Eight Weeks of Progressive Resistance Training Increased the Content of UCP1 in Visceral and Subcutaneous Adipose Tissue of Rats

Document Type : Research Articles

Authors

• Hani Firooz-zare ¹
• Alireza Safarzade ^{1, 2}
• Elahe Talebi-Garakani ^{1, 2}

¹ Department of Exercise Physiology, Faculty of Sports Sciences, University of Mazandaran, Babolsar, Iran

² Athletic Performance and Health Research Center, University of Mazandaran, Babolsar, Iran

https://doi.org/10.22067/jcmr.2024.87131.1088

Abstract

New evidence indicates that exercise training as a stimulant of adipose tissue thermogenesis can play a positive role in preventing obesity. The purpose of this research is to investigate the effect of eight weeks of progressive resistance training on the levels of proteins involved in the thermogenesis of visceral and subcutaneous adipose tissues in sucrosefed rats. Twenty- four male Wistar rats (222±26g, 4- 6 weeks) were divided into normal control, sucrose control, and progressive resistance training groups. The normal control group was fed only standard food and water. In addition to free access to water and standard food, the other two groups were fed a 10% sucrose solution. The exercise program started after two months of nutritional intervention and continued for 8 weeks, 3 days a week. 72 hours after the last training session and after 4 hours of fasting, the rats were anesthetized, and blood samples and visceral and subcutaneous adipose tissues were taken. Serum glucose and insulin levels and insulin resistance index along with tissue levels of PGC1α and UCP1 were measured. The results showed that the consumption of sucrose solution significantly increased serum glucose (P≥0.001) and insulin (P≥0.001) levels and insulin resistance index (P≥0.001) and decreased UCP1 levels in subcutaneous fat tissue (P≥0.03) compared to the control group. Also, progressive resistance training caused a significant decrease in insulin (P≥0.007), insulin resistance index (P≥0.025), and increased UCP1 levels in visceral(P≥0.032) and subcutaneous (P≥0.005) adipose tissue compared to the sucrose control group. However, the levels of PGC1α in visceral and subcutaneous fat tissues did not show any significant changes. The results showed that progressive resistance training, in addition to improving insulin sensitivity, can play an effective role in the process of browning white adipose tissue by increasing the level of UCP1 in visceral and subcutaneous adipose tissue, and as a therapeutic method for improving insulin resistance and obesity.

Keywords

• Progressive Resistance Training
• insulin resistance
• UCP1
• PGC-1&alpha

References

Aguilera, A. A., Díaz, G. H., Barcelata, M. L., Guerrero, O. A., & Ros, R. M. O. (2004). Effects of fish oil on hypertension, plasma lipids, and tumor necrosis factor-α in rats with sucrose-induced metabolic syndrome. The Journal of Nutritional Biochemistry, 15(6), 350-357.

Bettini, S., Favaretto, F., Compagnin, C., Belligoli, A., Sanna, M., Fabris, R., Serra, R., Dal Prà, C., Prevedello, L., Foletto, M., Vettor, R., Milan, G., & Busetto, L. (2019). Resting Energy Expenditure, Insulin Resistance and UCP1 Expression in Human Subcutaneous and Visceral Adipose Tissue of Patients With Obesity. Front Endocrinol (Lausanne), 10, 548.

Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Rasbach, K. A., Boström, E. A., Choi, J. H., & Long, J. Z. (2012). A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature, 481(7382), 463-468.

Carrière, A., Lagarde, D., Jeanson, Y., Portais, J.-C., Galinier, A., Ader, I., & Casteilla, L. (2020). The emerging roles of lactate as a redox substrate and signaling molecule in adipose tissues. Journal of physiology and biochemistry, 76, 241-250.

Chan, C. Y.-Y., Kendig, M., Boakes, R. A., & Rooney, K. (2013). Low-volume exercise can prevent sucrose-induced weight gain but has limited impact on metabolic measures in rats. European journal of nutrition, 52, 1721-1732.

Chen, G.-C., Huang, C.-Y., Chang, M.-Y., Chen, C.-H., Chen, S.-W., Huang, C.-j., & Chao, P.-M. (2011). Two unhealthy dietary habits featuring a high fat content and a sucrose-containing beverage intake, alone or in combination, on inducing metabolic syndrome in Wistar rats and C57BL/6J mice. Metabolism, 60(2), 155-164.

El Hafidi, M., Cuéllar, A., Ramı́rez, J., & Baños, G. (2001). Effect of sucrose addition to drinking water, that induces hypertension in the rats, on liver microsomal Δ9 and Δ5-desaturase activities. The Journal of Nutritional Biochemistry, 12(7), 396-403.

Evans, M., Cogan, K. E., & Egan, B. (2017). Metabolism of ketone bodies during exercise and training: physiological basis for exogenous supplementation. The Journal of physiology, 595(9), 2857-2871.

Feldmann, H. M., Golozoubova, V., Cannon, B., & Nedergaard, J. (2009). UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell metabolism, 9(2), 203-209.

García-Ruiz, E., Reynés, B., Díaz-Rúa, R., Ceresi, E., Oliver, P., & Palou, A. (2015). The intake of high-fat diets induces the acquisition of brown adipocyte gene expression features in white adipose tissue. International journal of obesity, 39(11), 1619-1629.

Hornberger Jr, T. A., & Farrar, R. P. (2004). Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Canadian journal of applied physiology, 29(1), 16-31.

Kahn, B. B., & Flier, J. S. (2000). Obesity and insulin resistance. J Clin Invest, 106(4), 473-481.

Kalinovich, A. V., de Jong, J. M., Cannon, B., & Nedergaard, J. (2017). UCP1 in adipose tissues: two steps to full browning. Biochimie, 134, 127-137.

Kawasaki, T., Kashiwabara, A., Sakai, T., Igarashi, K., Ogata, N., Watanabe, H., Ichiyanagi, K., & Yamanouchi, T. (2005). Long-term sucrose-drinking causes increased body weight and glucose intolerance in normal male rats. British journal of nutrition, 93(5), 613-618.

Khalafi, M., Mohebbi, H., Symonds, M. E., Karimi, P., Akbari, A., Tabari, E., Faridnia, M., & Moghaddami, K. (2020). The impact of moderate-intensity continuous or high-intensity interval training on adipogenesis and browning of subcutaneous adipose tissue in obese male rats. Nutrients, 12(4), 925.

Kopecky, J., Clarke, G., Enerbäck, S., Spiegelman, B., & Kozak, L. (1995). Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. The Journal of clinical investigation, 96(6), 2914-2923.

Lo, K. A., & Sun, L. (2013). Turning WAT into BAT: a review on regulators controlling the browning of white adipocytes. Bioscience reports, 33(5), e00065.

Mašek, T., Filipović, N., Vuica, A., & Starčević, K. (2017). Effects of treatment with sucrose in drinking water on liver histology, lipogenesis and lipogenic gene expression in rats fed high-fiber diet. Prostaglandins, Leukotrienes and Essential Fatty Acids, 116, 1-8.

Michurina, S., Stafeev, I., Podkuychenko, N., Sklyanik, I., Shestakova, E., Yah'yaev, K., Yurasov, A., Ratner, E., Menshikov, M., & Parfyonova, Y. (2020). Decreased UCP-1 expression in beige adipocytes from adipose-derived stem cells of type 2 diabetes patients associates with mitochondrial ROS accumulation during obesity. Diabetes Research and Clinical Practice, 169, 108410.

Min, M., Li-Fa, X., Dong, H., Jing, W., & Ming-Jie, B. (2017). Dietary patterns and overweight/obesity: a review article. Iranian journal of public health, 46(7), 869.

Mu, W.-J., Zhu, J.-Y., Chen, M., & Guo, L. (2021). Exercise-mediated browning of white adipose tissue: its significance, mechanism and effectiveness. International Journal of Molecular Sciences, 22(21), 11512.

Narita, T., Kobayashi, M., Itakura, K., Itagawa, R., Kabaya, R., Sudo, Y., Okita, N., & Higami, Y. (2018). Differential response to caloric restriction of retroperitoneal, epididymal, and subcutaneous adipose tissue depots in rats. Experimental Gerontology, 104, 127-137.

O'rourke, R., Metcalf, M., White, A., Madala, A., Winters, B., Maizlin, I., Jobe, B., Roberts, C., Slifka, M., & Marks, D. (2009). Depot-specific differences in inflammatory mediators and a role for NK cells and IFN-γ in inflammation in human adipose tissue. International journal of obesity, 33(9), 978-990.

Picoli, C. d. C., Gilio, G. R., Henriques, F., Leal, L. G., Besson, J. C., Lopes, M. A., Franzoi de Moraes, S. M., Hernandes, L., Batista Junior, M. L., & Peres, S. B. (2020). Resistance exercise training induces subcutaneous and visceral adipose tissue browning in Swiss mice. Journal of Applied Physiology, 129(1), 66-74.

Reddy, N. L., Tan, B. K., Barber, T. M., & Randeva, H. S. (2014). Brown adipose tissue: endocrine determinants of function and therapeutic manipulation as a novel treatment strategy for obesity. BMC obesity, 1(1), 1-12.

Rockstroh, D., Landgraf, K., Wagner, I. V., Gesing, J., Tauscher, R., Lakowa, N., Kiess, W., Bühligen, U., Wojan, M., & Till, H. (2015). Direct evidence of brown adipocytes in different fat depots in children. PloS one, 10(2), e0117841.

Schreiber, R., Reverte-salisa, L., Dong, H., Christensen, D. P., Sun, W., Gnad, T., Karavaeva, I., Nielsen, T. S., Kooijman, S., & Cero, C. Lipolysis drives expression of the constitutively active receptor GPR3 to induce adipose thermogenesis.

Sharma, B. K., Patil, M., & Satyanarayana, A. (2014). Negative regulators of brown adipose tissue (BAT)‐mediated thermogenesis. Journal of cellular physiology, 229(12), 1901-1907.

Shirkhani, S., Marandi, S. M., Kazeminasab, F., Ghaedi, K., Esfarjani, F., & Nasr-Esfahani, M. H. (2021). The effect of exercise on beige adipose tissue. Sport Physiology, 13(50), 17-38.

Souza Cruz, E. M., Bitencourt de Morais, J. M., Dalto da Rosa, C. V., da Silva Simões, M., Comar, J. F., de Almeida Chuffa, L. G., & Seiva, F. R. F. (2020). Long-term sucrose solution consumption causes metabolic alterations and affects hepatic oxidative stress in Wistar rats. Biol Open, 9(3). bio047282.

Stanford, K. I., Middelbeek, R. J., & Goodyear, L. J. (2015). Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes, 64(7), 2361-2368.

Stanhope, K. L. (2016). Sugar consumption, metabolic disease, and obesity: The state of the controversy. Critical reviews in clinical laboratory sciences, 53(1), 52-67.

Sun, S., Hanzawa, F., Umeki, M., Ikeda, S., Mochizuki, S., & Oda, H. (2018). Time-restricted feeding suppresses excess sucrose-induced plasma and liver lipid accumulation in rats. PloS one, 13(8), e0201261.

Tanimura, R., Kobayashi, L., Shirai, T., & Takemasa, T. (2022). Effects of exercise intensity on white adipose tissue browning and its regulatory signals in mice. Physiological Reports, 10(5), e15205.

Wajchenberg, B. L. o. (2000). Subcutaneous and Visceral Adipose Tissue: Their Relation to the Metabolic Syndrome. Endocrine Reviews, 21(6), 697-738.

Wang, P., Mariman, E., Renes, J., & Keijer, J. (2008). The secretory function of adipocytes in the physiology of white adipose tissue. Journal of Cellular Physiology, 216(1), 3-13.

Winn, N. C., Vieira-Potter, V. J., Gastecki, M. L., Welly, R. J., Scroggins, R. J., Zidon, T. M., Gaines, T. K. L., Woodford, M. L., Karasseva, N. G., & Kanaley, J. A. (2017). Loss of UCP1 exacerbates Western diet-induced glycemic dysregulation independent of changes in body weight in female mice. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 312(1), R74-R84.

Yang, Y. R., & Kwon, K.-S. (2020). Potential roles of exercise-induced plasma metabolites linking exercise to health benefits. Frontiers in Physiology, 11, 1620.

Yao, Z., Yan, Y., Zheng, X., Wang, M., Zhang, H., Li, H., & Chen, W. (2020). Dietary lactate supplementation protects against obesity by promoting adipose browning in mice. Journal of Agricultural and Food Chemistry, 68(50), 14841-14849.

Ye, Y., Liu, H., Zhang, F., & Hu, F. (2019). mTOR signaling in Brown and Beige adipocytes: implications for thermogenesis and obesity. Nutrition & metabolism, 16, 1-14.

Young, P., Arch, J., & Ashwell, M. (1984). Brown adipose tissue in the parametrial fat pad of the mouse. FEBS letters, 167(1), 10-14.

Zuriaga, M. A., Fuster, J. J., Gokce, N., & Walsh, K. (2017). Humans and mice display opposing patterns of “browning” gene expression in visceral and subcutaneous white adipose tissue depots. Frontiers in cardiovascular medicine, 4, 27.