Document Type : Original Article
Authors
1 MSc of Exercise Physiology, Department of Physical Education and Sport Sciences, Faculty of Humanities, Rasht Branch, Islamic Azad University, Rasht, Iran.
2 Assistant Professor at Department of Physical Education and Sport Science, Faculty of Humanities, Rasht Branch, Islamic Azad University, Rasht, Iran.
Abstract
Background and Aim: Among the many variables that affect muscle growth are myokines and myostatin. This study looked at how resistance-aerobic training affected the expression of genes related to fibronectin type III domain-containing protein 5 (FNDC5), myostatin and hypertrophy or hyperplasia in the immature rats’ gastrocnemius muscle. Materials and Methods: A total of ten male Wistar rats, aged two weeks were randomly divided into two control (five rats) and training (five rats) groups. The resistance training program consisted of three sessions each week for six weeks, during which time the participants would carry a weight and climb a one-meter ladder 26 times. For six weeks, on alternate days, aerobic exercise consisted of jogging on a treadmill at an intensity between 25 and 50% of a rat’s maximum speed. All of the rats were dissected and their skeletal muscles isolated 48 hours after the previous training session and after fasting for 8 hours. FNDC5 and myostatin expression were measured using Real-Time PCR. Using light microscopy, hypertrophy and hyperplasia were quantified. Prism software was used to analyze the data using an independent t-test at the p≤0.05 level. Results: Following six weeks of training, the training group had higher gene expression of FNDC5 (p=0.04) and hypertrophy (p=0.004) than the control group, but decreased gene expression of myostatin (p=0.01) in comparison. Nonetheless, there was no statistically significant difference between the two groups gastrocnemius muscle hyperplasia (p=0.22). Conclusion: It appears that resistance-aerobic exercise accompanied by increased expression of FNDC5 genes and decreased myostatin gene expression increased fast twitch fiber hypertrophy. This approach shows that muscle tissue in animal samples before puberty is trainable, independent of natural growth.
Keywords
Adams, G.R. (2006). Satellite cell proliferation and skeletal muscle hypertrophy. Applied Physiology, Nutrition, and Metabolism, 31(6), 782-790. https://doi.org/10.1139/h06-053.
Agascıoglu, E., Çolak, R., & Çakatay, U. (2022). Redox status biomarkers in the fast-twitch extensor digitorum longus resulting from the hypoxic exercise. Nagoya Journal of Medical Science, 84, 433-447. https://doi.org/10.18999/nagjms.84.2.433.
Alizadeh, H., Safarzadeh, A., & Talebi-Garakani, E. (2017). Effect of resistance training on serum meteorin-like hormone level and insulin resistance index in overweight adolescent boys. Journla of Arak University of Medicall Sciences, 20(7), 54-64. [In Persian]. http://jams.arakmu.ac.ir/article-1-5233-fa.html.
Alizadeh, R., Rezaei Nejad, R., Salehpour, M., & Sheikhi, S. (2017). The effect of acute circuit resistance exercise on plasma concentration of Brain-Derived Neurotrophic Factor (BDNF) in young men. Ebnesina, 19(4), 30-37. [In Persian] http://ebnesina.ajaums.ac.ir/article-1-508-en.html
Arabzadeh, E., Shirvani, H., Ebadi Zahmatkesh, M., Riyahi Malayeri, S., Meftahi, G. H., & Rostamkhani, F. (2022). Irisin/FNDC5 influences myogenic markers on skeletal muscle following high and moderate-intensity exercise training in STZ-diabetic rats. 3 Biotech, 12(9), 1-13. [In Persian]. https://doi.org/10.1007/s13205-022-03253-9.
Azimi Dokht, S.M.A., Gharakhanlou, R., Naghdi, N., Khodadadi, D., & Zare Zade Mehrizi, A.A. (2019). The effect of the treadmill running on genes expression ofthePGC-1α, FNDC5 and BDNF in hippocampus of male rats. Journal of Practical Studies of Biosciences in Sport, 7(14), 91-101. [In Persian]. https://doi.org/10.22077/jpsbs.2017.1037.1321.
Bagherpour Tabalvandani, M.M., Fadaei, M.R., & Elmieh, A. (2020). The effect of resistance-aerobic training on the growth of muscle fibers, serum testosterone and androgen receptors on soleus muscles, in different ages groups of male rats. Metabolism and Exercise, 10(2), 111-122. [In Persian]. https://doi.org/10.22124/jme.2021.19982.217.
Bazgir, B., Fathi, R., Valojerdi, M.R., Mozdziak, P., & Asgari, A. (2017). Satellite cells contribution to exercise mediated muscle hypertrophy and repair. Cell Journal (Yakhteh), 18(4), 473. [In Persian]. https://doi.org/10.22074/cellj.2016.4714.
Biglari, S., & Gaeini A. (2019). The effect of eight weeks of High-intensity Interval Training on the gene expression of the myogenic regulatory factors MyF5 and myogenin in the skeletal muscle of rats. Sport and Exercise Physiology, 2(11), 109-116. [In Persian]. https://joeppa.sbu.ac.ir/article_98928.html.
Biglari, S., Afousi, A.G., Mafi, F., & Shabkhiz, F. (2020). High-intensity interval training-induced hypertrophy in gastrocnemius muscle via improved IGF-I/Akt/FoxO and myostatin/Smad signaling pathways in rats. Physiology International, 107(2), 220-230. [In Persian]. https://doi.org/10.1556/2060.2020.00020.
Brenmoehl, J., Albrecht, E., Komolka, K., Schering, L., Langhammer, M., Hoeflich, A., & Maak, S. (2014). Irisin is elevated in skeletal muscle and serum of mice immediately after acute exercise. International Journal of Biological Sciences, 10(3), 338. https://doi.org/10.3389/fpsyg.2011.00226.
Consitt, L.A., & Clark, B.C. (2018). The vicious cycle of myostatin signaling in sarcopenic obesity: myostatin role in skeletal muscle growth, insulin signaling and implications for clinical trials. The Journal of Frailty & Aging, 7(1), 21-27. https://doi.org/10.14283/jfa.2017.33.
Engbers, J.D., Anderson, D., Tadayonnejad, R., Mehaffey, W.H., Molineux, M.L., & Turner, R.W. (2011). Distinct roles for IT and IH in controlling the frequency and timing of rebound spike responses. The Journal of Physiology, 589(22), 5391-5413. https://doi.org/10.1113/jphysiol.2011.215632.
Esazadeh, L., Hosseini Kakhk, A., Khajeie, R., & Hejazi, S.M. (2020). The effect of concurrent training order (resistance-aerobic) on some factors of physical fitness, functional capacity and serum levels of myostatin and follistatin hormones in postmenopausal women (clinical trial). Journal of Sport Biosciences, 12(2), 189-206. [In Persian]. https://doi.org/10.22059/jsb.2020.282311.1345.
Fadaei Chafy, M.R., Mohebbi, H., Rahmani Nia, F., & Arabzadeh, E. (2021). Possible cross-talk between leptin and insulin resistance in sedentary obese boys at different stages of puberty. Journal of Exercise & Organ Cross Talk, 1(1), 15-23. [In Persian]. https://doi.org/10.22034/jeoct.2021.290898.1008.
Farzanegi, P. (2021). TGF-β1 response to eight weeks combined training with different orders in slow and fast twitch muscles in Wistar rats. Razi Journal of Medical Sciences, 28(9), 11-20. [In Persian]. https://doi.org/10.1037/bul0000130.
Hadjizadeh Anvar, S., Kordi, M., Pournemati, P., Farajnia, S., Gharadaghi, N., & Rahmati, M. (2020). The effects of cold water immersion post repeated sprint activity on serum PGC-1α and irisin in young active men. Journal of Practical Studies of Biosciences in Sport, 8(15), 8-20. [In Persian]. https://doi.org/10.22077/jpsbs.2018.993.1313.
Hittel, D.S., Axelson, M., Sarna, N., Shearer, J., Huffman, K.M., & Kraus, W.E. (2010). Myostatin decreases with aerobic exercise and associates with insulin resistance. Medicine and Science in Sports and Exercise, 42(11), 2023. https://doi.org/10.1249/MSS.0b013e3181e0b9a8.
Hosseinzadeh, M., Rashid Lamir, A., & Hejazi, S.M. (2018). Are heart muscle irisin levels and FNDC5 gene expression regulated by endurance and resistance exercises? Annals of Applied Sport Science, 6(1), 21-28. [In Persian]. http://aassjournal.com/article-1-524-en.html.
Karimi, R., Fakhrpour, R., & Zarneshan, A. (2022). Effect of resistance training with milk protein concentrate (MPC) supplementation on serum levels of follistatin and myostatin and muscle hypertrophy in beginner bodybuilders. Journal of Applied Health Studies in Sport Physiology, 9(1), 151-163. [In Persian]. https://doi.org/10.22049/JAHSSP.2022.27812.1471.
Khodadadi, H., Rajabi, H., Seyyed Reza Attarzadeh, S.R, & Abbasian, S. (2014). The effect of high intensity interval training (HIIT) and pilates on levels of irisin and insulin resistance in overweight women. Iranian Journal of Endocrinology and Metabolism, 16(3), 190-196. [In Persian]. http://ijem.sbmu.ac.ir/article-1-1709-en.html.
Lanzi, C.R., Perdicaro, D.J., Tudela, J.G., Muscia, V., Fontana, A.R., Oteiza, P.I., & Prieto, M.A.V. (2020). Grape pomace extract supplementation activates FNDC5/irisin in muscle and promotes white adipose browning in rats fed a high-fat diet. Food & Function, 11(2), 1537-1546. https://doi.org/10.1039/C9FO02463H.
McCroskery, S., Thomas, M., Maxwell, L., Sharma, M., & Kambadur, R. (2003). Myostatin negatively regulates satellite cell activation and self-renewal. Journal of Cell Biology, 162(6), 1135-1147. https://doi.org/10.1083/jcb.200207056.
Mohammadi, R., Pourrahim-e- Ghouroghchi. A., & Khajehlandi, M. (2021). The effect of 8 weeks of resistance Ttaining with and without blood flow restriction on serum levels of insulin-like growth factor-1 and myostatin of athletic girls: A semi-experimental study. Journal of Rafsanjan University of Mediacal Sciences, 20(1), 53-68. [In Persian]. http://journal.rums.ac.ir/article-1-5758-en.html.
Mohammadnezhad, G., Matin Homayi, H., & Ghazalian, F. (2020). Effect of a 6-week resistance training program on transforming growth factor Beta-1 and myostatin genes expression in tendons of extensor digitorum longus and soleus muscles in rats. Journal of Arak University of Medical Sciences, 23(1), 82-91. [In Persian]. https://doi.org/10.32598/jams.23.1.5849.1.
Mohammadyari, S., Hadi, H., & Zohrabi, A.R. (2021). The effect of intense intermittent exercise on plasma levels of myostatin and IGF-1 in obese adolescents. Journal of Applied Health Studies in Sport Physiology, 8(2), 18-24. [In Persian]. https://doi.org/10.22049/JAHSSP.2021.27319.1369.
Nezami, S., Sharif, S., & Chezani Sharahi, A. (2017). The effect of resistance training with split method on hormones levels and muscle mass in young bodybuilder. Research in Sport Medicine and Technology, 15(13), 35-48. [In Persian]. http://jsmt.khu.ac.ir/article-1-212-en.html.
Neto, W.K., de Assis Silva, W., de Oliveira, T.V.A., Boas, A.E.D.S.V., Ciena, A.P., Anaruma, C.A., ... & Gama, E.F. (2022). Muscle hypertrophy is correlated with load progression delta, climb volume, and total load volume in rodents undergoing different ladder-based resistance training protocols. Tissue and Cell, 75, 101725. https://doi.org/10.1016/j.tice.2021.101725.
Nikooie, R., Jafari‐Sardoie, S., Sheibani, V., & Nejadvaziri Chatroudi, A. (2020). Resistance training‐induced muscle hypertrophy is mediated by TGF‐β1‐Smad signaling pathway in male Wistar rats. Journal of Cellular Physiology, 235(7-8), 5649-5665. [In Persian]. https://doi.org/10.1002/jcp.29497.
O’Leary, C., & Hackney, A. (2014). Acute and chronic effects of resistance exercise on the testosterone and cortisol responses in obese males: a systematic review. Physiological Research, 63 (6). https://doi.org/10.33549/physiolres.932627.
Pekkala, S., Wiklund, P.K., Hulmi, J.J., Ahtiainen, J.P., Horttanainen, M., Pöllänen, E., ... & Nyman, K. (2013). Are skeletal muscle FNDC5 gene expression and irisin release regulated by exercise and related to health? The Journal of Physiology, 591(21), 5393-5400. https://doi.org/10.1113/jphysiol.2013.263707.
Raschke, S., & Eckel, J. (2013). Adipo-myokines: two sides of the same coin—mediators of inflammation and mediators of exercise. Mediators of Inflammation, page of 320724. https://doi.org/10.1155/2013/320724.
Rashidlamir, A., Hoseinzadeh, M., & Zeiaddini Dashtkhaki, L. (2017). The effects of resistance and endurance training on the liver tissue FNDC5 mRNA gene expression in male rats. Annals of Applied Sport Science, 5(2), 51-60. [In Persian]. https://doi.org/10.18869/acadpub.aassjournal.5.2.51.
Reisi, J., Rajabi, H., Ghaedi, K., Marandi, S.-M., & Dehkhoda, M.-R. (2013). Effect of acute resistance training on plasma irisin protein level and expression of muscle FNDC5 and adipose tissue UCP1 genes in male rats. Journal of Isfahan Medical School, 31(256). [In Persian]
Sabag, A., Najafi, A., Michael, S., Esgin, T., Halaki, M., & Hackett, D. (2018). The compatibility of concurrent high intensity interval training and resistance training for muscular strength and hypertrophy: a systematic review and meta-analysis. Journal of Sports Sciences, 36(21), 2472-2483. https://doi.org/10.1080/02640414.2018.1464636.
Spineti, J., De Salles, B.F., Rhea, M.R., Lavigne, D., Matta, T., Miranda, F., ... & Simão, R. (2010). Influence of exercise order on maximum strength and muscle volume in nonlinear periodized resistance training. The Journal of Strength & Conditioning Research, 24(11), 2962-2969. https://doi.org/10.1519/JSC.0b013e3181e2e19b.
Taylor, W.E., Bhasin, S., Artaza, J., Byhower, F., Azam, M., Willard Jr, D.H., ... & Gonzalez-Cadavid, N. (2001). Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells. American Journal of Physiology-Endocrinology And Metabolism, 280(2), E221-E228. https://doi.org/10.1152/ajpendo.2001.280.2.E221.
Timmons, J.A., Baar, K., Davidsen, P.K., & Atherton, P.J. (2012). Is irisin a human exercise gene? Nature, 488(7413), E9-E10. https://doi.org/10.1038/nature11364.
Trowell, D., Vicenzino, B., Saunders, N., Fox, A., & Bonacci, J. (2020). Effect of strength training on biomechanical and neuromuscular variables in distance runners: a systematic review and meta-analysis. Sports Medicine, 50(1), 133-150. https://doi.org/10.1007/s40279-019-01184-9.
Agascıoglu, E., Çolak, R., & Çakatay, U. (2022). Redox status biomarkers in the fast-twitch extensor digitorum longus resulting from the hypoxic exercise. Nagoya Journal of Medical Science, 84, 433-447. https://doi.org/10.18999/nagjms.84.2.433.
Alizadeh, H., Safarzadeh, A., & Talebi-Garakani, E. (2017). Effect of resistance training on serum meteorin-like hormone level and insulin resistance index in overweight adolescent boys. Journla of Arak University of Medicall Sciences, 20(7), 54-64. [In Persian]. http://jams.arakmu.ac.ir/article-1-5233-fa.html.
Alizadeh, R., Rezaei Nejad, R., Salehpour, M., & Sheikhi, S. (2017). The effect of acute circuit resistance exercise on plasma concentration of Brain-Derived Neurotrophic Factor (BDNF) in young men. Ebnesina, 19(4), 30-37. [In Persian] http://ebnesina.ajaums.ac.ir/article-1-508-en.html
Arabzadeh, E., Shirvani, H., Ebadi Zahmatkesh, M., Riyahi Malayeri, S., Meftahi, G. H., & Rostamkhani, F. (2022). Irisin/FNDC5 influences myogenic markers on skeletal muscle following high and moderate-intensity exercise training in STZ-diabetic rats. 3 Biotech, 12(9), 1-13. [In Persian]. https://doi.org/10.1007/s13205-022-03253-9.
Azimi Dokht, S.M.A., Gharakhanlou, R., Naghdi, N., Khodadadi, D., & Zare Zade Mehrizi, A.A. (2019). The effect of the treadmill running on genes expression ofthePGC-1α, FNDC5 and BDNF in hippocampus of male rats. Journal of Practical Studies of Biosciences in Sport, 7(14), 91-101. [In Persian]. https://doi.org/10.22077/jpsbs.2017.1037.1321.
Bagherpour Tabalvandani, M.M., Fadaei, M.R., & Elmieh, A. (2020). The effect of resistance-aerobic training on the growth of muscle fibers, serum testosterone and androgen receptors on soleus muscles, in different ages groups of male rats. Metabolism and Exercise, 10(2), 111-122. [In Persian]. https://doi.org/10.22124/jme.2021.19982.217.
Bazgir, B., Fathi, R., Valojerdi, M.R., Mozdziak, P., & Asgari, A. (2017). Satellite cells contribution to exercise mediated muscle hypertrophy and repair. Cell Journal (Yakhteh), 18(4), 473. [In Persian]. https://doi.org/10.22074/cellj.2016.4714.
Biglari, S., & Gaeini A. (2019). The effect of eight weeks of High-intensity Interval Training on the gene expression of the myogenic regulatory factors MyF5 and myogenin in the skeletal muscle of rats. Sport and Exercise Physiology, 2(11), 109-116. [In Persian]. https://joeppa.sbu.ac.ir/article_98928.html.
Biglari, S., Afousi, A.G., Mafi, F., & Shabkhiz, F. (2020). High-intensity interval training-induced hypertrophy in gastrocnemius muscle via improved IGF-I/Akt/FoxO and myostatin/Smad signaling pathways in rats. Physiology International, 107(2), 220-230. [In Persian]. https://doi.org/10.1556/2060.2020.00020.
Brenmoehl, J., Albrecht, E., Komolka, K., Schering, L., Langhammer, M., Hoeflich, A., & Maak, S. (2014). Irisin is elevated in skeletal muscle and serum of mice immediately after acute exercise. International Journal of Biological Sciences, 10(3), 338. https://doi.org/10.3389/fpsyg.2011.00226.
Consitt, L.A., & Clark, B.C. (2018). The vicious cycle of myostatin signaling in sarcopenic obesity: myostatin role in skeletal muscle growth, insulin signaling and implications for clinical trials. The Journal of Frailty & Aging, 7(1), 21-27. https://doi.org/10.14283/jfa.2017.33.
Engbers, J.D., Anderson, D., Tadayonnejad, R., Mehaffey, W.H., Molineux, M.L., & Turner, R.W. (2011). Distinct roles for IT and IH in controlling the frequency and timing of rebound spike responses. The Journal of Physiology, 589(22), 5391-5413. https://doi.org/10.1113/jphysiol.2011.215632.
Esazadeh, L., Hosseini Kakhk, A., Khajeie, R., & Hejazi, S.M. (2020). The effect of concurrent training order (resistance-aerobic) on some factors of physical fitness, functional capacity and serum levels of myostatin and follistatin hormones in postmenopausal women (clinical trial). Journal of Sport Biosciences, 12(2), 189-206. [In Persian]. https://doi.org/10.22059/jsb.2020.282311.1345.
Fadaei Chafy, M.R., Mohebbi, H., Rahmani Nia, F., & Arabzadeh, E. (2021). Possible cross-talk between leptin and insulin resistance in sedentary obese boys at different stages of puberty. Journal of Exercise & Organ Cross Talk, 1(1), 15-23. [In Persian]. https://doi.org/10.22034/jeoct.2021.290898.1008.
Farzanegi, P. (2021). TGF-β1 response to eight weeks combined training with different orders in slow and fast twitch muscles in Wistar rats. Razi Journal of Medical Sciences, 28(9), 11-20. [In Persian]. https://doi.org/10.1037/bul0000130.
Hadjizadeh Anvar, S., Kordi, M., Pournemati, P., Farajnia, S., Gharadaghi, N., & Rahmati, M. (2020). The effects of cold water immersion post repeated sprint activity on serum PGC-1α and irisin in young active men. Journal of Practical Studies of Biosciences in Sport, 8(15), 8-20. [In Persian]. https://doi.org/10.22077/jpsbs.2018.993.1313.
Hittel, D.S., Axelson, M., Sarna, N., Shearer, J., Huffman, K.M., & Kraus, W.E. (2010). Myostatin decreases with aerobic exercise and associates with insulin resistance. Medicine and Science in Sports and Exercise, 42(11), 2023. https://doi.org/10.1249/MSS.0b013e3181e0b9a8.
Hosseinzadeh, M., Rashid Lamir, A., & Hejazi, S.M. (2018). Are heart muscle irisin levels and FNDC5 gene expression regulated by endurance and resistance exercises? Annals of Applied Sport Science, 6(1), 21-28. [In Persian]. http://aassjournal.com/article-1-524-en.html.
Karimi, R., Fakhrpour, R., & Zarneshan, A. (2022). Effect of resistance training with milk protein concentrate (MPC) supplementation on serum levels of follistatin and myostatin and muscle hypertrophy in beginner bodybuilders. Journal of Applied Health Studies in Sport Physiology, 9(1), 151-163. [In Persian]. https://doi.org/10.22049/JAHSSP.2022.27812.1471.
Khodadadi, H., Rajabi, H., Seyyed Reza Attarzadeh, S.R, & Abbasian, S. (2014). The effect of high intensity interval training (HIIT) and pilates on levels of irisin and insulin resistance in overweight women. Iranian Journal of Endocrinology and Metabolism, 16(3), 190-196. [In Persian]. http://ijem.sbmu.ac.ir/article-1-1709-en.html.
Lanzi, C.R., Perdicaro, D.J., Tudela, J.G., Muscia, V., Fontana, A.R., Oteiza, P.I., & Prieto, M.A.V. (2020). Grape pomace extract supplementation activates FNDC5/irisin in muscle and promotes white adipose browning in rats fed a high-fat diet. Food & Function, 11(2), 1537-1546. https://doi.org/10.1039/C9FO02463H.
McCroskery, S., Thomas, M., Maxwell, L., Sharma, M., & Kambadur, R. (2003). Myostatin negatively regulates satellite cell activation and self-renewal. Journal of Cell Biology, 162(6), 1135-1147. https://doi.org/10.1083/jcb.200207056.
Mohammadi, R., Pourrahim-e- Ghouroghchi. A., & Khajehlandi, M. (2021). The effect of 8 weeks of resistance Ttaining with and without blood flow restriction on serum levels of insulin-like growth factor-1 and myostatin of athletic girls: A semi-experimental study. Journal of Rafsanjan University of Mediacal Sciences, 20(1), 53-68. [In Persian]. http://journal.rums.ac.ir/article-1-5758-en.html.
Mohammadnezhad, G., Matin Homayi, H., & Ghazalian, F. (2020). Effect of a 6-week resistance training program on transforming growth factor Beta-1 and myostatin genes expression in tendons of extensor digitorum longus and soleus muscles in rats. Journal of Arak University of Medical Sciences, 23(1), 82-91. [In Persian]. https://doi.org/10.32598/jams.23.1.5849.1.
Mohammadyari, S., Hadi, H., & Zohrabi, A.R. (2021). The effect of intense intermittent exercise on plasma levels of myostatin and IGF-1 in obese adolescents. Journal of Applied Health Studies in Sport Physiology, 8(2), 18-24. [In Persian]. https://doi.org/10.22049/JAHSSP.2021.27319.1369.
Nezami, S., Sharif, S., & Chezani Sharahi, A. (2017). The effect of resistance training with split method on hormones levels and muscle mass in young bodybuilder. Research in Sport Medicine and Technology, 15(13), 35-48. [In Persian]. http://jsmt.khu.ac.ir/article-1-212-en.html.
Neto, W.K., de Assis Silva, W., de Oliveira, T.V.A., Boas, A.E.D.S.V., Ciena, A.P., Anaruma, C.A., ... & Gama, E.F. (2022). Muscle hypertrophy is correlated with load progression delta, climb volume, and total load volume in rodents undergoing different ladder-based resistance training protocols. Tissue and Cell, 75, 101725. https://doi.org/10.1016/j.tice.2021.101725.
Nikooie, R., Jafari‐Sardoie, S., Sheibani, V., & Nejadvaziri Chatroudi, A. (2020). Resistance training‐induced muscle hypertrophy is mediated by TGF‐β1‐Smad signaling pathway in male Wistar rats. Journal of Cellular Physiology, 235(7-8), 5649-5665. [In Persian]. https://doi.org/10.1002/jcp.29497.
O’Leary, C., & Hackney, A. (2014). Acute and chronic effects of resistance exercise on the testosterone and cortisol responses in obese males: a systematic review. Physiological Research, 63 (6). https://doi.org/10.33549/physiolres.932627.
Pekkala, S., Wiklund, P.K., Hulmi, J.J., Ahtiainen, J.P., Horttanainen, M., Pöllänen, E., ... & Nyman, K. (2013). Are skeletal muscle FNDC5 gene expression and irisin release regulated by exercise and related to health? The Journal of Physiology, 591(21), 5393-5400. https://doi.org/10.1113/jphysiol.2013.263707.
Raschke, S., & Eckel, J. (2013). Adipo-myokines: two sides of the same coin—mediators of inflammation and mediators of exercise. Mediators of Inflammation, page of 320724. https://doi.org/10.1155/2013/320724.
Rashidlamir, A., Hoseinzadeh, M., & Zeiaddini Dashtkhaki, L. (2017). The effects of resistance and endurance training on the liver tissue FNDC5 mRNA gene expression in male rats. Annals of Applied Sport Science, 5(2), 51-60. [In Persian]. https://doi.org/10.18869/acadpub.aassjournal.5.2.51.
Reisi, J., Rajabi, H., Ghaedi, K., Marandi, S.-M., & Dehkhoda, M.-R. (2013). Effect of acute resistance training on plasma irisin protein level and expression of muscle FNDC5 and adipose tissue UCP1 genes in male rats. Journal of Isfahan Medical School, 31(256). [In Persian]
Sabag, A., Najafi, A., Michael, S., Esgin, T., Halaki, M., & Hackett, D. (2018). The compatibility of concurrent high intensity interval training and resistance training for muscular strength and hypertrophy: a systematic review and meta-analysis. Journal of Sports Sciences, 36(21), 2472-2483. https://doi.org/10.1080/02640414.2018.1464636.
Spineti, J., De Salles, B.F., Rhea, M.R., Lavigne, D., Matta, T., Miranda, F., ... & Simão, R. (2010). Influence of exercise order on maximum strength and muscle volume in nonlinear periodized resistance training. The Journal of Strength & Conditioning Research, 24(11), 2962-2969. https://doi.org/10.1519/JSC.0b013e3181e2e19b.
Taylor, W.E., Bhasin, S., Artaza, J., Byhower, F., Azam, M., Willard Jr, D.H., ... & Gonzalez-Cadavid, N. (2001). Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells. American Journal of Physiology-Endocrinology And Metabolism, 280(2), E221-E228. https://doi.org/10.1152/ajpendo.2001.280.2.E221.
Timmons, J.A., Baar, K., Davidsen, P.K., & Atherton, P.J. (2012). Is irisin a human exercise gene? Nature, 488(7413), E9-E10. https://doi.org/10.1038/nature11364.
Trowell, D., Vicenzino, B., Saunders, N., Fox, A., & Bonacci, J. (2020). Effect of strength training on biomechanical and neuromuscular variables in distance runners: a systematic review and meta-analysis. Sports Medicine, 50(1), 133-150. https://doi.org/10.1007/s40279-019-01184-9.
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