Protective effect of aerobic exercise and concurrent L-carnitine supplementation on renal ischemia-reperfusion injury in male rats
Subject Areas :
Veterinary Clinical Pathology
Omid Azinfam
1
,
Farzad Zehsaz
2
,
Mir Alireza Nourazar
3
1 - Master's Degree Student, Faculty of Humanities, Tabriz Branch, Islamic Azad University, Tabriz, Iran.
2 - Associate Professor, Department of Physical Education, Faculty of Humanities, Tabriz Branch, Islamic Azad University, Tabriz, Iran.
3 - Assistant Professor, Department of Basic Sciences, Faculty of Veterinary Medicine, Tabriz Medical Sciences, Islamic Azad University, Tabriz, Iran.
Received: 2023-03-15
Accepted : 2023-08-06
Published : 2023-04-21
Keywords:
L-carnitine,
kidney,
Ischemia-reperfusion,
Aerobic exercise,
Abstract :
Aerobic exercise and L-carnitine consumption are associated with increasing the activity of antioxidant enzymes and reducing inflammatory processes, but their mechanisms in the face of kidney ischemia-reperfusion injury are not fully known. The aim of this study was to investigate the protective effect of aerobic exercise and L-carnitine consumption simultaneously on renal damage caused by ischemia-reperfusion in male rats. In this experimental study, 42 male Wistar rats were randomly divided into six equal groups and subjected to an eight-week aerobic exercise and six-week L-carnitine intake. At the end, mice were subjected to 45 minutes of kidney ischemia by surgery, and after 24 hours of blood supply, all mice were euthanized at the same time and sampling was done to evaluate the oxidant-antioxidant activity in their renal tissue. Finally, the data were analyzed by one-way analysis of variance (ANOVA) and Tukey's post hoc test using spss-26 software. In the rats of the ischemia-reperfusion group compared to the control group, a significant decrease in the activities of catalase, glutathione peroxidase, superoxide dismutase and total antioxidant capacity and a significant increase in malondialdehyde was observed (p<0.05). The interventions of aerobic exercise and L-carnitine had a significant effect on increasing the activity of catalase, glutathione peroxidase, superoxide dismutase and total antioxidant capacity and reducing malondialdehyde (p<0.05). Performing aerobic exercise and taking L-carnitine supplement at the same time is more effective in terms of increasing antioxidant activities and improving the renal pathological changes of rats, indicating their synergistic effect in protecting the kidney against damage caused by ischemia-reperfusion.
References:
Abreu, C., Cardozo, L., Stockler-Pinto, M.B., Esgalhado, M., Barboza, J.E., Frauches, R., et al. (2017). Does resistance exercise performed during dialysis modulate Nrf2 and NF-κB in patients with chronic kidney disease? Life Sciences, 188(1): 192-197.
Adel, M., Rami, M., Shaheen, D., Monir, R., Basheir, M., Nabawy, A., et al. (2020). L-Carnitine protects kidney against ischemia reperfusion injury via suppression of expression of tubular kidney injury molecule (Kim-1) and Wnt proteins (Beta-Catenin). Bulletin of Egyptian Society for Physiological Sciences, 40(1): 32-45.
Amaral, L.S., Souza, C.S., Lima, H. and Soares, T. (2020). Influence of exercise training on diabetic kidney disease: A brief physiological approach. Experimental Biology and Medicine, 245(13): 1142-1154.
Amouoghli Tabrizi, B. and Mohajeri, D. (2015). Study of the protective effects of crocin on experimental ischemia-reperfusion injury of the liver in rats. Veterinary Clinical Pathology, 9(2): 103-116. [In Persian]
Aydogdu, N., Atmaca, G., Yalcin, O., Taskiran, R., Tastekin, E. and Kaymak, K. (2006). Protective effects of L‐Carnitine on Myoglobinuric acute renal failure in Rats. Clinical and Experimental Pharmacology and Physiology, 33(1‐2): 119-124.
Bhalodia, Y., Kanzariya, N., Patel, R., Patel, N., Vaghasiya, J., Jivani, N., et al. (2009). Renoprotective activity of benincasa cerifera fruit extract on ischemia/reperfusion-induced renal damage in rat. Iranian Journal of Kidney Diseases, 3(2): 80-85.
Borges, J., França, G., Cruz, M., Lanza, R., Nascimento, A. and Lessa, M. (2017). Aerobic exercise training induces superior cardioprotection following myocardial ischemia reperfusion injury than a single aerobic exercise session in rats. Motriz: Revista de Educação Física, 23(Special Issue): 1-5.
Chen, Y., Cheng, C., Liu, C., Sue, Y., Chen, T., Hsu, Y., et al. (2021). Combined protective effects of oligo-fucoidan, fucoxanthin, and L-carnitine on the kidneys of chronic kidney disease mice. European Journal of Pharmacology, 892(5): 173-708.
Cipryan, L. (2018). The effect of fitness level on cardiac autonomic regulation, IL-6, total antioxidant capacity, and muscle damage responses to a single bout of high-intensity interval training. Journal of Sport and Health Science, 7(3): 363-371.
Coelho, B., Rocha, L., Scarabelot, K., Scheffer, D., Ronsani, M., Silveira, P., et al. (2010). Physical exercise prevents the exacerbation of oxidative stress parameters in chronic kidney disease. Journal of Renal Nutrition, 20(3): 169-175.
de Lima, W.V., Visona, I., Schor, N. and Almeida, W.S. (2019). Preconditioning by aerobic exercise reduces acute ischemic renal injury in rats. Physiological Reports, 7(14): 14-176.
de Sousa, C.V., Sales, M., Rosa, T.S., Lewis, J.E., de Andrade, R. and Simões, H. (2017). The antioxidant effect of exercise: a systematic review and meta-analysis. Sports Medicine, 47(2): 277-293.
Ding, Y.H., Mrizek, M., Lai, Q., Wu, Y., Reyes, R., Li, J., et al. (2006). Exercise preconditioning reduces brain damage and inhibits TNF-α receptor expression after hypoxia/reoxygenation: an in vivo and in vitro study. Current Neurovascular Research, 3(4): 263-271.
Dokmeci, D., Inan, M., Basaran, U., Yalcin, O., Aydogdu, N., Turan, F., et al. (2007). Protective effect of L‐carnitine on testicular ischaemia–reperfusion injury in rats. Cell Biochemistry and Function: Cellular Biochemistry and its Modulation by Active Agents or Disease, 25(6): 611-618.
Dostar Y. (2017). Protective study of regular aerobic exercise on heart ischemia-reperfusion injury in rats. Comparative Pathobiology 14(4): 2333-2344. [In Persian]
Estrela, G., Wasinski, F., Batista, R., Hiyane, M., Felizardo, R., Cunha, F., et al. (2017). Caloric restriction is more efficient than physical exercise to protect from cisplatin nephrotoxicity via PPAR-alpha activation. Frontiers in Physiology, 2(8): 116.
Faleiros, C., Francescato, H., Papoti, M., Chaves, L., Silva, C., Costa, R., et al. (2017). Effects of previous physical training on Adriamycin nephropathy and its relationship with endothelial lesions and angiogenesis in the renal cortex. Life Sciences, 169(15): 43-51.
Fathizadeh, H., Milajerdi, A., Reiner, Ž., Amirani, E., Asemi, Z., Mansournia, M., et al. (2020). The effects of L-carnitine supplementation on indicators of inflammation and oxidative stress: a systematic review and meta-analysis of randomized controlled trials. Journal of Diabetes & Metabolic Disorders, 19(2): 1879-1894. [In Persian]
Ferreira, G. and McKenna, M. (2017). L-Carnitine and acetyl-L-carnitine roles and neuroprotection in developing brain. Neurochemical Research, 42(6): 1661-1675.
Francescato, H.D., Almeida, L.F., Reis, N.G., Faleiros, C.M., Papoti, M., Costa, R., et al. (2018). Previous exercise effects in cisplatin-induced renal lesions in rats. Kidney and Blood Pressure Research, 43(2): 582-593.
Giudetti, A., Stanca, E., Siculella, L., Gnoni, G. and Damiano, F. (2016). Nutritional and hormonal regulation of citrate and carnitine/acylcarnitine transporters: two mitochondrial carriers involved in fatty acid metabolism. International Journal of Molecular Sciences, 17(6): 817.
Gomez-Cabrera, M.C., Salvador-Pascual, A., Cabo, H., Ferrando, B., and Viña, J. (2015). Redox modulation of mitochondriogenesis in exercise. Does antioxidant supplementation blunt the benefits of exercise training? Free Radical Biology and Medicine, 86(1): 37-46.
Hong, X., Zhao, X., Wang, G., Zhang, Z., Pei, H. and Liu, Z. (2017). Luteolin treatment protects against renal ischemia-reperfusion injury in rats. Mediators of inflammation, 2017 (Article ID; 9783893): 1-10.
Kart, A., Yapar, K., Karapehlivan, M., Tunca, R., Ogun, M. and Citil, M. (2006). Effects of L-carnitine on kidney histopathology, plasma and tissue total sialic acid, malondialdehyde and glutathione concentrations in response to gentamicin administration in Balb/C mice. Revue de Médecine Vétérinaire, 157(4): 179-184.
Kavouras, S.A., Panagiotakos, D.B., Pitsavos, C., Chrysohoou, C., Arnaoutis, G., Skoumas, Y., et al. (2010). Physical activity and adherence to Mediterranean diet increase total antioxidant capacity: The ATTICA study. Cardiology Research and Practice, 10(20): 21-28.
Koohpeyma, F., Siri, M., Allahyari, S., Mahmoodi, M., Saki, F. and Dastghaib, S. (2021). The effects of L-carnitine on renal function and gene expression of caspase-9 and Bcl-2 in monosodium glutamate‐induced rats. BMC Nephrology, 22(1): 1-11. [In Persian]
Lee, J., Park, S. and Kim, W. (2013). Exercise preconditioning reduces acute ischemic renal injury in Hsp70. 1 knockout mouse. Histology and Histopathology, 28(9): 1223-1232.
Liu, H.., Kao, H. and Wu, C. (2019). Exercise training upregulates SIRT1 to attenuate inflammation and metabolic dysfunction in kidney and liver of diabetic db/db mice. Nutrition & Metabolism, 16(1): 1-10.
Malek, M. and Nematbakhsh, M. (2015). Renal ischemia/reperfusion injury; from pathophysiology to treatment. Journal of Renal Injury Prevention, 4(2): 20-27. [In Persian]
Mas-Bargues, C., Escrivá, C., Dromant, M., Borrás, C. and Viña, J. (2021). Lipid peroxidation as measured by chromatographic determination of malondialdehyde. Human plasma reference values in health and disease. Archives of Biochemistry and Biophysics, 709(9): 10-16.
Moecke, D., Martins, G., Garlet, T., Bonorino, K., Luciani, M., Bion, M., et al. (2022). Aerobic Exercise Attenuates Kidney Injury, Improves Physical Performance, and Increases Antioxidant Defenses in Lungs of Adenine-Induced Chronic Kidney Disease Mice. Inflammation, 45(5): 1895-1910.
Mohajeri, D., Mousavi, G. and Mohammadi, P. (2013). Histopathological study of the effect of alcoholic extract of turnip root on kidney ischemia-reperfusion injury in rats. Veterinary Clinical Pathology, 6(2): 1549-1559. [In Persian]
Moraes, C., Marinho, S., Da Nobrega, A., de Oliveira Bessa, B., Jacobson, L., Stockler-Pinto, M., et al. (2014). Resistance exercise: a strategy to attenuate inflammation and protein-energy wasting in hemodialysis patients? International Urology and Nephrology, 46(8): 1655-1662.
Nameni, F. and nuranipilehrud, M. (2019). Comparing the Effects of Curcumin Supplementation and that of L-Carnitine Supplementation on Superoxide Dismutase, Glutathione Peroxidase, Catalase and Glutathione Reductase after Acute Exercise. Complementary Medicine Journal, 8(4): 3517-3530. [In Persian]
Nasirzadeh, M., Noorazar, M. and Roshangar, L. (2014). The effect of olive leaf alcoholic extract on renal ischemia-reperfusion injury in adult male rats. Veterinary Clinical Pathology, 8(1): 373-382. [In Persian]
Paula, S. M., Fernandes, T., Couto, G., Jordão, M., Oliveira, E., Michelini, L., et al. (2020). Molecular Pathways Involved in Aerobic Exercise Training Enhance Vascular Relaxation. Medicine and Science in Sports and Exercise, 52(10): 2117-2126.
Peake, J., Suzuki, K. and Coombes, J. (2007). The influence of antioxidant supplementation on markers of inflammation and the relationship to oxidative stress after exercise. The Journal of Nutritional Biochemistry, 18(6): 357-371.
Perico, N., Cattaneo, D., Sayegh, M. and Remuzzi, G. (2004). Delayed graft function in kidney transplantation. The Lancet, 364(9447): 1814-1827.
Rahimi, A., Kasbparast, M., Noura, M. and Kheirdeh, M. (2020). Combined effects of aerobic exercises and l-arginine ingestion on total antioxidant capacity (TAC) and C-reactive protein (CRP) in diabetic male rats. Journal of Physical Activity and Hormones, 4(3): 1-16. [In Persian]
Sahin, K., Tuzcu, M., Sahin, N., Ali, S. and Kucuk, O. (2010). Nrf2/HO-1 signaling pathway may be the prime target for chemoprevention of cisplatin-induced nephrotoxicity by lycopene. Food and Chemical Toxicology, 48(10): 2670-2674.
Sancaktutar, A., Bodakci, M., Hatipoglu, N., Soylemez, H., Basarılı, K. and Turkcu, G., (2014). The protective effects of pomegranate extracts against renal ischemia-reperfusion injury in male rats. Urology Annals, 6(1): 46-50.
Şıktar, E., Ekinci, D., Şıktar, E., Beydemir, Ş., Gülçin, İ. and Günay, M. (2011). Protective role of L-carnitine supplementation against exhaustive exercise induced oxidative stress in rats. European Journal of Pharmacology, 668(3): 407-413.
Tang, L., Wang, B. and Wu, Z. (2018). Aerobic exercise training alleviates renal injury by interfering with mitochondrial function in type-1 diabetic mice. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 24(18): 9081-9089.
Tousson, E., Keshta, A., Hussein, Y., Fekry, R. and Abo-Ghaneima, W. (2019). Renal protective effect of ginkgo biloba and L-carnitine extracts against pentylenetetrazol induced toxicity, oxidative stress, injury and proliferation alternation in epileptic rats. Annual Research & Review in Biology, 28(6): 1-13.
Vafamand, E., Bolboli, L., Talebi, A. and Nematbakhsh, M. (2017). The role of L-arginine and aerobic exercise in experimental renal ischemia reperfusion injury in male and female rats. Hormozgan Medical Journal, 21(1): 20-27. [In Persian]
Zarrindast, S., Ramezanpour, M. and Moghaddam, M. (2021). Effects of eight weeks of moderate intensity aerobic training and training in water on DNA damage, lipid peroxidation and total antioxidant capacity in sixty years sedentary women. Science & Sports, 36(3): 81-85. [In Persian]
Zheng, H., Zhang, H., Zhu, C., Li, H., Cui, S., Jin, J., et al. (2021). L-Carnitine protects against tacrolimus-induced renal injury by attenuating programmed cell death via PI3K/AKT/PTEN signaling. Acta Pharmacologica Sinica, 42(1): 77-87.
_||_
Abreu, C., Cardozo, L., Stockler-Pinto, M.B., Esgalhado, M., Barboza, J.E., Frauches, R., et al. (2017). Does resistance exercise performed during dialysis modulate Nrf2 and NF-κB in patients with chronic kidney disease? Life Sciences, 188(1): 192-197.
Adel, M., Rami, M., Shaheen, D., Monir, R., Basheir, M., Nabawy, A., et al. (2020). L-Carnitine protects kidney against ischemia reperfusion injury via suppression of expression of tubular kidney injury molecule (Kim-1) and Wnt proteins (Beta-Catenin). Bulletin of Egyptian Society for Physiological Sciences, 40(1): 32-45.
Amaral, L.S., Souza, C.S., Lima, H. and Soares, T. (2020). Influence of exercise training on diabetic kidney disease: A brief physiological approach. Experimental Biology and Medicine, 245(13): 1142-1154.
Amouoghli Tabrizi, B. and Mohajeri, D. (2015). Study of the protective effects of crocin on experimental ischemia-reperfusion injury of the liver in rats. Veterinary Clinical Pathology, 9(2): 103-116. [In Persian]
Aydogdu, N., Atmaca, G., Yalcin, O., Taskiran, R., Tastekin, E. and Kaymak, K. (2006). Protective effects of L‐Carnitine on Myoglobinuric acute renal failure in Rats. Clinical and Experimental Pharmacology and Physiology, 33(1‐2): 119-124.
Bhalodia, Y., Kanzariya, N., Patel, R., Patel, N., Vaghasiya, J., Jivani, N., et al. (2009). Renoprotective activity of benincasa cerifera fruit extract on ischemia/reperfusion-induced renal damage in rat. Iranian Journal of Kidney Diseases, 3(2): 80-85.
Borges, J., França, G., Cruz, M., Lanza, R., Nascimento, A. and Lessa, M. (2017). Aerobic exercise training induces superior cardioprotection following myocardial ischemia reperfusion injury than a single aerobic exercise session in rats. Motriz: Revista de Educação Física, 23(Special Issue): 1-5.
Chen, Y., Cheng, C., Liu, C., Sue, Y., Chen, T., Hsu, Y., et al. (2021). Combined protective effects of oligo-fucoidan, fucoxanthin, and L-carnitine on the kidneys of chronic kidney disease mice. European Journal of Pharmacology, 892(5): 173-708.
Cipryan, L. (2018). The effect of fitness level on cardiac autonomic regulation, IL-6, total antioxidant capacity, and muscle damage responses to a single bout of high-intensity interval training. Journal of Sport and Health Science, 7(3): 363-371.
Coelho, B., Rocha, L., Scarabelot, K., Scheffer, D., Ronsani, M., Silveira, P., et al. (2010). Physical exercise prevents the exacerbation of oxidative stress parameters in chronic kidney disease. Journal of Renal Nutrition, 20(3): 169-175.
de Lima, W.V., Visona, I., Schor, N. and Almeida, W.S. (2019). Preconditioning by aerobic exercise reduces acute ischemic renal injury in rats. Physiological Reports, 7(14): 14-176.
de Sousa, C.V., Sales, M., Rosa, T.S., Lewis, J.E., de Andrade, R. and Simões, H. (2017). The antioxidant effect of exercise: a systematic review and meta-analysis. Sports Medicine, 47(2): 277-293.
Ding, Y.H., Mrizek, M., Lai, Q., Wu, Y., Reyes, R., Li, J., et al. (2006). Exercise preconditioning reduces brain damage and inhibits TNF-α receptor expression after hypoxia/reoxygenation: an in vivo and in vitro study. Current Neurovascular Research, 3(4): 263-271.
Dokmeci, D., Inan, M., Basaran, U., Yalcin, O., Aydogdu, N., Turan, F., et al. (2007). Protective effect of L‐carnitine on testicular ischaemia–reperfusion injury in rats. Cell Biochemistry and Function: Cellular Biochemistry and its Modulation by Active Agents or Disease, 25(6): 611-618.
Dostar Y. (2017). Protective study of regular aerobic exercise on heart ischemia-reperfusion injury in rats. Comparative Pathobiology 14(4): 2333-2344. [In Persian]
Estrela, G., Wasinski, F., Batista, R., Hiyane, M., Felizardo, R., Cunha, F., et al. (2017). Caloric restriction is more efficient than physical exercise to protect from cisplatin nephrotoxicity via PPAR-alpha activation. Frontiers in Physiology, 2(8): 116.
Faleiros, C., Francescato, H., Papoti, M., Chaves, L., Silva, C., Costa, R., et al. (2017). Effects of previous physical training on Adriamycin nephropathy and its relationship with endothelial lesions and angiogenesis in the renal cortex. Life Sciences, 169(15): 43-51.
Fathizadeh, H., Milajerdi, A., Reiner, Ž., Amirani, E., Asemi, Z., Mansournia, M., et al. (2020). The effects of L-carnitine supplementation on indicators of inflammation and oxidative stress: a systematic review and meta-analysis of randomized controlled trials. Journal of Diabetes & Metabolic Disorders, 19(2): 1879-1894. [In Persian]
Ferreira, G. and McKenna, M. (2017). L-Carnitine and acetyl-L-carnitine roles and neuroprotection in developing brain. Neurochemical Research, 42(6): 1661-1675.
Francescato, H.D., Almeida, L.F., Reis, N.G., Faleiros, C.M., Papoti, M., Costa, R., et al. (2018). Previous exercise effects in cisplatin-induced renal lesions in rats. Kidney and Blood Pressure Research, 43(2): 582-593.
Giudetti, A., Stanca, E., Siculella, L., Gnoni, G. and Damiano, F. (2016). Nutritional and hormonal regulation of citrate and carnitine/acylcarnitine transporters: two mitochondrial carriers involved in fatty acid metabolism. International Journal of Molecular Sciences, 17(6): 817.
Gomez-Cabrera, M.C., Salvador-Pascual, A., Cabo, H., Ferrando, B., and Viña, J. (2015). Redox modulation of mitochondriogenesis in exercise. Does antioxidant supplementation blunt the benefits of exercise training? Free Radical Biology and Medicine, 86(1): 37-46.
Hong, X., Zhao, X., Wang, G., Zhang, Z., Pei, H. and Liu, Z. (2017). Luteolin treatment protects against renal ischemia-reperfusion injury in rats. Mediators of inflammation, 2017 (Article ID; 9783893): 1-10.
Kart, A., Yapar, K., Karapehlivan, M., Tunca, R., Ogun, M. and Citil, M. (2006). Effects of L-carnitine on kidney histopathology, plasma and tissue total sialic acid, malondialdehyde and glutathione concentrations in response to gentamicin administration in Balb/C mice. Revue de Médecine Vétérinaire, 157(4): 179-184.
Kavouras, S.A., Panagiotakos, D.B., Pitsavos, C., Chrysohoou, C., Arnaoutis, G., Skoumas, Y., et al. (2010). Physical activity and adherence to Mediterranean diet increase total antioxidant capacity: The ATTICA study. Cardiology Research and Practice, 10(20): 21-28.
Koohpeyma, F., Siri, M., Allahyari, S., Mahmoodi, M., Saki, F. and Dastghaib, S. (2021). The effects of L-carnitine on renal function and gene expression of caspase-9 and Bcl-2 in monosodium glutamate‐induced rats. BMC Nephrology, 22(1): 1-11. [In Persian]
Lee, J., Park, S. and Kim, W. (2013). Exercise preconditioning reduces acute ischemic renal injury in Hsp70. 1 knockout mouse. Histology and Histopathology, 28(9): 1223-1232.
Liu, H.., Kao, H. and Wu, C. (2019). Exercise training upregulates SIRT1 to attenuate inflammation and metabolic dysfunction in kidney and liver of diabetic db/db mice. Nutrition & Metabolism, 16(1): 1-10.
Malek, M. and Nematbakhsh, M. (2015). Renal ischemia/reperfusion injury; from pathophysiology to treatment. Journal of Renal Injury Prevention, 4(2): 20-27. [In Persian]
Mas-Bargues, C., Escrivá, C., Dromant, M., Borrás, C. and Viña, J. (2021). Lipid peroxidation as measured by chromatographic determination of malondialdehyde. Human plasma reference values in health and disease. Archives of Biochemistry and Biophysics, 709(9): 10-16.
Moecke, D., Martins, G., Garlet, T., Bonorino, K., Luciani, M., Bion, M., et al. (2022). Aerobic Exercise Attenuates Kidney Injury, Improves Physical Performance, and Increases Antioxidant Defenses in Lungs of Adenine-Induced Chronic Kidney Disease Mice. Inflammation, 45(5): 1895-1910.
Mohajeri, D., Mousavi, G. and Mohammadi, P. (2013). Histopathological study of the effect of alcoholic extract of turnip root on kidney ischemia-reperfusion injury in rats. Veterinary Clinical Pathology, 6(2): 1549-1559. [In Persian]
Moraes, C., Marinho, S., Da Nobrega, A., de Oliveira Bessa, B., Jacobson, L., Stockler-Pinto, M., et al. (2014). Resistance exercise: a strategy to attenuate inflammation and protein-energy wasting in hemodialysis patients? International Urology and Nephrology, 46(8): 1655-1662.
Nameni, F. and nuranipilehrud, M. (2019). Comparing the Effects of Curcumin Supplementation and that of L-Carnitine Supplementation on Superoxide Dismutase, Glutathione Peroxidase, Catalase and Glutathione Reductase after Acute Exercise. Complementary Medicine Journal, 8(4): 3517-3530. [In Persian]
Nasirzadeh, M., Noorazar, M. and Roshangar, L. (2014). The effect of olive leaf alcoholic extract on renal ischemia-reperfusion injury in adult male rats. Veterinary Clinical Pathology, 8(1): 373-382. [In Persian]
Paula, S. M., Fernandes, T., Couto, G., Jordão, M., Oliveira, E., Michelini, L., et al. (2020). Molecular Pathways Involved in Aerobic Exercise Training Enhance Vascular Relaxation. Medicine and Science in Sports and Exercise, 52(10): 2117-2126.
Peake, J., Suzuki, K. and Coombes, J. (2007). The influence of antioxidant supplementation on markers of inflammation and the relationship to oxidative stress after exercise. The Journal of Nutritional Biochemistry, 18(6): 357-371.
Perico, N., Cattaneo, D., Sayegh, M. and Remuzzi, G. (2004). Delayed graft function in kidney transplantation. The Lancet, 364(9447): 1814-1827.
Rahimi, A., Kasbparast, M., Noura, M. and Kheirdeh, M. (2020). Combined effects of aerobic exercises and l-arginine ingestion on total antioxidant capacity (TAC) and C-reactive protein (CRP) in diabetic male rats. Journal of Physical Activity and Hormones, 4(3): 1-16. [In Persian]
Sahin, K., Tuzcu, M., Sahin, N., Ali, S. and Kucuk, O. (2010). Nrf2/HO-1 signaling pathway may be the prime target for chemoprevention of cisplatin-induced nephrotoxicity by lycopene. Food and Chemical Toxicology, 48(10): 2670-2674.
Sancaktutar, A., Bodakci, M., Hatipoglu, N., Soylemez, H., Basarılı, K. and Turkcu, G., (2014). The protective effects of pomegranate extracts against renal ischemia-reperfusion injury in male rats. Urology Annals, 6(1): 46-50.
Şıktar, E., Ekinci, D., Şıktar, E., Beydemir, Ş., Gülçin, İ. and Günay, M. (2011). Protective role of L-carnitine supplementation against exhaustive exercise induced oxidative stress in rats. European Journal of Pharmacology, 668(3): 407-413.
Tang, L., Wang, B. and Wu, Z. (2018). Aerobic exercise training alleviates renal injury by interfering with mitochondrial function in type-1 diabetic mice. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 24(18): 9081-9089.
Tousson, E., Keshta, A., Hussein, Y., Fekry, R. and Abo-Ghaneima, W. (2019). Renal protective effect of ginkgo biloba and L-carnitine extracts against pentylenetetrazol induced toxicity, oxidative stress, injury and proliferation alternation in epileptic rats. Annual Research & Review in Biology, 28(6): 1-13.
Vafamand, E., Bolboli, L., Talebi, A. and Nematbakhsh, M. (2017). The role of L-arginine and aerobic exercise in experimental renal ischemia reperfusion injury in male and female rats. Hormozgan Medical Journal, 21(1): 20-27. [In Persian]
Zarrindast, S., Ramezanpour, M. and Moghaddam, M. (2021). Effects of eight weeks of moderate intensity aerobic training and training in water on DNA damage, lipid peroxidation and total antioxidant capacity in sixty years sedentary women. Science & Sports, 36(3): 81-85. [In Persian]
Zheng, H., Zhang, H., Zhu, C., Li, H., Cui, S., Jin, J., et al. (2021). L-Carnitine protects against tacrolimus-induced renal injury by attenuating programmed cell death via PI3K/AKT/PTEN signaling. Acta Pharmacologica Sinica, 42(1): 77-87.