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Melatonin and Exercise Counteract Sarcopenic Obesity through Preservation of Satellite Cell Function.

ABSTRACT: Sarcopenic obesity (SO) is characterized by atrophic skeletal muscle impairment (sarcopenia) and obesity, which is associated with adverse outcomes of morbidity and mortality in elderly people. We investigated the effects of melatonin and exercise training on SO in 32-week-old senescence-accelerated mouse-prone-8 (SAMP8) mice fed a normal diet or a high-fat diet for 16 weeks. Melatonin, exercise, or melatonin and exercise for 8 weeks displayed reductions in the SO-induced impairment of skeletal muscle function and atrophy. Specifically, a decrease in mitochondrial calcium retention capacity in skeletal muscles observed in the HFD-con group was attenuated in melatonin and/or exercise intervention groups. More importantly, HFD-con mice displayed a lower number of Pax7+ satellite cells (SCs) and higher expression of p16^ink than P8ND mice, which were attenuated by melatonin and/or exercise interventions. The cellular senescence in SC-derived primary myoblasts from HFD-con mice was significantly attenuated in myoblasts from the melatonin and/or exercise groups, which was reproduced in a senescence model of H₂O₂-treated C2C12 myoblasts. Our results suggest that melatonin and exercise training attenuate SO-induced skeletal muscle dysfunction, at least in part, through preserving the SC pool by inhibiting cellular senescence and attenuating mitochondrial dysfunction.

SUBMITTER: Mankhong S

PROVIDER: S-EPMC10094434 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Melatonin and Exercise Counteract Sarcopenic Obesity through Preservation of Satellite Cell Function.

Mankhong Sakulrat S Kim Sujin S Moon Sohee S Lee Jae-Seon JS Cho Eun-Jeong EJ Kwak Hyo-Bum HB Park Dong-Ho DH Ryu Ji-Kan JK Kang Ju-Hee JH

International journal of molecular sciences 20230323 7

Sarcopenic obesity (SO) is characterized by atrophic skeletal muscle impairment (sarcopenia) and obesity, which is associated with adverse outcomes of morbidity and mortality in elderly people. We investigated the effects of melatonin and exercise training on SO in 32-week-old senescence-accelerated mouse-prone-8 (SAMP8) mice fed a normal diet or a high-fat diet for 16 weeks. Melatonin, exercise, or melatonin and exercise for 8 weeks displayed reductions in the SO-induced impairment of skeletal ...[more]

PMID: 37047070

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Project description:BackgroundSarcopenia is characterized by the loss of skeletal muscle mass and muscle function with increasing age. The skeletal muscle mass of older people who endure sarcopenia may be improved via the practice of strength training and tai chi. However, it remains unclear if the hybridization of strength exercise training and traditional Chinese exercise will have a better effect.ObjectiveWe designed a strength training and tai chi exercise hybrid program to improve sarcopenia in older people. Moreover, explainable artificial intelligence was used to predict postintervention sarcopenic status and quantify the feature contribution.MethodsTo assess the influence of sarcopenia in the older people group, 93 participated as experimental participants in a 24-week randomized controlled trial and were randomized into 3 intervention groups, namely the tai chi exercise and strength training hybrid group (TCSG; n=33), the strength training group (STG; n=30), and the control group (n=30). Abdominal computed tomography was used to evaluate the skeletal muscle mass at the third lumbar (L3) vertebra. Analysis of demographic characteristics of participants at baseline used 1-way ANOVA and χ2 tests, and repeated-measures ANOVA was used to analyze experimental data. In addition, 10 machine-learning classification models were used to calculate if these participants could reverse the degree of sarcopenia after the intervention.ResultsA significant interaction effect was found in skeletal muscle density at the L3 vertebra, skeletal muscle area at the L3 vertebra (L3 SMA), grip strength, muscle fat infiltration, and relative skeletal muscle mass index (all P values were <.05). Grip strength, relative skeletal muscle mass index, and L3 SMA were significantly improved after the intervention for participants in the TCSG and STG (all P values were <.05). After post hoc tests, we found that participants in the TCSG experienced a better effect on L3 SMA than those in the STG and participants in the control group. The LightGBM classification model had the greatest performance in accuracy (88.4%), recall score (74%), and F1-score (76.1%).ConclusionsThe skeletal muscle area of older adults with sarcopenia may be improved by a hybrid exercise program composed of strength training and tai chi. In addition, we identified that the LightGBM classification model had the best performance to predict the reversion of sarcopenia.

Project description:BackgroundSkeletal muscle remodelling can cause clinically important changes in muscle phenotypes. Satellite cells (SCs) myogenic potential underlies the maintenance of muscle plasticity. Accumulating evidence shows the importance of succinate in muscle metabolism and function. However, whether succinate can affect SC function and subsequently coordinate muscle remodelling to exercise remains unexplored.MethodsA mouse model of high-intensity interval training (HIIT) was used to investigate the effects of succinate on muscle remodelling and SC function by exercise capacity test and biochemical methods. Mice with succinate receptor 1 (SUCNR1)-specific knockout in SCs were generated as an in vivo model to explore the underlying mechanisms. RNA sequencing of isolated SCs was performed to identify molecular changes responding to succinate-SUCNR1 signalling. The effects of identified key molecules on the myogenic capacity of SCs were investigated using gain- and loss-of-function assays in vitro. To support the translational application, the clinical efficacy of succinate was explored in muscle-wasting mice.ResultsAfter 21 days of HIIT, mice supplemented with 1.5% succinate exhibited striking gains in grip strength (+0.38 ± 0.04 vs. 0.26 ± 0.03 N, p < 0.001) and endurance (+276.70 ± 55.80 vs. 201.70 ± 45.31 s, p < 0.05), accompanied by enhanced muscle hypertrophy and neuromuscular junction regeneration (p < 0.001). The myogenic capacity of SCs was significantly increased in gastrocnemius muscle of mice supplemented with 1% and 1.5% succinate (+16.48% vs. control, p = 0.008; +47.25% vs. control, p < 0.001, respectively). SUCNR1-specific deletion in SCs abolished the modulatory influence of succinate on muscle adaptation in response to exercise, revealing that SCs respond to succinate-SUCNR1 signalling, thereby facilitating muscle remodelling. SUCNR1 signalling markedly upregulated genes associated with stem cell differentiation and phosphorylation pathways within SCs, of which p38α mitogen-activated protein kinase (MAPK; fold change = 6.7, p < 0.001) and protein kinase C eta (PKCη; fold change = 12.5, p < 0.001) expressions were the most enriched, respectively. Mechanistically, succinate enhanced the myogenic capacity of isolated SCs by activating the SUCNR1-PKCη-p38α MAPK pathway. Finally, succinate promoted SC differentiation (1.5-fold, p < 0.001), ameliorating dexamethasone-induced muscle atrophy in mice (p < 0.001).ConclusionsOur findings reveal a novel function of succinate in enhancing SC myogenic capacity via SUCNR1, leading to enhanced muscle adaptation in response to exercise. These findings provide new insights for developing pharmacological strategies to overcome muscle atrophy-related diseases.

Dataset Information

Melatonin and Exercise Counteract Sarcopenic Obesity through Preservation of Satellite Cell Function.

Publications

Melatonin and Exercise Counteract Sarcopenic Obesity through Preservation of Satellite Cell Function.

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