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Physiological Responses to Swimming-Induced Exercise in the Adult Zebrafish Regenerating Heart.

ABSTRACT: Exercise promotes a set of physiological responses known to provide long-term health benefits and it can play an important role in cardioprotection. In the present study, we examined cardiac responses to exercise training in the adult zebrafish and in the context of cardiac regeneration. We found that swimming-induced exercise increased cardiomyocyte proliferation and that this response was also found under regenerating conditions, when exercise was performed either prior to and after ventricular cryoinjury (CI). Exercise prior to CI resulted in a mild improvement in cardiac function and lesion recovery over the non-exercise condition. Transcriptomic profiling of regenerating ventricles in cryoinjured fish subjected to exercise identified genes possibly involved in the cardioprotective effects of exercise and that could represent potential targets for heart regeneration strategies. Taken together, our results suggest that exercise constitutes a physiological stimulus that may help promote cardiomyogenic mechanisms of the vertebrate heart through the induction of cardiomyocyte proliferation. The zebrafish exercise model may be useful for investigating the potential cardioprotective effects of exercise in teleost fish and to contribute to further identify and develop novel avenues in basic research to promote heart regeneration.

SUBMITTER: Rovira M

PROVIDER: S-EPMC6174316 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Physiological Responses to Swimming-Induced Exercise in the Adult Zebrafish Regenerating Heart.

Rovira Mireia M Borràs Daniel M DM Marques Inês J IJ Puig Carolina C Planas Josep V JV

Frontiers in physiology 20181001

Exercise promotes a set of physiological responses known to provide long-term health benefits and it can play an important role in cardioprotection. In the present study, we examined cardiac responses to exercise training in the adult zebrafish and in the context of cardiac regeneration. We found that swimming-induced exercise increased cardiomyocyte proliferation and that this response was also found under regenerating conditions, when exercise was performed either prior to and after ventricula ...[more]

PMID: 30327615

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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.

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, resilience, and robustness 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 (February-October) in 1,500 L tanks. 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 1 (IGF1), and (3) heart and muscle gene expression of the GH and IGF1 receptors and the muscle transcriptome by deep RNA sequencing (RNAseq). Fish size after 8 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. Flow conditioning at 1 BL s-1 provided optimal conditions for growth and uniformity, but also stress (lowest baseline plasma cortisol), robustness (higher condition factor and larger hearts), and energy mobilization (increased plasma glucose). Although flow enhanced growth linearly with swimming speed, also the percentage of lordotic fish increased with exercise, particularly high for swimming at 2 BL s-1. The absence of important differences in plasma GH and IGF1, and expression levels of their receptors in heart and white skeletal muscle, indicated that other factors may be involved in growth enhancement. RNAseq of the white skeletal muscle showed upregulated expression of genes involved in muscle contraction, muscle development and its molecular regulation, and immune genes that may play a role in the muscle repair mechanism. An exercise regime of swimming at 1 BL s-1 can be considered as optimal for farming robust seabream although the increase of skeletal deformities should be avoided.

Project description:BACKGROUND: 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. We previously reported on the potential of adult zebrafish as a tractable experimental model for exercise physiology, established its optimal swimming speed and showed that swimming-induced contractile activity potentiated somatic growth. Given that the underlying exercise-induced transcriptional mechanisms regulating muscle mass in vertebrates 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. RESULTS: 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±88 vs. 1.665±106 ?m2) and vascularization (298±23 vs. 458±38 capillaries/mm2) was found in exercised over non-exercised fish. Gene expression profiling by microarray analysis evidenced the activation of a series of complex transcriptional networks of extracellular and intracellular signaling molecules and pathways involved in the regulation of muscle mass (e.g. IGF-1/PI3K/mTOR, BMP, MSTN), myogenesis and satellite cell activation (e.g. PAX3, FGF, Notch, Wnt, MEF2, Hh, EphrinB2) and angiogenesis (e.g. VEGF, HIF, Notch, EphrinB2, KLF2), some of which had not been previously associated with exercise-induced contractile activity. CONCLUSIONS: The results from the present study show that exercise-induced contractile activity in adult zebrafish promotes a coordinated adaptive response in fast muscle that leads to increased muscle mass by hypertrophy and increased vascularization by angiogenesis. We propose that these phenotypic adaptations are the result of extensive transcriptional changes induced by exercise. Analysis of the transcriptional networks that are activated in response to exercise in the adult zebrafish fast muscle resulted in the identification of key signaling pathways and factors for the regulation of skeletal muscle mass, myogenesis and angiogenesis that have been remarkably conserved during evolution from fish to mammals. These results further support the validity of the adult zebrafish as an exercise model to decipher the complex molecular and cellular mechanisms governing skeletal muscle mass and function in vertebrates.

Dataset Information

Physiological Responses to Swimming-Induced Exercise in the Adult Zebrafish Regenerating Heart.

Publications

Physiological Responses to Swimming-Induced Exercise in the Adult Zebrafish Regenerating Heart.

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