The effect of 8 weeks of resistance training on muscle function and some proteins related to sarcopenia in soleus muscle of obese aged male rats

Document Type : Research Paper I Open Access I Released under (CC BY-NC 4.0) license

Authors

1 PhD student of exercise physiology, Faculty of Physical Education and Sport Sciences, University of Tehran, Tehran, Iran.

2 Associate Professor of Exercise Physiology Department, Faculty of Physical Education and Sport Sciences, University of Tehran, Tehran, Iran.

3 Assistant Professor, Department of Exercise Physiology, Faculty of Physical Education and Sport Sciences, University of Tehran , Tehran, Iran.

Abstract

Aim:   Resistance training is one of the most effective methods to reduce fat tissue and   prevention of reducing muscle mass and strength loss (sarcopenia). The aim of this study was to investigate the effect of 8 weeks of resistance training on protein amounts of FOXO3, Murf1 and Atrogin-1 and also muscle strength of obese aged male rats. Method: Out of 30 Wistar male rats (age: 15 months and weight: 320 to 350 grams), 10 were separated as control group and the rest became obese under a high-fat diet for 12 weeks.  Then the obese rats (with Lee index higher than 310) were divided into two groups: obese control and resistance training. The resistance training group performed training program (ladder-climbing) for 8 weeks, 3 sessions per week (3 sets of 8 reps with %25, %50, %75 and %100 of body weight). The amounts of FOXO3, Murf1 and Arogin-1 proteins were measured by ELISA method in soleus muscle. muscle strength was also measured by forelimb grip strength test. The levels of protein were analyzed using ANOVA and Tukey and muscle strength were analyzed with ANCOVA and Bonferroni post hoc test. Results: Compared to the control group, obesity increased FOXO3, Murf1 and Arogin-1 proteins (p=0.000) and decreased muscle strength (p=0.000) in the obese control group. on the other hand, resistance training decreased the values of FOXO3 (p=0.003), Murf1 (p=0.005) and Arogin-1 (p=0.012) and increased forelimb grip strength (p=0.000) in the training group compared to the obese control group. Conclusion: Although obesity increased muscle atrophy markers, the results of this research showed that resistance training plays an important role in maintaining muscle mass and increasing muscle strength in obese aged rats by reducing muscle atrophy markers.

Keywords

Main Subjects


  1. Ji LL, Yeo D, Kang C. Muscle disuse atrophy caused by discord of intracellular signaling. Antioxidants & redox signaling. 2020;33(11):727-44.

    1. Sartori R, Romanello V, Sandri M. Mechanisms of muscle atrophy and hypertrophy: Implications in health and disease. Nature communications. 2021;12(1):1-12.
    2. Lee S-R, Khamoui AV, Jo E, Park B-S, Zourdos MC, Panton LB, et al. Effects of chronic high-fat feeding on skeletal muscle mass and function in middle-aged mice. Aging clinical and experimental research. 2015:27(4): 403-11.
    3. Paris MT, Bell KE, Mourtzakis M. Myokines and adipokines in sarcopenia: understanding cross-talk between skeletal muscle and adipose tissue and the role of exercise. Current opinion in pharmacology. 2020;61:52-6.
    4. Carter E, Thomas M, Murynka T, Rowan SL, Wright KJ, Huba E, et al. Slow twitch soleus muscle is not protected from sarcopenia in senescent rats. Experimental gerontology. 2010;45(9):662-70.
    5. Eriksson J, Taimela S, Koivisto V. Exercise and the metabolic syndrome. Diabetologia. 1997;40(2):125-35.
    6. Kim TN, Park MS, Ryu JY, Choi HY, Hong HC, Yoo HJ, et al. Impact of visceral fat on skeletal muscle mass and vice versa in a prospective cohort study: the Korean Sarcopenic Obesity Study (KSOS). PloS one. 2014;9(12):e115407.
    7. Ou Y, Jobu K, Ishida T, Morisawa S, Fujita H, Kawada K, et al. Saikokeishikankyoto extract alleviates muscle atrophy in KKAy mice. Journal of Natural Medicines.2022:1-10.
    8. Kim TN, Park MS, Lim KI, Choi HY, Yang SJ, Yoo HJ, et al. Relationships between sarcopenic obesity and insulin resistance, inflammation, and vitamin D status: the K orean S arcopenic O besity S tudy. Clinical endocrinology. 2013;78(4):525-32.
    9. Li H, Malhotra S, Kumar A. Nuclear factor-kappa B signaling in skeletal muscle atrophy. Journal of molecular medicine. 2008;86(10):1113-26.
    10. Singh A, Phogat J, Yadav A, Dabur R. The dependency of autophagy and ubiquitin proteasome system during skeletal muscle atrophy. Biophysical Reviews. 2021;13(2):203-19.
    11. Kang S-H, Lee H-A, Kim M, Lee E, Sohn UD, Kim I. Forkhead box O3 plays a role in skeletal muscle atrophy through expression of E3 ubiquitin ligases MuRF-1 and atrogin-1 in Cushing’s syndrome. American Journal of Physiology-Endocrinology and Metabolism. 2017;312(6):E495-E507.
    12. Aryana I, Aprianta I, Kuswardhani R. Role of Interleukin-15 in Sarcopenia: Future New Target Therapy. Int J Geriatr Gerontol. 2017;10: IJGG-104 DOI.
    13. Hord JM, Lawler JM. ROS and nNOS in the regulation of disuse-induced skeletal muscle atrophy. The Plasticity of Skeletal Muscle: Springer; 2017. p231-50.
    14. Wagatsuma A, Shiozuka M, Takayama Y, Hoshino T, Mabuchi K, Matsuda R. Effects of ageing on expression of the muscle-specific E3 ubiquitin ligases and Akt-dependent regulation of Foxo transcription factors in skeletal muscle. Molecular and cellular biochemistry. 2016;412(1):59-72.
    15. Brown LA, Perry Jr RA, Haynie WS, Lee DE, Rosa-Caldwell ME, Brown JL, et al. Moderators of skeletal muscle maintenance are compromised in sarcopenic obese mice. Mechanisms of Ageing and Development. 2021;194:111404.
    16. Medicine ACoS. Progression models in resistance training for healthy adults. Med Sci Spor Exerc. 2002; 34:364-80.
    17. Bae JH, Seo DY, Lee SH, Shin C, Jamrasi P, Han J, et al. Effects of exercise on AKT/PGC1-α/FOXO3a pathway and muscle atrophy in cisplatin-administered rat skeletal muscle. Korean J Physiol Pharmacol. 2021;25(6):585-92.
    18. Moradi Y, Zehsaz F, Nourazar MA. Concurrent exercise training and Murf-l and Atrogin-1 gene expression in the vastus lateralis muscle of male Wistar rats. Apunts Sports Medicine.2020;55(205):7-21.
    19. Wang M, Tan Y, Shi Y, Wang X, Liao Z, Wei P. Diabetes and sarcopenic obesity: pathogenesis, diagnosis, and treatments. Frontiers in endocrinology. 2020;568:11.
    20. Barazzoni R, Bischoff S, Boirie Y, Busetto L, Cederholm T, Dicker D, et al. Sarcopenic obesity: time to meet the challenge. Obesity facts. 2018;11(4):294-305.
    21. Joseph AM, Adhihetty PJ, Leeuwenburgh C. Beneficial effects of exercise on age‐related mitochondrial dysfunction and oxidative stress in skeletal muscle. The Journal of physiology. 2016;594(18):5105-23.
    22. Pahlavani HA. Exercise Therapy for People With Sarcopenic Obesity: Myokines and Adipokines as Effective Actors. Frontiers in Endocrinology.2022;13.
    23. Adamo ML, Farrar RP. Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing research reviews. 2006;5(3):310-31.
    24. Gopalan V, Yaligar J, Michael N, Kaur K, Anantharaj R, Verma S, et al. A 12-week aerobic exercise intervention results in improved metabolic function and lower adipose tissue and ectopic fat in high-fat diet fed rats. Bioscience Reports. 2021;41(1):BSR20201707-BSR.
    25. Lu Y, Li H, Shen S-W, Shen Z-H, Xu M, Yang C-J, et al. Swimming exercise increases serum irisin level and reduces body fat mass in high-fat-diet fed Wistar rats. Lipids in health and disease. 2016;15(1): 1-8.
    26. Lima TdR, Voltarelli FA, Freire LS, da Silva FA, de Almeida PC, Ávila ETP, et al. High‐fat diet and fructose drink introduced after weaning rats, induces a better human obesity model than very high‐fat diet. Journal of Food Biochemistry. 2021;45(4):e13671.
    27. Vilela TC, Effting PS, dos Santos Pedroso G, Farias H, Paganini L, Sorato HR, et al. Aerobic and strength training induce changes in oxidative stress parameters and elicit modifications of various cellular components in skeletal muscle of aged rats. Experimental gerontology. 2018;21:106-7.
    28. Scheffer DL, Silva LA, Tromm CB, da Rosa GL, Silveira PC, de Souza CT, et al. Impact of different resistance training protocols on muscular oxidative stress parameters. Applied Physiology, Nutrition, and Metabolism. 2012;37(6):1239-46.
    29. Christian CJ, Benian GM. Animal models of sarcopenia. Aging Cell. 2020;19:(10) e13223.

    .31.          Xie Wq, He M, Yu Dj, Wu Yx, Wang Xh, Lv S, et al. Mouse models of sarcopenia: classification and evaluation. Journal of Cachexia, Sarcopenia and Muscle. 2021;12(3): 538-54.

    1. Kim J-y, Choi MJ, So B, Kim H-j, Seong JK, Song W. The preventive effects of 8 weeks of resistance training on glucose tolerance and muscle fiber type composition in Zucker rats. Diabetes & metabolism journal. 2015;39(5):424-33.
    2. Walker DK, Dickinson JM, Timmerman KL, Drummond MJ, Reidy PT, Fry CS, et al. Exercise, amino acids and aging in the control of human muscle protein synthesis. Medicine and science in sports and exercise. 2011;43(12):2249.
    3. 34. Gomes MJ, Martinez PF, Pagan LU, Damatto RL, Cezar MDM, Lima ARR, et al. Skeletal muscle aging: influence of oxidative stress and physical exercise. Oncotarget. 2017;8(12): 20428.
    4. Li B, Feng L, Wu X, Cai M, Yu JJ, Tian Z. Effects of different modes of exercise on skeletal muscle mass and function and IGF-1 signaling during early aging in mice. Journal of Experimental Biology. 2022;225(21):jeb244650.
    5. 36. Zeng Z, Liang J, Wu L, Zhang H, Lv J, Chen N. Exercise-induced autophagy suppresses sarcopenia through Akt/mTOR and Akt/FoxO3a signal pathways and AMPK-mediated mitochondrial quality control. Frontiers in Physiology. 2020;11:583478.
    6. 37. Ribeiro MBT, Guzzoni V, Hord JM, Lopes GN, Marqueti RdC, de Andrade RV, et al. Resistance training regulates gene expression of molecules associated with intramyocellular lipids, glucose signaling and fiber size in old rats. Scientific reports. 2017;7(1):1-13.
    7. 38. Shabkhiz F, Khalafi M, Rosenkranz S, Karimi P, Moghadami K. Resistance training attenuates circulating FGF-21 and myostatin and improves insulin resistance in elderly men with and without type 2 diabetes mellitus: A randomised controlled clinical trial. European journal of sport science. 2021;21(4):636-45.
    8. 39. Dastah S, Babaei S. Effect of aquatic training on serum Fetuin-A, ANGPTL4 and FGF21 levels in type 2 diabetic obese women. Journal of Applied Health Studies in Sport 2021;8(2):51-60. [In Persian].

     

    1. 40. Alizadeh L, Tofighi A, Azar JT. The Effect of Eight Weeks of High Intensity Interval Training (HIIT) on Serum Irisin, Fgf21 and Glycemic Indices in Type 2 Diabetic Women. Journal of Applied Health Studies in Sport Physiology. 2019;6(2):17-24. [In Persian].
    2. Léger B, Cartoni R, Praz M, Lamon S, Dériaz O, Crettenand A, et al. Akt signalling through GSK‐3β, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. The Journal of physiology. 2006;576(3):923-33.
    3. 42. Ato S, Makanae Y, Kido K, Fujita S. Contraction mode itself does not determine the level of mTORC1 activity in rat skeletal muscle. Physiological reports. 2016;4(19):e12976.
    4. 43. Shamsi M, Rahimi MR. The Effect of Eight Weeks of Resistance Training with Green Tea Extract Supplement On Serum Levels of Adiponectin and Pentraxin-3 In Obese Men. Journal of Applied Health Studies in Sport Physiology. 2021;8(2):94-101. [In Persian].
    5. Kang S, Park K-M, Sung K-Y, Yuan Y, Lim S-T. Effect of resistance exercise on the lipolysis pathway in obese pre-and postmenopausal women. Journal of Personalized Medicine. 2021;11(9):874.
    6. Laurindo CP, Gregorio KCR, Moreno ACR, Agostinho JMV, Campos EC, Nai GA, et al. Resistance training mitigates hepato-cardiac changes and muscle mitochondrial protein reductions in rats with diet-induced obesity. Heliyon. 2021;7(11):e08374.