Skip to main content
Log in

The effect of swimming training on oxidative stress, SIRT1 gene expression, and histopathology of hepatic tissue in type 2 diabetic rats

  • Original Article
  • Published:
Biologia Futura Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aebi, H. (1984) Catalase in vitro. Methods Enzymol. 105, 121–126.

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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, 2679–2687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blander, G., Guarente, L. (2004) The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73, 417–435.

    Article  CAS  PubMed  Google Scholar 

  • 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, 576–584.

    CAS  PubMed  Google Scholar 

  • 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, 49–64.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 436–443.

    Article  CAS  PubMed  Google Scholar 

  • 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, 70–81.

    Article  CAS  PubMed  Google Scholar 

  • 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, 101–107.

    Article  CAS  PubMed  Google Scholar 

  • 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, 1447–1463.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 177–185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 500–508.

    Article  CAS  PubMed  Google Scholar 

  • 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, 203–208.

    Article  Google Scholar 

  • 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, 622–636.

    Article  CAS  PubMed  Google Scholar 

  • 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, 371–378.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 633–639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 305–312.

    Article  CAS  PubMed  Google Scholar 

  • 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.

  • 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, 380–390.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nassir, F., Ibdah, J. A. (2016) Sirtuins and nonalcoholic fatty liver disease. World J. Gastroenterol. 22, 10084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 334–344.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Paglia, D. E., Valentine, W. N. (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70, 158–169.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szkudelski, T., Szkudelska, K. (2015) Resveratrol and diabetes: from animal to human studies. Biochim. Biophys. Acta 1852, 1145–1154.

    Article  CAS  PubMed  Google Scholar 

  • 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, 309–319.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, D., Johnson, P. (2000) Exercise modulates antioxidant enzyme gene expression in rat myocardium and liver. J. Appl. Physiol. 88, 1791–1796.

    Article  CAS  PubMed  Google Scholar 

  • 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, 862–868.

    Article  CAS  PubMed  Google Scholar 

  • 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, 726–729.

    CAS  Google Scholar 

  • 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, 882–887.

    CAS  PubMed  Google Scholar 

  • 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, E1179–E1186.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 269–276.

    Article  CAS  PubMed  Google Scholar 

  • 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, 929–936.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roya Naderi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghiasi, R., Naderi, R., Mozaffar, A. et al. The effect of swimming training on oxidative stress, SIRT1 gene expression, and histopathology of hepatic tissue in type 2 diabetic rats. BIOLOGIA FUTURA 70, 167–174 (2019). https://doi.org/10.1556/019.70.2019.21

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1556/019.70.2019.21

Keywords

Navigation