Acute Interval and Continuous Moderate-Intensity Exercise Enhanced Circadian Thermogenic Activity through Browning-related Genes in Obese Adolescent Female

Authors

DOI:

https://doi.org/10.11113/mjfas.v17n5.2271

Keywords:

Thermogenic, exercise, PGC-1α, FNDC-5, obesity

Abstract

Thermogenesis is associated with oxidation activity in muscle and fat tissue, the target of non-pharmacological therapy in preventing the increase in obesity. This research was designed to reveal the circadian profile of thermogenic gene expression after the acute interval and continuous moderate-intensity exercise. The subjects were 22 randomly selected obese adolescent females who met the predetermined inclusion criteria. The study subjects were then divided into three groups: control group (CG), acute interval moderate-intensity exercise group (AIMIE), and acute continuous moderate-intensity exercise group (ACMIE). Acute interval and continuous exercise were performed by running on a treadmill for 40-45 minutes, while moderate-intensity was defined as 60%-70% of the maximum heart rate (HRmax). The blood samples were collected initially (pre-exercise), followed by 10 minutes, 6 hours, and 24 hours post-acute interval and continuous moderate-intensity exercise treatment. Measurement of peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1α) and fibronectin type III domain 5 (FNDC-5) expressions in protein level were confirmed by enzyme-linked immunosorbent assay (ELISA) method. Data were analyzed using one way-ANOVA and two way-ANOVA with a significant level of 5%. The findings suggest a substantial increase in the expression of PGC-1α and FNDC-5 after exercise compared to before the workout. A significant difference in PGC-1α and FNDC-5 expressions between the control group compared to AIMIE and ACMIE (p ≤ 0.05) has been observed. However, there is no significant difference in PGC-1α and FNDC-5 expressions after exercise between AIMIE and ACMIE (p ≥ 0.05). In conclusion, acute interval and continuous moderate-intensity exercise increase the expression of thermogenesis-related genes. Hence, acute interval and continuous moderate-intensity exercise might be potential non-pharmacological therapy to prevent, reduce, and control the increasing prevalence of obesity.

References

M. F. Hussain, A. Roesler, and L. Kazak, “Regulation of adipocyte thermogenesis: mechanisms controlling obesity,” The FEBS journal, vol. 287, no. 16, pp. 3370–3385, 2020. https://doi.org/10.1111/febs.15331.

N. K. Tayagi, A. Solanky, S. N. Jamali, M. Azharuddin, K. Ali, and I. Ahmad, “Aerobic Training, in Combination with Listening Music, Changes Post-Exercise Cardiac Autonomic Function in Collegiate Overweight and Obese Individuals,”. Asian Journal of Sports Medicine, vol. 11, no. 1, pp. e97122, 2020. https://doi.org/10.5812/asjsm.97122.

I. L. P. Bonfante, M. P. T. Chacon-Mikahil, D. T. Brunelli, A. F. Gáspari, R. G. Duft, A. G. Oliveira, T. G. Araujo, M. J. A. Saad, and C. R. Cavaglieri, “Obese with higher FNDC5/Irisin levels have a better metabolic profile, lower lipopolysaccharide levels and type 2 diabetes risk,” Archives of Endocrinology and Metabolism, vol. 61, no. 6, pp. 524–533, 2017. https://doi.org/10.1590/2359-3997000000305.

G. Sanchez-Delgado, B. Martinez-Tellez, J. Olza, C. M. Aguilera, Á. Gil, and J. R. Ruiz, “Role of Exercise in the Activation of Brown Adipose Tissue,” Annals of Nutrition and Metabolism, vol. 67, no. 1, pp. 21–32, 2015. https://doi.org/10.1159/000437173.

Y. Onder, and C. B. Green, “Rhythms of metabolism in adipose tissue and mitochondria. Neurobiology of Sleep and Circadian Rhythms, vol. 4, pp. 57–63, 2018. https://doi.org/10.1016/j.nbscr.2018.01.001.

A. W. C. Man, H. Li, and N. Xia, “Impact of Lifestyles (Diet and Exercise) on Vascular Health: Oxidative Stress and Endothelial Function,” Oxidative Medicine and Cellular Longevity, vol. 2020, Article ID 1496462, pp. 1–22, 2020. https://doi.org/10.1155/2020/1496462.

J. Kim, and Y. Jee, “EMS-effect of Exercises with Music on Fatness and Biomarkers of Obese Elderly Women,” Medicina (Kaunas), vol. 56, no. 4, pp. 158, 2020. https://doi.org/10.3390/medicina56040158.

E. A. Castro, E. V. Carraça, R. Cupeiro, B. López-Plaza, P. J. Teixeira, D. González-Lamuño, and A. B. Peinado, “The Effects of the Type of Exercise and Physical Activity on Eating Behavior and Body Composition in Overweight and Obese Subjects. Nutrients, vol. 12, no. 2, pp. 557, 2020. https://doi.org/10.3390/nu12020557.

L. G. Leal, M. A. Lopes, and M. L. Batista, Physical Exercise-Induced Myokines and Muscle-Adipose Tissue Crosstalk: A Review of Current Knowledge and the Implications for Health and Metabolic Diseases. Frontiers in Physiology, vol. 9, 2018. https://doi.org/10.3389/fphys.2018.01307.

Wylie-Rosett, J., and S. S. Jhangiani, “Obesity and Disease in an Interconnected World: A Systems Approach to Turn Huge Challenges into Amazing Opportunities,” Sharjah: Bentham Science Publishers, pp. 3–29, 2015. https://doi.org/10.2174/9781681080369115010006.

A. Petridou, A. Siopi, and V. Mougios, “Exercise in the management of obesity,” Metabolism, vol. 92, pp. 163–169, 2019. https://doi.org/10.1016/j.metabol.2018.10.009.

J. J. Ruiz-Ramie, J. L. Barber, and M. A. Sarzynski, “Effects of exercise on HDL functionality,” Current Opinion in Lipidology, vol. 30, no. 1, pp. 16–23, 2019. https://doi.org/10.1097/MOL.0000000000000568.

H. Bekele, A. Asefa, B. Getachew, A. M. Belete, “Barriers and Strategies to Lifestyle and Dietary Pattern Interventions for Prevention and Management of TYPE-2 Diabetes in Africa, Systematic Review,” Journal of Diabetes Research, vol. 2020, Article ID 7948712, pp. 1–14, 2020. https://doi.org/10.1155/2020/7948712.

P. C. Dinas, I. M. Lahart, J. A. Timmons, P-A. Svensson, Y. Koutedakis, A. D. Flouris, and G. S. Metsios, “Effects of physical activity on the link between PGC-1a and FNDC5 in muscle, circulating Ιrisin and UCP1 of white adipocytes in humans: A systematic review,” F1000Research, vol. 6, 286, 2017. https://doi.org/10.12688/f1000research.11107.1.

R. Tanaka, S. Fuse, M. Kuroiwa, S. Amagasa, T. Endo, A. Ando, R. Kime, Y. Kurosawa, T. Hamaoka, “Vigorous-Intensity Physical Activities Are Associated with High Brown Adipose Tissue Density in Humans,” International Journal of Environmental Research and Public Health, vol. 17, no. 8, pp. 2796, 2020. https://doi.org/10.3390/ijerph17082796.

Tanaka, H., Ueno, S., Aoyagi, R., Hatamoto, Y., Jackowska, M., Shiose, K., and Higaki, Y, “Easily performed interval exercise induces to increase in skeletal muscle PGC-1α gene expression.” Integrative Molecular Medicine, vol. 4., no. 4, pp. 1–4, 2017. https://doi.org/10.15761/IMM.1000293.

J. G. Knudsen, M. Murholm, A. L. Carey, R. S. Biensø, A. L. Basse, T. L. Allen, J. Hidalgo, B. A. Kingwell, M. A. Febbraio, J. B. Hansen, and H. Pilegaard, “Role of IL-6 in Exercise Training- and Cold-Induced UCP1 Expression in Subcutaneous White Adipose Tissue,” PLoS ONE, vol. 9, no. e84910, 2014. https://doi.org/10.1371/journal.pone.0084910.

C. Laurens, A. Bergouignan, and C. Moro, “Exercise-Released Myokines in the Control of Energy Metabolism,” Frontiers in Physiology, vol. 11, no. 91, 2020. https://doi.org/10.3389/fphys.2020.00091.

L. Elizondo-Montemayor, A. M. Gonzalez-Gil, O. Tamez-Rivera, C. Toledo-Salinas, M. Peschard-Franco, N. A. Rodríguez-Gutiérrez, C. Silva-Platas, and G. Garcia-Rivas, “Association between Irisin, hs-CRP, and Metabolic Status in Children and Adolescents with Type 2 Diabetes Mellitus,” Mediators of Inflammation, vol. 2019, Article ID 6737318, pp. 1–13, 2019. https://doi.org/10.1155/2019/6737318.

Ikeda, K., and T. Yamada, “UCP1 Dependent and Independent Thermogenesis in Brown and Beige Adipocytes,” Frontiers in Endocrinology, vol. 11, no. 498, 2020. https://doi.org/10.3389/fendo.2020.00498.

L. Catalano-Iniesta, V. Sánchez Robledo, M. C. Iglesias-Osma, A. G. Albiñana, S. Carrero, E. J. Blanco, M. Carretero-Hernández, J. Carretero, and M. J. García-Barrado, “Evidences for Expression and Location of ANGPTL8 in Human Adipose Tissue,” Journal of Clinical Medicine, vol. 9, no. 2, pp. 512, 2020. https://doi.org/10.3390/jcm9020512.

N. Perakakis, G. A. Triantafyllou, J. M. Fernández-Real, J. Y. Huh, K. H. Park, J. Seufert, C. S. Mantzoros, “Physiology and role of irisin in glucose homeostasis,” Nature Reviews Endocrinology, vol. 13, no. 6, pp. 324–337, 2017. https://doi.org/10.1038/nrendo.2016.221.

M. Enteshary, F. Esfarjani, and J. Reisi, “Comparison of the Effects of Two Different Intensities of Combined Training on Irisin, Betatrophin, and Insulin Levels in Women with Type 2 Diabetes,” Asian Journal of Sports Medicine, vol. 10, no. 2, pp. e68943, 2019. https://doi.org/10.5812/asjsm.68943.

F. Rabiee, L. Lachinani, S. Ghaedi, M. H. Nasr-Esfahani, T. L. Megraw, and K. Ghaedi, “New insights into the cellular activities of Fndc5/Irisin and its signaling pathways,” Cell & Bioscience, vol. 10, no. 51, 2020. https://doi.org/10.1186/s13578-020-00413-3.

M. Abu-Farha, D. Sriraman, P. Cherian, I. AlKhairi, N. Elkum, K. Behbehani, and J. Abubaker, “Circulating ANGPTL8/Betatrophin Is Increased in Obesity and Reduced after Exercise Training,” PLoS One, vol. 11, no. e0147367, 2016. https://doi.org/10.1371/journal.pone.0147367.

G. Z. Schaun, C. L. Alberton, D. O. Ribeiro, and S. S. Pinto, “Acute effects of high-intensity interval training and moderate-intensity continuous training sessions on cardiorespiratory parameters in healthy young men,” European Journal of Applied Physiology, vol. 117, no. 11, pp. 1437–1444, 2017. https://doi.org/10.1007/s00421-017-3636-7.

C. Granata, R. S. F. Oliveira, J. P. Little, K. Renner, and D. J. Bishop, “Sprint-interval but not continuous exercise increases PGC-1α protein content and p53 phosphorylation in nuclear fractions of human skeletal muscle,” Scientific Reports, vol. 7, no. 44227, 2017. https://doi.org/10.1038/srep44227.

D. V. Popov, “Adaptation of Skeletal Muscles to Contractile Activity of Varying Duration and Intensity: The Role of PGC-1α,” Biochemistry (Moscow), vol. 83, no. 6, pp. 613–628, 2018. https://doi.org/10.1134/S0006297918060019.

M. Khalafi, H. Mohebbi, M. E. Symonds, P. Karimi, A. Akbari, E. Tabari, M. Faridnia, and K. Moghaddami, “The Impact of Moderate-Intensity Continuous or High-Intensity Interval Training on Adipogenesis and Browning of Subcutaneous Adipose Tissue in Obese Male Rats,” Nutrients, vol. 12, no. 4, pp. 925, 2020. https://doi.org/10.3390/nu12040925.

C. A. M. Gonçalves, P. M. S. Dantas, I. K. dos Santos, M. Dantas, D. C. P. da Silva, B. G. A. T. Cabral, R. O. Guerra, and G. B. C. Júnior, “Effect of Acute and Chronic Aerobic Exercise on Immunological Markers: A Systematic Review,” Frontiers in Physiology, vol. 10, no. 1602, 2020. https://doi.org/10.3389/fphys.2019.01602.

Sugiharto, D. Merawati, R. G. Kinanti, H. Susanto, A. Taufiq, and Sunaryono, “The Attenuation of Physical-Physiological Stresses through Musical-High Intensity Exercise Co-Treatment in Non-Athlete Individual,” Journal of Physics: Conference Series, vol. 1093, no. 012026, 2018. https://doi.org/10.1088/1742-6596/1093/1/012026.

B. M. Antunes, F. E. Rossi, L. M. Oyama, J. C. Rosa-Neto, and F. S. Lira, “Exercise intensity and physical fitness modulate lipoproteins profile during acute aerobic exercise session,” Scientific Reports, vol. 10, Article number 4160, 2020. https://doi.org/10.1038/s41598-020-61039-6.

S. Rius-Pérez, I. Torres-Cuevas, I. Millán, Á. L. Ortega, and S. Pérez, “PGC-1α, Inflammation, and Oxidative Stress: An Integrative View in Metabolism,” Oxidative Medicine and Cellular Longevity, vol. 2020, Article ID 1452696, pp. 1–20, 2020. https://doi.org/10.1155/2020/1452696.

C. Larson, M. Opichka, M. L. McGlynn, C. W. Collins, and D. Slivka, “Exercise- and Cold-Induced Human PGC-1α mRNA Isoform Specific Responses,” International Journal of Environmental Research and Public Health, vol. 17, no. 16, pp. 5740, 2020. https://doi.org/10.3390/ijerph17165740.

I. G. Fatouros,“Is irisin the new player in exercise-induced adaptations or not? A 2017 update,” Clinical Chemistry and Laboratory Medicine (CCLM), vol. 56, no. 4, pp. 525-548, 2018. https://doi.org/10.1515/cclm-2017-0674.

H. Nygaard, G. Slettaløkken, G. Vegge, I. Hollan, J. E. Whist, T. Strand, B. R. Rønnestad, and S. Ellefsen, “Irisin in Blood Increases Transiently after Single Sessions of Intense Endurance Exercise and Heavy Strength Training,” PLOS ONE, vol. 10, no. e0121367, 2015. https://doi.org/10.1371/journal.pone.0121367.

L. Parker, C. S. Shaw, L. Banting, I. Levinger, K. M. Hill, A. J. McAinch, and N. K. Stepto, “Acute Low-Volume High-Intensity Interval Exercise and Continuous Moderate-Intensity Exercise Elicit a Similar Improvement in 24-h Glycemic Control in Overweight and Obese Adults,” Frontiers in Physiology, vol. 7, no. 661, 2017. https://doi.org/10.3389/fphys.2016.00661.

Y. Tsuchiya, S. Mizuno, and K. Goto, “Irisin response to downhill running exercise in humans,” J Exerc Nutrition Biochem, vol. 22, no. 2, pp. 12–17, 2018. https://doi.org/10.20463/jenb.2018.0011.

V. O. A. Santos, R. A. V. Browne, D. C. Souza, V. A. F. Matos, G. A. D. Macêdo, L. F. Farias-Junior, J. C. Farias-Júnior, E. C. Costa, and A. P. T. Fayh, Effects of High-Intensity Interval and Moderate-Intensity Continuous Exercise on Physical Activity and Sedentary Behavior Levels in Inactive Obese Males: A Crossover Trial. J Sports Sci Med, vol. 18, no. 3, pp. 390–398, 2019.

S. Qiu, E. Bosnyák, G. Treff, J. M. Steinacker, A. M. Nieß, K. Krüger, F. C. Mooren, M. Zügel, and U. Schumann, “Acute exercise-induced irisin release in healthy adults: Associations with training status and exercise mode,” European Journal of Sport Science, vol. 18, no. 9, pp. 1226–1233, 2018. https://doi.org/10.1080/17461391.2018.1478452

G. A. Tew, D. Leighton, R. Carpenter, S. Anderson, L. Langmead, J. Ramage, J. Faulkner, E. Coleman, C. Fairhurst, M. Seed, and L. Bottoms, “High-intensity interval training and moderate-intensity continuous training in adults with Crohn’s disease: a pilot randomised controlled trial,” BMC Gastroenterology, vol. 19, no. 1, pp. 19, 2019. https://doi.org/10.1186/s12876-019-0936-x.

K. A. Dias, C. B. Ingul, A. E. Tjonna, S. E. Keating, S. R. Gomersall, T. Follestad, M. S. Hosseini, S. M. Hollekim-Strand, T. B. Ro, M. Haram, E. M. Huuse, P. S. W. Davies, P. A. Cain, G. M. Leong, and J. S. Coombes, “Effect of High-Intensity Interval Training on Fitness, Fat Mass and Cardiometabolic Biomarkers in Children with Obesity: A Randomised Controlled Trial,” Sports Medicine, vol. 48, no. 3, pp. 733-746, 2017. https://doi.org/10.1007/s40279-017-0777-0.

J. Zhao, Z. Su, C. Qu, and Y. Dong, “Effects of 12 Weeks Resistance Training on Serum Irisin in Older Male Adults,” Frontiers in Physiology, vol. 8, no. 171, 2017. https://doi.org/10.3389/fphys.2017.00171.

C-F. Cheng, H-C. Ku, and H. Lin, “PGC-1α as a Pivotal Factor in Lipid and Metabolic Regulation,” International Journal of Molecular Sciences, vol. 19, no. 11, pp. 3447, 2018. https://doi.org/10.3390/ijms19113447.

F. Giolo De Carvalho, and L. Sparks, “Targeting White Adipose Tissue with Exercise or Bariatric Surgery as Therapeutic Strategies in Obesity,” Biology, vol. 8, no. 1, pp. 16, 2019. https://doi.org/10.3390/biology8010016.

B. Otero-Díaz, M. Rodríguez-Flores, V. Sánchez-Muñoz, F. Monraz-Preciado, S. Ordoñez- Ortega, V. Becerril-Elias, G. Baay-Guzmán, R. Obando-Monge, E. García-García, B. Palacios-González, M. T. Villarreal-Molina, M. Sierra-Salazar, and B. Antuna-Puente, “Exercise Induces White Adipose Tissue Browning Across the Weight Spectrum in Humans,” Front. Physiol, vol. 9, no. 1781, 2018. https://doi.org/10.3389/fphys.2018.01781.

J. Reisi, K. Ghaedi, H. Rajabi, and S. M. Marandi, “Can Resistance Exercise Alter Irisin Levels and Expression Profiles of FNDC5 and UCP1 in Rats?,” Asian J Sports Med, vol. 7, no. 4, 2016. https://doi.org/10.5812/asjsm.35205.

N. Brandt, M. M. Dethlefsen, J. Bangsbo, and H. Pilegaard, “PGC-1α and exercise intensity dependent adaptations in mouse skeletal muscle,” PLOS ONE, vol. 12, no. e0185993, 2017. https://doi.org/10.1371/journal.pone.0185993.

S. Ringholm, J. G. Knudsen, L. Leick, A. Lundgaard, M. Munk Nielsen, and H. Pilegaard, “PGC-1α Is Required for Exercise and Exercise Training-Induced UCP1 Up-Regulation in Mouse White Adipose Tissue,” PLOS ONE, vol. 8, no. e64123, 2013. https://doi.org/10.1371/journal.pone.0064123.

N. Chen, Q. Li, J. Liu, and S. Jia, “Irisin, an exercise-induced myokine as a metabolic regulator: an updated narrative review: Irisin as a Metabolic Regulator,” Diabetes/Metabolism Research and Reviews, vol. 32, no. 1, pp. 51–59, 2016. https://doi.org/10.1002/dmrr.2660.

N. Kim, J. Kim, C. Yoo, K. Lim, T. Akimoto, and J. Park, “Effect of acute mid-intensity treadmill exercise on the androgen hormone level and uncoupling protein-1 expression in brown fat tissue of mouse,” Journal of Exercise Nutrition & Biochemistry, vol. 22, no. 1, pp. 15–21, 2018. https://doi.org/10.20463/jenb.2018.0003.

J. Y. Huh, V. Mougios, A. Kabasakalis, I. Fatourus, A. Siopi, I. I. Douroudos, A. Filippaios, G. Panagiotou, K. H. Park, and C. S. Mantzoros, “Exercise-induced irisin secretion is independent of age or fitness level and increased irisin may directly modulate muscle metabolism through AMPK activation,” Journal of Clinical Endocrinology and Metabolism, vol. 99, no. 11, pp. E2154-E2161, 2014. https://doi.org/10.1210/jc.2014-1437.

M. Pang, J. Yang, J. Rao, H. Wang, J. Zhang, S. Wang, X. Chen, and X. Dong, “Time-Dependent Changes in Increased Levels of Plasma Irisin and Muscle PGC-1α and FNDC5 after Exercise in Mice,” The Tohoku Journal of Experimental Medicine, vol. 244, no. 2, pp. 93–103, 2018. https://doi.org/10.1620/tjem.244.93.

C. M. Dieli-Conwright, J. L. Kiwata, C. T. Tuzon, T. M. Spektor, F. R. Sattler, J.C. Rice, and E. T. Schroeder, “Acute Response of PGC-1α and IGF-1 Isoforms to Maximal Eccentric Exercise in Skeletal Muscle of Postmenopausal Women,” Journal of Strength and Conditioning Research, vol. 30, no. 4, pp. 1161–1170, 2016. https://doi.org/10.1519/JSC.0000000000001171.

E. Badawy, N. A. El-laithy, S. M. Morsy, M. N. Ashour, T. R. Elias, M. M. Masoud, O. Aly, Role of swimming on muscle PGC-1α, FNDC5 mRNA, and assessment of serum omentin, adropin, and irisin in high carbohydrate high fat (HCHF) diet induced obesity in rats. Egyptian Journal of Medical Human Genetics, vol. 21, Article number 37, 2020. https://doi.org/10.1186/s43042-020-00080-6.

S. Lee, L. Garcia, A. D. Leon, R. Z. Bustos, B. Campos, J. A. Krentzel, L. Mandarino, and D. K. Coletta, “167-OR: Exercise Training Alters Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1 Alpha (PGC-1 Alpha) DNA Methylation in Human Skeletal Muscle,” Diabetes, vol. 69, no. 1, 2020. https://doi.org/10.2337/db20-167-OR.

F. Norheim, T. M. Langleite, M. Hjorth, T. Holen, A. Kielland, H. K. Stadheim, H. L. Gulseth, K. I. Birkeland, J. Jensen, and C. A. Drevon, “The effects of acute and chronic exercise on PGC-1α, irisin and browning of subcutaneous adipose tissue in humans,” FEBS Journal, vol. 281, no. 3, pp. 739-749, 2014. https://doi.org/10.1111/febs.12619.

Y. Fukushima, S. Kurose, H. Shinno, H. Cao Thi Thu, A. Tamanoi, H. Tsutsumi, T. Hasegawa, T. Nakajima, and Y. Kimura, “Relationships between serum irisin levels and metabolic parameters in Japanese patients with obesity: Irisin levels and metabolic parameters,” Obesity Science & Practice, vol. 2, no. 2, pp. 203–209, 2016. https://doi.org/10.1002/osp4.43.

C. Skovgaard, N. Brandt, H. Pilegaard, and J. Bangsbo, Combined speed endurance and endurance exercise amplify the exercise-induced PGC-1α and PDK4 mRNA response in trained human muscle. Physiological Reports, vol. 4, no. e12864, 2016. https://doi.org/10.14814/phy2.12864.

M. Cao, M. Quan, and J. Zhuang, “Effect of High-Intensity Interval Training versus Moderate-Intensity Continuous Training on Cardiorespiratory Fitness in Children and Adolescents: A Meta-Analysis,” International Journal of Environmental Research and Public Health, vol. 16, no. 9, pp. 1533, 2019. https://doi.org/10.3390/ijerph16091533.

S. Yang, E. Loro, S. Wada, B. Kim, W-J. Tseng, K. Li, T.S. Khurana, and Z. Arany, “Functional effects of muscle PGC-1alpha in aged animals,” Skeletal Muscle, vol. 10, Article number 14, 2020. https://doi.org/10.1186/s13395-020-00231-8.

J. F. Halling, and H. Pilegaard, “PGC-1α-mediated regulation of mitochondrial function and physiological implications,” Applied Physiology, Nutrition, and Metabolism, vol. 45, no. 9, pp. 927–936, 2020. https://doi.org/10.1139/apnm-2020-0005.

C. W. Taylor, S. A. Ingham, J. E. A. Hunt, N. R. W. Martin, J. S. M. Pringle, R. A. Ferguson, “Exercise duration-matched interval and continuous sprint cycling induce similar increases in AMPK phosphorylation, PGC-1α and VEGF mRNA expression in trained individuals,” European Journal of Applied Physiology, vol. 116, no. 8, pp. 1445–1454, 2016. https://doi.org/10.1007/s00421-016-3402-2.

G. L. McKie, and D. C. Wright, “Biochemical adaptations in white adipose tissue following aerobic exercise: from mitochondrial biogenesis to browning,” Biochemical Journal, vol. 477, no. 6. pp. 1061–1081, 2020. https://doi.org/10.1042/BCJ20190466.

J-S. Park, J. O. Holloszy, K. Kim, and J-H. Koh, “Exercise Training-Induced PPARβ Increases PGC-1α Protein Stability and Improves Insulin-Induced Glucose Uptake in Rodent Muscles,” Nutrients, vol. 12, no. 3, pp. 652, 2020. https://doi.org/10.3390/nu12030652.

C. Scheele, and S. Nielsen, Metabolic regulation and the anti-obesity perspectives of human brown fat. Redox Biology, vol. 12, pp. 770–775, 2017. https://doi.org/10.1016/j.redox.2017.04.011.

H. Islam, D. A. Hood, and B. J. Gurd, “Looking beyond PGC-1α: emerging regulators of exercise-induced skeletal muscle mitochondrial biogenesis and their activation by dietary compounds,” Applied Physiology, Nutrition, and Metabolism, vol. 45, no. 1, pp. 11–23, 2020. https://doi.org/10.1139/apnm-2019-0069.

J. A. Hawley, M. Hargreaves, M. J. Joyner, and J. R. Zierath, “Integrative Biology of Exercise,” Cell, vol. 159, no. 4, pp. 738–749, 2014. https://doi.org/10.1016/j.cell.2014.10.029.

X. Xie, T. Gao, M. Yang, P. Chen, H. Jin, L. Yang, and X. Yu, “Associations of betatrophin levels with irisin in Chinese women with normal glucose tolerance,” Diabetology & metabolic syndrome, vol. 7, Article number 26, 2015. https://doi.org/10.1186/s13098-015-0019-2.

E. Murawska-Cialowicz, P. Wolanski, J. Zuwala-Jagiello, Y. Feito, M. Petr, J. Kokstejn, P. Stastny, and D. Goliński, “Effect of HIIT with Tabata Protocol on Serum Irisin, Physical Performance, and Body Composition in Men,” International Journal of Environmental Research and Public Health, vol. 17, no. 10, pp. 3589. https://doi.org/10.3390/ijerph17103589.

M. Gerber, C. Imboden, J. Beck, S. Brand, F. Colledge, A. Eckert, E. Holsboer-Trachsler, U. Pühse, and M. Hatzinger, “Effects of Aerobic Exercise on Cortisol Stress Reactivity in Response to the Trier Social Stress Test in Inpatients with Major Depressive Disorders: A Randomized Controlled Trial,” Journal of clinical medicine, vol. 9, no. 5, pp. 1419, 2020. https://doi.org/10.3390/jcm9051419.

J. Luo, C. Tang, X. Chen, Z. Ren, H. Qu, R. Chen, and Z. Tong, “Impacts of Aerobic Exercise on Depression-Like Behaviors in Chronic Unpredictable Mild Stress Mice and Related Factors in the AMPK/PGC-1α Pathway,” International Journal of Environmental Research and Public Health, vol. 17, no. 6, pp. 2042, 2020. https://doi.org/10.3390/ijerph17062042.

M. Khammassi, N. Ouerghi, M. Said, M. Feki, Y. Khammassi, B. Pereira, D. Thivel, and A. Bouassida, “Continuous Moderate-Intensity but Not High-Intensity Interval Training Improves Immune Function Biomarkers in Healthy Young Men,” Journal of Strength and Conditioning Research, vol. 34, no. 1, pp. 249–256, 2020. https://doi.org/10.1519/JSC.0000000000002737.

M. A. Stults-Kolehmainen, and R. Sinha, “The Effects of Stress on Physical Activity and Exercise,” Sports Med. Vol. 44, no. 1, pp. 81–121, 2014. https://doi.org/10.1007/s40279-013-0090-5.

J. Williamson, and G. Davison, “Targeted Antioxidants in Exercise-Induced Mitochondrial Oxidative Stress: Emphasis on DNA Damage,” Antioxidants, vol. 9, no. 11, pp. 1142, 2020. https://doi.org/10.3390/antiox9111142.

F. de Souza-Teixeira, J. Alonso-Molero, C. Ayán, L. Vilorio-Marques, A. J. Molina, C. González-Donquiles, V. Dávila-Batista, T. Fernández-Villa, J. A. de Paz, and V. Martín, PGC-1α as a Biomarker of Physical Activity-Protective Effect on Colorectal Cancer. Cancer prevention research (Philadelphia, Pa.), vol. 11, no. 9, pp. 523–534, 2018. https://doi.org/10.1158/1940-6207.CAPR-17-0329.

J. L. Ruas, J. P. White, R. R. Rao, S. Kleiner, K. T. Brannan, B. C. Harrison, N. P. Greene, J. Wu, J. L. Estall, B. A. Irving, I. R. Lanza, K. A. Rasbach, M. Okutsu, K. S. Nair, Z. Yan, L. A. Leinwand, and B. M. Spiegelman, “A PGC-1α Isoform Induced by Resistance Training Regulates Skeletal Muscle Hypertrophy,” Cell, vol. 151, no. 6, pp. 1319–1331, 2012. https://doi.org/10.1016/j.cell.2012.10.050.

K. Mannerkorpi, K. Landin-Wilhelmsen, A. Larsson, Å. Cider, O. Arodell, and J. L. Bjersing, “Acute effects of physical exercise on the serum insulin-like growth factor system in women with fibromyalgia,” BMC Musculoskelet Disord, vol. 18, no. 1, pp. 37, 2017. https://doi.org/10.1186/s12891-017-1402-y.

M. Wiecek, J. Szymura, M. Maciejczyk, M. Kantorowicz, and Z. Szygula, “Acute Anaerobic Exercise Affects the Secretion of Asprosin, Irisin, and Other Cytokines – A Comparison Between Sexes,” Frontiers in Physiology, vol. 9, no. 1782, 2018. https://doi.org/10.3389/fphys.2018.01782.

E. S. van der Valk, M., Savas, and E. F. C. van Rossum, “Stress and Obesity: Are There More Susceptible Individuals?,” Current obesity reports, vol. 7, no. 2, pp. 193–203, 2018. https://doi.org/10.1007/s13679-018-0306-y.

D. C. Nieman, and L. M. Wentz, “The compelling link between physical activity and the body’s defense system,” Journal of Sport and Health Science, vol. 8, no. 3, pp. 201–217, 2019. https://doi.org/10.1016/j.jshs.2018.09.009.

Sugiharto, “Physiological Effects of Music during Exercise Secretion of Hormones Cortisol and Endorphins,” Folia Medica Indonesia, vol. 45, no. 72, pp.121–129, 2009.

C. Simioni, G. Zauli, A. M. Martelli, M. Vitale, G. Sacchetti, A. Gonelli, and L. M. Neri, Oxidative stress: role of physical exercise and antioxidant nutraceuticals in adulthood and aging,” Oncotarget, vol. 9, no. 24, pp. 17181–17198, 2018. https://doi.org/10.18632/oncotarget.24729.

P. Vidal, and K. I. Stanford, “Exercise-Induced Adaptations to Adipose Tissue Thermogenesis. Frontiers in Endocrinology, vol. 11, no. 270, 2020. https://doi.org/10.3389/fendo.2020.00270.

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30-10-2021