Exploring the effect of exercise on the transcriptome of zebrafish larvae (Danio rerio)

Abstract

SummaryIn adult vertebrates, endurance training leads to physiological, metabolical and molecular adaptations which improve endurance performance. Only very few studies have focused on adaptive responses to endurance training during early vertebrate development, and molecular data is limited. Here, we explored the effect of swim-training on the transcriptome of the zebrafish during early development on a quantitative and spatial gene expression level. We subjected larval zebrafish from 5 to 14 dpf (days post fertilization) to swim-training and performed a whole genome microarray analysis of trained and control fish sampled at 10 dpf. In addition, we investigated if swim-training affected the expression of genes involved in muscle growth and structure with quantitative real-time PCR in trained and control fish sampled at 5 and 14 dpf. To obtain a general overview of the effects of swimtraining on the transcriptome, we selected 52 genes from the whole genome microarray analysis based on a number of criteria. In situ hybridization demonstrated that 15 genes were specifically expressed in the brain, muscle, kidneys, liver, pancreas or intestines. Thus, swim-training led to molecular changes already after 6 days of swim-training and in a variety of organ systems. In addition, the expression of slow fiber markers was increased after 10 days of swim-training, indicating that muscle can already shift towards a slow aerobic phenotype during zebrafish larval development. Taken together, this study demonstrates that significant changes occur, even at early stages, as an adaptive response to endurance training during early vertebrate development.

An overview on the teleost bone mechanophysiology

“…The transduction of mechanical signals through the canaliculi network of the teleost cellular bone is not well understood and underlying mechanisms have not yet been proven to be comparable to those in mammalian or avian bone (Fiaz et al., ). Despite being different in respect to the occurrence of osteocytes, both acellular and cellular teleost bones are capable of responding to mechanical changes and adapt accordingly (Aceto et al., ; Cardeira, Bensimon‐Brito, Pousão‐Ferreira, Cancela, & Gavaia, ; Cardeira, Mendes, Pousão‐Ferreira, Cancela, & Gavaia, ; Chatani et al., ; Fiaz et al., ; Fiaz, Léon‐Kloosterziel, et al., ; Gorman, Handrigan, Jin, Wallis, & Breden, ; Kihara, Ogata, Kawano, Kubota, & Yamaguchi, ; Kitamura et al., ; Kranenbarg, van Cleynenbreugel, Schipper, & van Leeuwen, ; Kranenbarg, Waarsing, Muller, Weinans, & van Leeuwen, ; Owen, Eynon, Woodgate, Davies, & Fox, ; Suzuki et al., ; Totland et al., ; Witten, Gil‐Martens, Hall, Huysseune, & Obach, ; Yano et al., ; Ytteborg, Torgersen, Baeverfjord, & Takle, ; Ytteborg et al., ). It is thus clear that the teleost bone holds a functional mechanosensing system, in which osteocytes (at least for the acellular bone) do not play a central role.…”

“…Exercise is long known to impact a variety of biological systems due to its mechanical action on cells and tissues. While the wheel‐running model is probably the most classical system used to exercise mammalian models, such as the mouse and rat (Allen et al., ), swim training has been widely used to exercise teleost models, such as zebrafish (Bagatto, Pelster, & Burggren, ; Fiaz et al., ; Fiaz, Léon‐Kloosterziel, et al., ; McClelland, Craig, Dhekney, & Dipardo, ; van der Meulen et al., ; Palstra et al., ). Swimming exercise increases the mechanical loading on bone structures, by increasing hydrodynamic forces and by directly affecting muscle activity.…”

“…Among teleosts, the zebrafish (Danio rerio). and the Japanese medaka (Oryzias latipes) medaka) are prominent biomedical models for studying bone mechanobiology, including the impacts of microgravity and swimming activity (Chatani et al, 2015(Chatani et al, , 2016Fiaz et al, 2012;Fiaz, Léeon-Kloosterziel, van Leeuwen, & Kranenbarg, 2014;Fiaz, Léon-Kloosterziel, van Leeuwen, & Kranenbarg, 2014;Renn, Winkler, Schartl, Fischer, & Goerlich, 2006). Accordingly, the fraction of corresponding scientific production including zebrafish and teleost bone has increased greatly since the 1980s (Figure 1a…”

Fish is Fish: the use of experimental model species to reveal causes of skeletal diversity in evolution and disease

“…Because of the experimental accessibility and large numbers of offspring stemming from a single cross, zebrafish and medaka provide an experimental capability to analyze mechanisms underlying disease states. One area of research has centered on skeletogenesis and the causes of skull malformations, osteoporosis, defects of osteoblasts and osteoclasts, verbal fusion, and pathological ectopic ossification Bensimon‐Brito et al., ,b; Cooper et al., ; Kaplan et al., ; To et al., ; Vanoevelen et al., ; Willems et al., ; Gibbs et al., ; Fiaz et al., ). Given an available disease model in a fish, the altered developmental and physiological mechanisms underlying the observed pathology can be investigated and potential therapeutic strategies can then be tested for efficacy.…”

Fish skeletal biology and beyond

“…Aquaculture and human medicine aim for a healthy skeleton and largely explore epigenetic factors to improve skeletal quality. The importance of phenotypic plasticity for evolution and speciation is reviewed in the first section of this volume (Gunter and Meyer, ) and addressed by several authors in the third section (Fiaz et al., ,b; Fleming et al., ; Lajus et al., ; Torres‐Núñez et al., ; Yurtseva et al., ). Section four, ‘Development and Malformations’, reports about recent data aiming at improving our understanding of fish skeletal pathology, a prerequisite to ensure healthy skeletal development of farmed fish.…”