Ameliorative effects of melatonin on intestinal oxidative damage in streptozotocin-induced diabetic rats

Yıl 2020, Cilt: 50 Sayı: 3, 160 - 167, 30.12.2020

Zatiye Ayça Çevikelli Yakut Gizem Buse Akçay Özge Çevik Göksel Şener

Öz

investigated. Methods: Male Sprague-Dawley rats were assigned into 5 groups (10 rats in each): Control, diabetes, diabetes+insulin, diabetes+melatonin, and diabetes+insulin+melatonin groups. Streptozotocin (60 mg/kg) was administered intraperitoneally to the rats to induce diabetes. At the end of 8 weeks of treatment, after blood glucose measurement and subsequent decapitation, glutathione (GSH) and malondialdehyde (MDA) levels and caspase-3, myeloperoxidase (MPO), and superoxide dismutase (SOD) activities in the intestinal tissue were investigated. Results: In diabetic animals, elevated blood glucose levels caused oxidant damage in the intestinal tissue that was demonstrated with increased MDA levels, caspase and MPO activities, and decreased GSH levels and SOD activities. Although melatonin demonstrated more significant results than insulin, separate administration of both melatonin and insulin improved the oxidative damage parameters compared to the diabetes group. In the combined treatment group, all parameters were back to control levels statistically more significant when compared with the treatment-alone. Conclusion: Melatonin has been shown to protect intestinal tissue from diabetic oxidant damage. With insulin treatment in type I diabetes, melatonin supplements may increase the quality of life through reducing complications.

Anahtar Kelimeler

Diabetes mellitus, oxidative damage, intestine, insulin, melatonin

Kaynakça

• Alikhani, V., Keshavarzi, Z., Hadjzadeh, M. A. R., & Karimi, S. (2015). The effect of melatonin on gastric parameters following diabetes induction in male rats. Acta Endocrinologica (Buc), 11(2), 155–161. https://doi.org/10.4183/aeb.2015.155
• • Anarkooli, I. J., Sankian, M., Ahmadpour, S., Varasteh, A. R., & Haghir, H. (2008). Evaluation of Bcl-2 family gene expression and caspase-3 activity in hippocampus STZ- induced diabetic rats. Experimental Diabetes Research, 2008, 638467. https://doi. org/10.1155/2008/638467
• • Bansal, A. K., & Bilaspuri, G. S. (2011). Impact of oxidative stress and antioxidants on semen functions. Veterinary Medicine International, 2011, 686137. https://doi.org/10.4061/2011/686137
• • Beuge, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–311. https://doi.org/10.1016/ s0076-6879(78)52032-6
• • Beutler, E., Duron, O., & Kelly, B. M. (1963). Improved method for the determination of blood glutathione. Journal of Laboratory and Clinical Medicine, 61, 882–888.
• • Bhor, V. M., Raghuram, N., & Sivakami, S. (2004). Oxidative damage and altered antioxidant enzyme activities in the small intestine of streptozotocin-induced diabetic rats. The International Journal of Biochemistry & Cell Biology, 36, 89–97.
• • Bolkent, S., Bolkent, S., Yanardag, R., Mutlu, O., & Yildirim, S. (2006). Alterations in somatostatin cells and biochemical parameters following zinc supplementation in gastrointestinal tissue of streptozotocin- induced diabetic rats. Acta Histochem Cytochem, 39(1), 9–15. https://doi.org/10.1267/ahc.05054
• • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(2), 248–254. https://doi.org/10.1006/abio.1976.9999
• • Costes, S., Boss, M., Thomas, A. P., & Matveyenko, A. V. (2015). Activation of Melatonin Signaling Promotes β-Cell Survival and Function. Molecular Endocrinology, 29(5), 682–692. https://doi. org/10.1210/me.2014-1293
• • Çevik, Ö., Oba, R., Macit, Ç., Çetinel, Ş., Çilingir-Kaya, Ö.T., Şener, E., & Şener, G. (2012). Lycopene inhibits caspase-3 activity and reduces oxidativeorgan damage in a rat model of thermal injury. Burns, 38(6), 861–871. https://doi.org/10.1016/j.burns.2012.01.006
• • Djordjevic, G. M., Djuric, S. S., Djordjevic, V. B., Apostolski, S., & Zivkovic, M. (2011). The role of oxidative stress in pathogenesis of diabetic neuropathy: Erythrocyte superoxide dismutase, catalase and glutathione peroxidase level in relation to peripheral nerve conduction in diabetic neuropathy patients. Dr. Colleen Croniger (Ed.), Role of the Adipocyte in Development of Type 2 Diabetes (pp. 153-178). Rijeka, Croatia: InTech.. Retrieved from https://www.intechopen.com/ books/role-of-the-adipocyte-in-development-of-type-2-diabetes/ the-role-of-oxidative-stress-in-pathogenesis-of-diabetic-neuropathy- erythrocyte-superoxide-dismutase
• • Esposito, E., & Cuzzocrea, S. (2010). Antiinflammatory activity of melatonin in central nervous system. Current Neuropharmacology, 8(3), 228–242. https://doi.org/10.2174/157015910792246155
• • Garcia, A. G., Rodrigues, M. R., Alonso, C. G., Rodrigues-Ochoa, D. Y., & Aguilar, C. A. (2015). Myeloperoxidase is associated with insulin resistance and inflammation in overweight subjects with first-degree relatives with Type 2 diabetes mellitus. Diabetes & Metabolism Journal, 39(1), 59–65. https://doi.org/10.4093/dmj.2015.39.1.59
• • Ghosh, S., Khazaei, M., Moien-Afshari, F., Ang, L. S., Granville, D. J., Verchere, C. B. … Laher, I. (2009). Moderate exercise attenuates caspase-3 activity, oxidative stress, and inhibits progression of diabetic renal disease in db/db mice. American Journal of Physiology- Renal Physiology, 296(4), 700–708. https://doi.org/10.1152/ ajprenal.90548.2008
• • Gurel-Gokmen, B., Ipekci, H., Oktay, S., Alev, B., Ustundag, U. V., Ak, E., Tunali-Akbay, T. (2018). Melatonin improves hyperglycemia induced damages in rat brain. Diabetes Metabolism Research and Reviews, 34(8), e3060. https://doi.org/10.1002/dmrr.3060
• • Hadjzadeh, M. A. R., Alikhani, V., Hosseinian, S., Zarei, B., & Keshavarzi, Z. (2018). The effect of melatonin against gastric oxidative stress and dyslipidemia in streptozotocin-ınduced diabetic rats. Acta Endocrinologica (Buchar), 14(4), 453–458. https://doi. org/10.4183/aeb.2018.453
• • Hardin, J. A., Donegan, L., Woodman, R. C., Trevenen, C., & Gall, D. G. (2002). Mucosal inflammation in a genetic model of spontaneous type I diabetes mellitus. Canadian Journal of Physiology and Pharmacology, 80(11), 1064–1070. https://doi.org/10.1139/y02-138
• • Hillegas, L. M., Griswold, D. E., Brickson, B., & Winslow, C. A. (1990). Assessment of myeloperoxidase activity in whole rat kidney. Journal of Pharmacological Methods, 24(4), 285–295. https://doi. org/10.1016/0160-5402(90)90013-b
• • Husni, A., Anggara, F. P., Isnansetyo, A., & Nugroho, A. E. (2016). Blood glucose level and lipid profile of streptozotozin-induced diabetic rats treated with Sargassum polystum extract. International Journal of Pharmaceutical and Clinical Research, 8(5), 445– 450. https://doi.org/10.3923/jbs.2016.58.64
• • Hussain, S. A., Khadim, H. M., Khalaf, B. H., Ismail, S. H., Hussein, K. I., & Sahib, A. S. (2006). Effects of melatonin and zinc on glycemic control in Type 2 diabetic patients poorly controlled with metformin. Saudi Medical Journal, 27(10),1483–1488.
• • Ighodaro, O. M. (2018). Molecular pathways associated with oxidative stress in diabetes mellitus. Biomedicine & Pharmacotherapy, 108, 656–662.
• • Kochar, N. I., & Umathe, S. N. (2009). Beneficial effects of L-arginine against diabetes-induced oxidative stress in gastrointestinal tissues in rats. Pharmacological Reports, 61, 665–672. https://doi. org/10.1016/s1734-1140(09)70118-5
• • Kowluru, R., & Koppolu, P. (2002). Diabetes-induced activation of caspase- 3 in retina: effect of antioxidant therapy. Free Radical Research, 36(9), 993–999. https://doi.org/10.1080/ 1071576021000006572
• • Liadis, N., Murakami, K., Eweida, M., Elford, A. R., Sheu, L., Gaisano, H. Y. … Woo, M. (2005). Caspase-3-dependent β-cell apoptosis in the initiation of autoimmune diabetes Mellitus. Molecular and Cellular Biology, 25(9), 3620–3629. https://doi.org/10.1128/ MCB.25.9.3620-3629.2005
• • Loven, D. P., Scheld, H. P., Oberley, L. W., Wilson, H. D., Bruch, L., Niehaus, C. L. (1982). Superoxide dismutase activity in the intestine of the streptozotocin-diabetic rat. Endocrinology, 111(3), 737–742. https://doi.org/10.1210/endo-111-3-737
• • Mandal, M., Varghese, A., Gaviraju, V. K., Talwar, S. N., Malini, S. S. (2019). Impact of hyperglycaemia on molecular markers of oxidative stress and antioxidants in type 2 diabetes mellitus. Clinical Diabetology, 8(4), 215–222. https://doi.org/10.5603/DK.2019.0015
• • Montilla, P. L., Tunez, I. F., de Agueda, C. M., Gascon, F. L., Soria, J. V. (1998). Protective role of melatonin and retinol palmitate in oxidative stress and hyperlipidemic nephropathy induced by adriamycin in rats. Journal of Pineal Research, 25(2), 86–93. https://doi. org/10.1111/j.1600-079x.1998.tb00544.x
• • Mylroie, A. A., Collins, H., Umbles, C., Kyle, J. (1986). Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicology and Applied Pharmacology, 82(3), 512–520. https://doi.org/10.1016/0041- 008x(86)90286-3
• • Nogueira, T. C., Lellis-Santos, C., Jesus, D. S., Taneda, M., Rodrigues, S. C., Amaral, F. G. … Anhe, G. F. (2011). Absence of melatonin induces night-time hepatic insulin resistance and increased gluconeogenesis due to stimulation of nocturnal unfolded protein response. Endocrinology, 152(4), 1253–1263. https://doi. org/10.1210/en.2010-1088
• • Onk, D., Onk, O. A., Erol, H. S., Özkaraca, M., Çomaklı, S., Ayazoğlu, T. A., … Ünver, S. (2018). Effect of melatonin on antioxidant capacity, ınflammation and apoptotic cell death in lung tissue of diabetic rats. Acta Cirurgica Brasileira, 33(4), 375–385. https://doi. org/10.1590/s0102-865020180040000009
• • Owino, S., Buonfiglio, D. D. C., Tchio, C., Tosini, G. (2019). Melatonin signaling a key regulator of glucose homeostasis and energy metabolism. Frontiers in Endocrinology, 10, 488. https://doi. org/10.3389/fendo.2019.00488
• • Paskaloğlu, K., Şener, G., Ayanoğlu-Dülger, G. (2004). Melatonin treatment protects against diabetes-induced functional and biochemical changes in rat aorta and corpus cavernosum. European Journal of Pharmacology, 499(3), 345–354. https://doi. org/10.1016/j.ejphar.2004.08.002
• • Santhi, T., Shaik, J. B., Mahendran, B. (2017). Myeloperoxidase levels predicts the vascular dysfunction in patients with Type 2 Diabetes Mellitus. Journal of Dental and Medical Sciences, 16(3), 30–34.
• • Song, P., Xu, J., Song, Y., Jiang, S., Yuan, H., Zhang, X. (2015). Association of plasma myeloperoxidase level with risk of coronary artery disease in patients with Type 2 diabetes. Disease Markers, 2015, 761939. https://doi.org/10.1155/2015/761939
• • Ullah, A., Khan, A., Khan, I. (2016). Diabetes mellitus and oxidative stress––A concise review. Saudi Pharmaceutical Journal, 24, 547–553. https://doi.org/10.1016/j.jsps.2015.03.013
• • Vural, H., Sabuncu, T., Arslan, S.O., Aksoy, N. (2001). Melatonin inhibits lipid peroxidation and stimulates the antioxidant status of diabetic rats. Journal of Pineal Research, 31, 193–198. https://doi. org/10.1034/j.1600-079x.2001.310301.x
• • Wolosin, J. D., & Edelman, S. V. (2000). Diabetes and the gastrointestinal tract. Clinical Diabetes, 18(4), 148.
• • Yang, X., Zou, D., Tang, S., Fan, T., Su, H., Hu, R. … Wang, Y. (2016). Ameliorative effect of melatonin against increased intestinal permeability in diabetic rats: possible involvement of MLCK-dependent MLC phosphorylation. Molecular Cellular Biochemistry, 416(1- 2), 23–32. https://doi.org/10.1007/s11010-016-2691-4.