel the increased energy demands. Importantly, our study identified novel molecular mechanisms regulating muscle mass and function in vertebrates. Adult zebrafish were subjected or not to a swim training regime consisting of swimming at the optimal swimming speed for this species for 6 h/day, 5 days/week for a total of 4 weeks (20 experimental days). Total RNA of fast muscle from individual non-exercised (n = 8) and exercised (n = 8) zebrafish was analyzed.

Project description:A longer on-land rearing period of Gilthead seabream Sparus aurata before transfer to sea-cages would allow the farmer to benefit from exercise-enhanced growth and resilience as induced by increasing water flow in the tanks. In this study, the physiological effects of flow-conditioning were investigated by subjecting large groups of experimental fish to minimal flow or to flow regimes inducing swimming exercise at 1 or 2 Body Length (BL) s-1 for a period of 8 months (Feb.-Oct.) in 1,500 l RAS tanks. Fish size after eight months of flow conditioning was 92 ± 27 g body weight (BW) for fish under minimal flow; 106 ± 24 g BW (+15%) at 1 BL s-1, and 125 ± 27 g BW (+36%) at 2 BL s-1. Although flow enhanced growth linearly with swimming speed, the number of malformed fish was significantly higher for swimming at 2 BL s-1 indicating that the mechanical load imposed by exercise was too high for a developing juvenile. Fish representing the three treatment groups were then used for: (1) a stress challenge netting test and plasma cortisol measurement (baseline, peaking and recovery levels); (2) blood plasma measurements of glucose, triglycerides, lactate, cholesterol, growth hormone (GH) and insulin-like growth factor I (IGF-I), and heart and muscle gene expression of the GH and IGF-I receptors and the muscle transcriptome by deep RNA sequencing (RNAseq). Flow conditioning at 1 BL s-1 provided optimal conditions for growth and stress coping without energetic depletion and morphological deformation. The absence of important differences in plasma GH and IGF-I, and expression levels of the receptors in heart and white skeletal muscle, indicated that other factors may be involved in growth enhancement. RNAseq of the white skeletal muscle showed that transcription regulators play an important role. Also expression of immune genes is strongly up-regulated. Whereas muscle of fish conditioned at 1 BL s-1 shows up-regulated expression of structural genes such as troponins and myosins, muscle of fish conditioned at 2 BL s-1 shows up-regulated expression of skeletal genes instead which may reflect the mechanism behind morphological deformations.

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Cortisol acting through the glucocorticoid receptor is not responsible for exercise-enhanced growth but does affect the white skeletal muscle transcriptome in zebrafish (Danio rerio)

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