{"title":"Systemic effect of combined functional overload and endurance-type swimming exercise on whole body metabolism in mice.","authors":"Takanaga Shirai, Kazuki Uemichi, Ryoto Iwai, Hayato Shinkai, Tomohiro Iwata, Riku Tanimura, Shunsuke Sugiyama, Tohru Takemasa","doi":"10.1152/ajpendo.00433.2024","DOIUrl":null,"url":null,"abstract":"<p><p>In this study, we examined the effects of concurrent functional overload and endurance exercise on muscle hypertrophy, mitochondrial function, and systemic adaptations in male mice. The mice were assigned to three groups: Sham (Sham), overload-induced hypertrophy (OL), and overload with concurrent 60-min free swimming (5 times/wk) (OL + Swim), for 4 wk. Although OL promoted muscle hypertrophy and protein synthesis through the Akt/mammalian/mechanistic target of rapamycin (mTOR) signaling pathway, the addition of swimming (OL + Swim) attenuated these effects, resulting in less pronounced muscle growth and a smaller increase in myofiber cross-sectional area. Notably, the OL + Swim group exhibited enhanced mitochondrial activity and glycogen content compared with the OL group. Both the OL and OL + Swim groups showed elevated rates of protein synthesis, with a significant upregulation of AMP-activated kinase (AMPK) and peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α) in the OL + Swim group, suggesting enhanced mitochondrial biogenesis and adaptation. Concurrent training also resulted in systemic benefits, including reduced inguinal and epididymal white adipocyte size, improved mitochondrial enzyme activities in adipose and liver tissues, and higher levels of fibronectin type III domain containing protein 5 (FNDC5), fibroblast growth factor 21 (FGF21), and brain-derived neurotrophic factor (BDNF) in serum, which contributed to enhanced muscle protein synthesis in cultured muscle cells. These results highlight the trade-offs between muscle hypertrophy and metabolic health in mice and underscore the importance of balanced training regimens to optimize overall metabolic health and muscle function. Our results provide further insight into how concurrent strength and endurance training can be optimized for health and performance benefits.<b>NEW & NOTEWORTHY</b> This study provides novel insights into the mechanisms underlying the interference effect that occurs in concurrent training, highlighting the potential systemic benefits of combining resistance and endurance exercises. Despite a reduction in muscle hypertrophy, concurrent training enhances metabolic adaptations and systemic health markers and offers a comprehensive approach to improving both muscle and metabolic fitness.</p>","PeriodicalId":7594,"journal":{"name":"American journal of physiology. Endocrinology and metabolism","volume":"328 5","pages":"E695-E710"},"PeriodicalIF":3.1000,"publicationDate":"2025-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"American journal of physiology. Endocrinology and metabolism","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1152/ajpendo.00433.2024","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/4/18 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"ENDOCRINOLOGY & METABOLISM","Score":null,"Total":0}
引用次数: 0
Abstract
In this study, we examined the effects of concurrent functional overload and endurance exercise on muscle hypertrophy, mitochondrial function, and systemic adaptations in male mice. The mice were assigned to three groups: Sham (Sham), overload-induced hypertrophy (OL), and overload with concurrent 60-min free swimming (5 times/wk) (OL + Swim), for 4 wk. Although OL promoted muscle hypertrophy and protein synthesis through the Akt/mammalian/mechanistic target of rapamycin (mTOR) signaling pathway, the addition of swimming (OL + Swim) attenuated these effects, resulting in less pronounced muscle growth and a smaller increase in myofiber cross-sectional area. Notably, the OL + Swim group exhibited enhanced mitochondrial activity and glycogen content compared with the OL group. Both the OL and OL + Swim groups showed elevated rates of protein synthesis, with a significant upregulation of AMP-activated kinase (AMPK) and peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α) in the OL + Swim group, suggesting enhanced mitochondrial biogenesis and adaptation. Concurrent training also resulted in systemic benefits, including reduced inguinal and epididymal white adipocyte size, improved mitochondrial enzyme activities in adipose and liver tissues, and higher levels of fibronectin type III domain containing protein 5 (FNDC5), fibroblast growth factor 21 (FGF21), and brain-derived neurotrophic factor (BDNF) in serum, which contributed to enhanced muscle protein synthesis in cultured muscle cells. These results highlight the trade-offs between muscle hypertrophy and metabolic health in mice and underscore the importance of balanced training regimens to optimize overall metabolic health and muscle function. Our results provide further insight into how concurrent strength and endurance training can be optimized for health and performance benefits.NEW & NOTEWORTHY This study provides novel insights into the mechanisms underlying the interference effect that occurs in concurrent training, highlighting the potential systemic benefits of combining resistance and endurance exercises. Despite a reduction in muscle hypertrophy, concurrent training enhances metabolic adaptations and systemic health markers and offers a comprehensive approach to improving both muscle and metabolic fitness.
期刊介绍:
The American Journal of Physiology-Endocrinology and Metabolism publishes original, mechanistic studies on the physiology of endocrine and metabolic systems. Physiological, cellular, and molecular studies in whole animals or humans will be considered. Specific themes include, but are not limited to, mechanisms of hormone and growth factor action; hormonal and nutritional regulation of metabolism, inflammation, microbiome and energy balance; integrative organ cross talk; paracrine and autocrine control of endocrine cells; function and activation of hormone receptors; endocrine or metabolic control of channels, transporters, and membrane function; temporal analysis of hormone secretion and metabolism; and mathematical/kinetic modeling of metabolism. Novel molecular, immunological, or biophysical studies of hormone action are also welcome.