How do exercise training variables stimulate processes related to mitochondrial biogenesis in slow and fast trout muscle fibres?
exercise training
mitochondria
skeletal muscle
Journal
Experimental physiology
ISSN: 1469-445X
Titre abrégé: Exp Physiol
Pays: England
ID NLM: 9002940
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
29
10
2020
accepted:
27
01
2021
pubmed:
30
1
2021
medline:
1
4
2022
entrez:
29
1
2021
Statut:
ppublish
Résumé
What is the central question of this study? Exercise is known to promote mitochondrial biogenesis in skeletal muscle, but what are the most relevant training protocols to stimulate it? What is the main finding and its importance? As in mammals, training in rainbow trout affects slow and fast muscle fibres differently. Exercise intensity, relative to volume, duration and frequency, is the most relevant training variable to stimulate the processes related to mitochondrial biogenesis in both red and white muscles. This study offers new insights into muscle fibre type-specific transcription and expression of genes involved in mitochondrial adaptations following training. Exercise is known to be a powerful way to improve health through the stimulation of mitochondrial biogenesis in skeletal muscle, which undergoes cellular and molecular adaptations. One of the current challenges in human is to define the optimal training stimulus to improve muscle performance. Fish are relevant models for exercise training physiology studies mainly because of their distinct slow and fast muscle fibres. Using rainbow trout, we investigated the effects of six different training protocols defined by manipulating specific training variables (such as exercise intensity, volume, duration and frequency), on mRNAs and some proteins related to four subsystems (AMP-activated protein kinase-peroxisome proliferator-activated receptor γ coactivator-1α signalling pathway, mitochondrial function, antioxidant defences and lactate dehydrogenase (LDH) metabolism) in both red and white muscles (RM and WM, respectively). In both muscles, high-intensity exercise stimulated more mRNA types and enzymatic activities related to mitochondrial biogenesis than moderate-intensity exercise. For volume, duration and frequency variables, we demonstrated fibre type-specific responses. Indeed, for high-intensity interval training, RM transcript levels are increased by a low training volume, but WM transcript responses are stimulated by a high training volume. Moreover, transcripts and enzymatic activities related to mitochondria and LDH show that WM tends to develop aerobic metabolism with a high training volume. For transcript stimulation, WM requires a greater duration and frequency of exercise than RM, whereas protein adaptations are efficient with a long training duration and a high frequency in both muscles.
Substances chimiques
Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
938-957Informations de copyright
© 2021 The Authors. Experimental Physiology © 2021 The Physiological Society.
Références
Altringham, J. D. & Ellerby, D. J. (1999). Fish swimming: patterns in muscle function. Journal of Experimental Biology, 202, 3397-3403.
Bamman, M. M., Cooper, D. M., Booth, F. W., Chin, E. R., Neufer, P. D., Trappe, S., Lightfoot, J. T., Kraus, W. E. & Joyner, M. J. (2014). Exercise biology and medicine: Innovative research to improve global health. Mayo Clinic Proceedings, 89, 148-153.
Beddow, T. A. & McKinley, R. S. (1999). Importance of electrode positioning in biotelemetry studies estimating muscle activity in fish. Journal of Fish Biology, 54, 819-831.
Bishop, D. J., Botella, J. & Granata, C. (2019). CrossTalk opposing view: Exercise training volume is more important than training intensity to promote increases in mitochondrial content. Journal of Physiology, 597, 4115-4118.
Bishop, D. J., Granata, C. & Eynon, N. (2014). Can we optimise the exercise training prescription to maximise improvements in mitochondria function and content? Biochimica et Biophysica Acta, 1840, 1266-1275.
Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board of Canada, 21, 1183-1226.
Burgetz, I. J., Rojas-Vargas, A., Hinch, S. G. & Randall, D. J. (1998). Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology, 201, 2711-2721.
Castro, V., Grisdale-Helland, B., Helland, S. J., Kristensen, T., Jørgensen, S. M., Helgerud, J., Claireaux, G., Farrell, A. P., Krasnov, A. & Takle, H. (2011). Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar). Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology, 160, 278-290.
Craig, P. M., Moyes, C. D. & LeMoine, C. M. R. (2018). Sensing and responding to energetic stress: evolution of the AMPK network. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology, 224, 156-169.
Davie, P. S., Wells, R. M. G. & Tetens, V. (1986). Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isozymes: Evidence for increased aerobic capacity of white muscle. Journal of Experimental Zoology, 237, 159-171.
Eya, J., Ukwuaba, V., Yossa, R., Gannam, A., Eya, J. C., Ukwuaba, V. O., Yossa, R. & Gannam, A. L. (2015). Interactive effects of dietary lipid and phenotypic feed efficiency on the expression of nuclear and mitochondrial genes involved in the mitochondrial electron transport chain in rainbow trout. International Journal of Molecular Sciences, 16, 7682-7706.
Farrell, A. P. (2008). Comparisons of swimming performance in rainbow trout using constant acceleration and critical swimming speed tests. Journal of Fish Biology, 72, 693-710.
Fiorenza, M., Gunnarsson, T. P., Hostrup, M., Iaia, F. M., Schena, F., Pilegaard, H. & Bangsbo, J. (2018). Metabolic stress-dependent regulation of the mitochondrial biogenic molecular response to high-intensity exercise in human skeletal muscle. Journal of Physiology, 596, 2823-2840.
Gabriel, B. M. & Zierath, J. R. (2017). The limits of exercise physiology: from performance to health. Cell Metabolism, 25, 1000-1011.
Ghiarone, T., Andrade-Souza, V. A., Learsi, S. K., Tomazini, F., Ataide-Silva, T., Sansonio, A., Fernandes, M. P., Saraiva, K. L., Figueiredo, R., Tourneur, Y., Kuang, J., Lima-Silva, A. E. & Bishop, D. J. (2019). Twice-a-day training improves mitochondrial efficiency, but not mitochondrial biogenesis, compared with once-daily training. Journal of Applied Physiology, 127, 713-725.
Gibala, M. J., Little, J. P., MacDonald, M. J. & Hawley, J. A. (2012). Physiological adaptations to low-volume, high-intensity interval training in health and disease. Journal of Physiology, 590, 1077-1084.
Gillen, J. B., Martin, B. J., MacInnis, M. J., Skelly, L. E., Tarnopolsky, M. A. & Gibala, M. J. (2016). Twelve weeks of sprint interval training improves indices of cardiometabolic health similar to traditional endurance training despite a five-fold lower exercise volume and time commitment. PLoS One, 11, e0154075.
Godin, R., Ascah, A. & Daussin, F. N. (2010). Intensity-dependent activation of intracellular signalling pathways in skeletal muscle: role of fibre type recruitment during exercise. Journal of Physiology, 588, 4073-4074.
Granata, C., Jamnick, N. A. & Bishop, D. J. (2018). Training-induced changes in mitochondrial content and respiratory function in human skeletal muscle. Sports Medicine, 48, 1809-1828.
Grundy, D. (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. Experimental Physiology, 100, 755-758.
Gunnarsson, L., Kristiansson, E., Rutgersson, C., Sturve, J., Fick, J., Förlin, L. & Larsson, D. G. J. (2009). Pharmaceutical industry effluent diluted 1:500 affects global gene expression, cytochrome P450 1A activity, and plasma phosphate in fish. Environmental Toxicology and Chemistry, 28, 2639-2647.
He, F., Li, J., Liu, Z., Chuang, C.-C., Yang, W. & Zuo, L. (2016). Redox mechanism of reactive oxygen species in exercise. Frontiers in Physiology, 7, 486.
He, W., Xia, W., Cao, Z.-D. & Fu, S.-J. (2013). The effect of prolonged exercise training on swimming performance and the underlying biochemical mechanisms in juvenile common carp (Cyprinus carpio). Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology, 166, 308-315.
Horii, N., Hasegawa, N., Fujie, S., Uchida, M., Miyamoto-Mikami, E., Hashimoto, T., Tabata, I. & Iemitsu, M. (2017). High-intensity intermittent exercise training with chlorella intake accelerates exercise performance and muscle glycolytic and oxidative capacity in rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 312, R520-R528.
Huertas, J. R., Casuso, R. A., Agustín, P. H. & Cogliati, S. (2019). Stay fit, stay young: mitochondria in movement: the role of exercise in the new mitochondrial paradigm. Oxidative Medicine and Cellular Longevity, 2019, 7058350.
Hvas, M. & Oppedal, F. (2017). Sustained swimming capacity of Atlantic salmon. Aquaculture Environment Interactions, 9, 361-369.
Jäger, S., Handschin, C., St.-Pierre, J. & Spiegelman, B. M. (2007). AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proceedings of the National Academy of Sciences, USA 104, 12017-12022.
Jayne, B. C. & Lauder, G. V. (1994). How swimming fish use slow and fast muscle fibers: implications for models of vertebrate muscle recruitment. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology, 175, 123-131.
Ji, L. L., Kang, C. & Zhang, Y. (2016). Exercise-induced hormesis and skeletal muscle health. Free Radical Biology and Medicine, 98, 113-122.
Ji, L. L. & Zhang, Y. (2014). Antioxidant and anti-inflammatory effects of exercise: role of redox signaling. Free Radical Research, 48, 3-11.
Jones, D. R. (1982). Anaerobic exercise in teleost fish. Canadian Journal of Zoology, 60, 1131-1134.
Karjalainen, J. J., Kiviniemi, A. M., Hautala, A. J., Piira, O.-P., Lepojärvi, E. S., Perkiömäki, J. S., Junttila, M. J., Huikuri, H. V. & Tulppo, M. P. (2015). Effects of physical activity and exercise training on cardiovascular risk in coronary artery disease patients with and without type 2 diabetes. Diabetes Care, 38, 706-715.
Kolditz, C., Borthaire, M., Richard, N., Corraze, G., Panserat, S., Vachot, C., Lefèvre, F. & Médale, F. (2008). Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 294, R1154-R1164.
Kristensen, D. E., Albers, P. H., Prats, C., Baba, O., Birk, J. B. & Wojtaszewski, J. F. P. (2015). Human muscle fibre type-specific regulation of AMPK and downstream targets by exercise. Journal of Physiology, 593, 2053-2069.
Laursen, P. B., Marsh, S. A., Jenkins, D. G. & Coombes, J. S. (2007). Manipulating training intensity and volume in already well-trained rats: effect on skeletal muscle oxidative and glycolytic enzymes and buffering capacity. Applied Physiology, Nutrition and Metabolism, 32, 434-442.
Leary, S. C., Lyons, C. N., Rosenberger, A. G., Ballantyne, J. S., Stillman, J. & Moyes, C. D. (2003). Fiber-type differences in muscle mitochondrial profiles. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 285, R817-R826.
Leek, B. T., Mudaliar, S. R. D., Henry, R., Mathieu-Costello, O. & Richardson, R. S. (2001). Effect of acute exercise on citrate synthase activity in untrained and trained human skeletal muscle. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 280, R441-R447.
LeMoine, C. M. R., Craig, P. M., Dhekney, K., Kim, J. J. & McClelland, G. B. (2010). Temporal and spatial patterns of gene expression in skeletal muscles in response to swim training in adult zebrafish (Danio rerio). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology, 180, 151-160.
Li, X.-M., Pang, X., Zheng, H., Li, X.-J., Fu, S.-J. & Zhang, Y.-G. (2017). Effects of prolonged exercise training and exhaustive chasing training on the swimming performance of an endangered bream Megalobrama pellegrini. Aquatic Biology, 26, 125-135.
Lim, S. T., Kay, R. M. & Bailey, G. S. (1975). Lactate dehydrogenase isozymes of salmonid fish. Evidence for unique and rapid functional divergence of duplicated H-4 lactate dehydrogenases. Journal of Biological Chemistry, 250, 1790-1800.
Lin, J., Handschin, C. & Spiegelman, B. M. (2005). Metabolic control through the PGC-1 family of transcription coactivators. Cell Metabolism, 1, 361-370.
Ljubicic, V., Joseph, A.-M., Saleem, A., Uguccioni, G., Collu-Marchese, M., Lai, R. Y. J., Nguyen, L. M.-D. & Hood, D. A. (2010). Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: Effects of exercise and aging. Biochimica et Biophysica Acta, 1800, 223-234.
MacInnis, M. J. & Gibala, M. J. (2017). Physiological adaptations to interval training and the role of exercise intensity. Journal of Physiology, 595, 2915-2930.
MacInnis, M. J., Skelly, L. E. & Gibala, M. J. (2019). CrossTalk proposal: Exercise training intensity is more important than volume to promote increases in human skeletal muscle mitochondrial content. Journal of Physiology, 597, 4111-4113.
MacInnis, M. J., Zacharewicz, E., Martin, B. J., Haikalis, M. E., Skelly, L. E., Tarnopolsky, M. A., Murphy, R. M. & Gibala, M. J. (2017). Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. Journal of Physiology, 595, 2955-2968.
Magnoni, L. J., Crespo, D., Ibarz, A., Blasco, J., Fernández-Borràs, J. & Planas, J. V. (2013). Effects of sustained swimming on the red and white muscle transcriptome of rainbow trout (Oncorhynchus mykiss) fed a carbohydrate-rich diet. Comparative Biochemistry and Physiology. Part A: Molecular and Integrative Physiology, 166, 510-521.
Magnoni, L. J., Palstra, A. P. & Planas, J. V. (2014). Fueling the engine: induction of AMP-activated protein kinase in trout skeletal muscle by swimming. Journal of Experimental Biology, 217, 1649-1652.
McClelland, G. B. (2012). Muscle remodeling and the exercise physiology of fish. Exercise and Sport Sciences Reviews, 40, 165-173.
McClelland, G. B., Craig, P. M., Dhekney, K. & Dipardo, S. (2006). Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). Journal of Physiology, 577, 739-751.
Miyamoto-Mikami, E., Tsuji, K., Horii, N., Hasegawa, N., Fujie, S., Homma, T., Uchida, M., Hamaoka, T., Kanehisa, H., Tabata, I. & Iemitsu, M. (2018). Gene expression profile of muscle adaptation to high-intensity intermittent exercise training in young men. Scientific Reports, 8, 16811.
Morash, A. J., Vanderveken, M. & McClelland, G. B. (2014). Muscle metabolic remodeling in response to endurance exercise in salmonids. Frontiers in Physiology, 5, 452.
Olesen, J., Kiilerich, K. & Pilegaard, H. (2010). PGC-1α-mediated adaptations in skeletal muscle. Pflugers Archiv European Journal of Physiology, 460, 153-162.
Pengam, M., Moisan, C., Simon, B., Guernec, A., Inizan, M. & Amérand, A. (2020). Training protocols differently affect AMPK-PGC-1α signaling pathway and redox state in trout muscle. Comparative Biochemistry and Physiology. Part A: Molecular and Integrative Physiology, 243, 110673.
Perry, C. G. R., Lally, J., Holloway, G. P., Heigenhauser, G. J. F., Bonen, A. & Spriet, L. L. (2010). Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. Journal of Physiology, 588, 4795-4810.
Powers, S. K. & Jackson, M. J. (2008). Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiological Reviews, 88, 1243-1276.
Richards, J. C., Johnson, T. K., Kuzma, J. N., Lonac, M. C., Schweder, M. M., Voyles, W. F. & Bell, C. (2011). Short-term sprint interval training increases insulin sensitivity in healthy adults but does not affect the thermogenic response to β-adrenergic stimulation. Experimental Physiology, 588, 2961-2972.
Stavrinou, P. S., Bogdanis, G. C., Giannaki, C. D., Terzis, G. & Hadjicharalambous, M. (2018). High-intensity interval training frequency: cardiometabolic effects and quality of life. International Journal of Sports Medicine, 39, 210-217.
Steinbacher, P. & Eckl, P. (2015). Impact of oxidative stress on exercising skeletal muscle. Biomolecules, 5, 356-377.
Stickland, N. C. (1983). Growth and development of muscle fibres in the rainbow trout (Salmo gairdneri). Journal of Anatomy, 137, 323-333.
Trewin, A. J., Berry, B. J. & Wojtovich, A. P. (2018). Exercise and mitochondrial dynamics: keeping in shape with ROS and AMPK. Antioxidants, 7, 7.
Tudorache, C., de Boeck, G. & Claireaux, G. (2013). Forced and preferred swimming speeds of fish: A methodological approach. In Swimming Physiology of Fish: Towards Using Exercise to Farm a Fit Fish in Sustainable Aquaculture, ed. Palstra AP & Planas JV, pp. 81-108.Springer, Berlin, Heidelberg.
Westermann, B. (2010). Mitochondrial fusion and fission in cell life and death. Nature Reviews. Molecular Cell Biology, 11, 872-884.
Wieser, W., Lackner, R., Hinterleitner, S. & Platzer, U. (1987). Distribution and properties of lactate dehydrogenase isoenzymes in red and white muscle of freshwater fish. Fish Physiology and Biochemistry, 3, 151-162.