View More View Less
  • 1 Tabriz University of Medical Sciences, Iran
  • 2 Tabriz University of Medical Sciences, Iran
  • 3 Urmia University of Medical Sciences, Iran
  • 4 Urmia University of Medical Sciences, Iran
  • 5 Tabriz University of Medical Sciences, Iran
Restricted access

Introduction

Elevated oxidative stress in type 2 diabetes mellitus (T2DM) has been proposed as one of the major risk factors in pathophysiology of several organ damages including liver tissue.

Materials and methods

In this study, we evaluated the effect of swimming training on hepatic oxidative markers, SIRT1 gene expression, and histological alterations in T2DM. Twenty-eight male Wistar rats were randomly assigned into four groups (N = 7): control, exercise, diabetic, and diabetic + exercise. One week after the induction of T2DM, rats were subjected to swimming (60 min/5 days a week) for 12 weeks. At the end of the experiment, oxidative markers (SOD, GPx, CAT activities, and MDA level) and SIRT1 gene expression were measured in the liver by special kits and RT-PCR, respectively. Hematoxylin–eosin statins were used for histological alterations.

Results

Swimming training attenuated MDA levels and enhanced SOD, GPx, and CAT activities in the liver of diabetic animals. Furthermore, swimming training restored the expression of SIRT1 in T2DM. Histopathological finding of the hepatic tissue confirmed a protective role for swimming training in diabetic rats.

Conclusion

Our findings indicate that swimming training attenuates oxidative stress probably by upregulation of SIRT1 in the liver of type 2 diabetic rats.

  • Aebi, H. (1984) Catalase in vitro. Methods Enzymol. 105, 121126.

  • Al-Busafi, S. A., Bhat, M., Wong, P., Ghali, P., Deschenes, M. (2012) Antioxidant therapy in nonalcoholic steatohepatitis. Hepat. Res. Treat. 2012, 947575.

    • Search Google Scholar
    • Export Citation
  • Biyashev, D., Veliceasa, D., Topczewski, J., Topczewska, J. M., Mizgirev, I., Vinokour, E., Reddi, A. L., Licht, J. D., Revskoy, S. Y., Volpert, O. V. (2012) miR-27b controls venous specification and tip cell fate. Blood 119, 26792687.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Blander, G., Guarente, L. (2004) The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73, 417435.

  • Cao, M. M., Lu, X., Liu, G. D., Su, Y., Li, Y. B., Zhou, J. (2018) Resveratrol attenuates type 2 diabetes mellitus by mediating mitochondrial biogenesis and lipid metabolism via Sirtuin type 1. Exp. Ther. Med. 15, 576584.

    • Search Google Scholar
    • Export Citation
  • Chiş, I., Mureşan, A., Oros, A., Nagy, A., Clichici, S. (2016) Protective effects of quercetin and chronic moderate exercise (training) against oxidative stress in the liver tissue of streptozotocin-induced diabetic rats. Acta Physiol. Hung. 103, 4964.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cho, J., Lee, I., Kim, D., Koh, Y., Kong, J., Lee, S., Kang, H. (2014) Effect of aerobic exercise training on non-alcoholic fatty liver disease induced by a high fat diet in C57BL/6 mice. J. Exerc. Nutr. Biochem. 18, 339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Colak, Y., Ozturk, O., Senates, E., Tuncer, I., Yorulmaz, E., Adali, G., Doganay, L., Enc, F. Y. (2011) SIRT1 as a potential therapeutic target for treatment of nonalcoholic fatty liver disease. Med. Sci Monit. 17, HY5.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Dart, A. B., Martens, P. J., Rigatto, C., Brownell, M. D., Dean, H. J., Sellers, E. A. (2014) Earlier onset of complications in youth with type 2 diabetes. Diabetes Care 37, 436443.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • de Bem, G. F., da Costa, C. A., Cordeiro, V. D. S. C., Santos, I. B., de Carvalho, L. C. R. M., de Andrade Soares, R., Ribeiro, J. H., de Souza, M. A. V., da Cunha Sousa, P. J., Ognibene, D. T. (2018) Euterpe oleracea Mart. (açaí) seed extract associated with exercise training reduces hepatic steatosis in type 2 diabetic male rats. J. Nutr. Biochem. 52, 7081.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Delmas-Beauvieux, M. C., Peuchant, E., Couchouron, A., Constans, J., Sergeant, C., Simonoff, M., Pellegrin, J. L., Leng, B., Conri, C., Clerc, M. (1996) The enzymatic antioxidant system in blood and glutathione status in human immunodeficiency virus (HIV)-infected patients: effects of supplementation with selenium or beta-carotene. Am. J. Clin. Nutr. 64, 101107.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Franz, M. J., Boucher, J. L., Rutten-Ramos, S., VanWormer, J. J. (2015) Lifestyle weight-loss intervention outcomes in overweight and obese adults with type 2 diabetes: a systematic review and meta-analysis of randomized clinical trials. J. Acad. Nutr. Diet. 115, 14471463.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ghiasi, R., Soufi, F. G., Hossein Somi, M., Mohaddes, G., Bavil, F. M., Naderi, R., Alipour, M. R. (2015) Swim training improves HOMA-IR in type 2 diabetes induced by high fat diet and low dose of streptozotocin in male rats. Adv. Pharm. Bull. 5, 379.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Han, J., Wei, M., Wang, Q., Li, X., Zhu, C., Mao, Y., Wei, L., Sun, Y., Jia, W. (2015) Association of genetic variants of SIRT1 with type 2 diabetes mellitus. Gene Expr. 16, 177185.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Iskender, H., Dokumacioglu, E., Sen, T. M., Ince, I., Kanbay, Y., Saral, S. (2017) The effect of hesperidin and quercetin on oxidative stress, NF-κB and SIRT1 levels in a STZ-induced experimental diabetes model. Biomed. Pharmacother. 90, 500508.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kakarla, P., Vadluri, G., Reddy Kesireddy, S. (2005) Response of hepatic antioxidant system to exercise training in aging female rat. J. Exp. Zoolog. A Comp. Exp. Biol. 303, 203208.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kitada, M., Kume, S., Kanasaki, K., Takeda-Watanabe, A., Koya, D. (2013) Sirtuins as possible drug targets in type 2 diabetes. Curr. Drug Targets 14, 622636.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Klisic, A., Isakovic, A., Kocic, G., Kavaric, N., Jovanovic, M., Zvrko, E., Skerovic, V., Ninic, A. (2018) Relationship between oxidative stress, inflammation and dyslipidemia with fatty liver index in patients with type 2 diabetes mellitus. Exp. Clin. Endocrinol. Diabetes 126, 371378.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lässer, C., Eldh, M., Lötvall, J. (2012) Isolation and characterization of RNA-containing exosomes. J. Vis. Exp. 59, e3037.

  • Lima, F. D., Stamm, D. N., Della-Pace, I. D., Dobrachinski, F., de Carvalho, N. R., Royes, L. F. F., Soares, F. A., Rocha, J. B., González-Gallego, J., Bresciani, G. (2013) Swimming training induces liver mitochondrial adaptations to oxidative stress in rats submitted to repeated exhaustive swimming bouts. PLoS One 8, e55668.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Liu, H., Sheng, M., Liu, Y., Wang, P., Chen, Y., Chen, L., Wang, W., Li, B. (2015) Expression of SIRT1 and oxidative stress in diabetic dry eye. Int. J. Clin. Exp. Pathol. 8, 7644.

    • Search Google Scholar
    • Export Citation
  • Liu, P., Feng, T., Zuo, X., Wang, X., Luo, J., Li, N., Han, X., Zhu, N., Xu, S., Xu, Y. (2018) A novel SIRT1 activator E6155 improves insulin sensitivity in type 2 diabetic KKAy mice. Biochem. Biophys. Res. Commun. 498, 633639.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lovis, P., Gattesco, S., Regazzi, R. (2008) Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs. Biol. Chem. 389, 305312.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mohammadi, M., Ghaznavi, R., Keyhanmanesh, R., Sadeghipour, H. R., Naderi, R., Mohammadi, H. (2013) Voluntary exercise prevents lead-induced elevation of oxidative stress and inflammation markers in male rat blood. Sci. World J. 2013.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Naderi, R., Mohaddes, G., Mohammadi, M., Alihemmati, A., Badalzadeh, R., Ghaznavi, R., Ghyasi, R., Mohammadi, S. (2015a) Preventive effects of garlic (Allium sativum) on oxidative stress and histopathology of cardiac tissue in streptozotocin-induced diabetic rats. Acta Physiol. Hung. 102, 380390.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Naderi, R., Mohaddes, G., Mohammadi, M., Ghaznavi, R., Ghyasi, R., Vatankhah, A. M. (2015b) Voluntary exercise protects heart from oxidative stress in diabetic rats. Adv. Pharm. Bull. 5, 231.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nassir, F., Ibdah, J. A. (2016) Sirtuins and nonalcoholic fatty liver disease. World J. Gastroenterol. 22, 10084.

  • Oliveira, V. N. D., Bessa, A., Jorge, M. L. M. P., Oliveira, R. J. D. S., de Mello, M. T., De Agostini, G. G., Jorge, P. T., Espindola, F. S. (2012) The effect of different training programs on antioxidant status, oxidative stress, and metabolic control in type 2 diabetes. Appl. Physiol. Nutr. Metab. 37, 334344.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Padiya, R., Khatua, T. N., Bagul, P. K., Kuncha, M., Banerjee, S. K. (2011) Garlic improves insulin sensitivity and associated metabolic syndromes in fructose fed rats. Nutr. Metab. 8, 53.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Paglia, D. E., Valentine, W. N. (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70, 158169.

    • Search Google Scholar
    • Export Citation
  • Smith, B. W., Adams, L. A. (2011) Nonalcoholic fatty liver disease and diabetes mellitus: pathogenesis and treatment. Nat. Rev. Endocrinol. 7, 456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Song, R., Xu, W., Chen, Y., Li, Z., Zeng, Y., Fu, Y. (2011) The expression of Sirtuins 1 and 4 in peripheral blood leukocytes from patients with type 2 diabetes. Eur. J. Histochem. 55, e10.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Szkudelski, T., Szkudelska, K. (2015) Resveratrol and diabetes: from animal to human studies. Biochim. Biophys. Acta 1852, 11451154.

  • Tucker, P. S., Fisher-Wellman, K., Bloomer, R. J. (2008) Can exercise minimize postprandial oxidative stress in patients with type 2 diabetes? Curr. Diabetes Rev. 4, 309319.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wilson, D., Johnson, P. (2000) Exercise modulates antioxidant enzyme gene expression in rat myocardium and liver. J. Appl. Physiol. 88, 17911796.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wu, H., Jin, M., Han, D., Zhou, M., Mei, X., Guan, Y., Liu, C. (2015) Protective effects of aerobic swimming training on high-fat diet induced nonalcoholic fatty liver disease: regulation of lipid metabolism via PANDER-AKT pathway. Biochem. Biophys. Res. Commun. 458, 862868.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Xu, J., Li, N., Wang, J., Zhang, C., Ding, S., Jiao, Y. (2012) Hepatic SIRT1 and UCP2 expressions in rats with type 2 diabetes mellitus and nonalcoholic fatty liver. Nan fang yi ke da xue xue bao [J. South. Med. Univ.] 32, 726729.

    • Search Google Scholar
    • Export Citation
  • Xu, J., Li, N., Wang, J., Zhang, C., Ding, S., Jiao, Y., Zhang, J. (2013) Effect of metformin on the expression of SIRT1 and UCP2 in rat liver of type 2 diabetes mellitus and nonalcoholic fatty liver. Zhong Nan Da Xue Xue Bao Yi Xue Ban 38, 882887.

    • Search Google Scholar
    • Export Citation
  • Yamazaki, Y., Usui, I., Kanatani, Y., Matsuya, Y., Tsuneyama, K., Fujisaka, S., Bukhari, A., Suzuki, H., Senda, S., Imanishi, S. (2009) Treatment with SRT1720, a SIRT1 activator, ameliorates fatty liver with reduced expression of lipogenic enzymes in MSG mice. Am. J. Physiol. Endocrinol. Metab. 297, E1179E1186.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yang, Q., Wang, W-W., Ma, P., Ma, Z-X., Hao, M., Adelusi, T. I. (2017) Swimming training alleviated insulin resistance through Wnt3a/β-catenin signaling in type 2 diabetic rats. Iranian J. Basic Med. Sci. 20, 1220.

    • Search Google Scholar
    • Export Citation
  • Yi, X., Cao, S., Chang, B., Zhao, D., Gao, H., Wan, Y., Shi, J., Wei, W., Guan, Y. (2013) Effects of acute exercise and chronic exercise on the liver leptin-AMPK-ACC signaling pathway in rats with type 2 diabetes. J. Diabetes Res. 2013, 946432.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Zhang, F., Li, Z. L., Xu, X. M., Hu, Y., Yao, J. H., Xu, W., Jing, H. R., Wang, S., Ning, S. L., Tian, X. F. (2015) Protective effects of icariin-mediated SIRT1/FOXO3 signaling pathway on intestinal ischemia/reperfusion-induced acute lung injury. Mol. Med. Rep. 11, 269276.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Zheng, Y., Liu, T., Wang, Z., Xu, Y., Zhang, Q., Luo, D. (2018) Low molecular weight fucoidan attenuates liver injury via SIRT1/AMPK/PGC1α axis in db/db mice. Int. J. Biol. Macromol. 112, 929936.

    • Crossref
    • Search Google Scholar
    • Export Citation