Interaperitoneal Administration of Αlpha-Tocopherol Loaded Nanoparticles Improves Ischemia-Reperfusion Injury in Rat Ovaries Torsion and Detorsion Model

Houman Azizizadeh, Alireza Najafpour

Abstract

Objective: To investigate effects of intraperitoneally administration of α-tocopherol loaded nanoparticles (TNP) on ischemia-reperfusion injury in ovaries.

Methods: Thirty-five healthy female Wistar rats ~250g were randomized into seven experimental groups (n = 5): Group SHAM: The rats underwent only laparotomy. Group Ischemia: A 3- hour ischemia only. Group I/R: A 3-hour ischemia and a 3-hour reperfusion. Group I/T: A 3-hour ischemia only and 100 mg/kg intraperitoneal administration (IP) of α-tocopherol 2.5 hours after induction of ischemia. Group I/R/T: A 3-hour ischemia, a 3-hour reperfusion and 100 mg/kg IP of α-tocopherol 2.5 hours after induction of ischemia. Group I/TNP: A 3-hour ischemia only and 1 mg/kg IP of TNP 2.5 hours after induction of ischemia. Group I/R/TNP: A 3-hour ischemia, a 3-hour reperfusion and 1 mg/kg IP of TNP 2.5 hours after induction of ischemia.

Results: Animals treated with αTNP showed significantly ameliorated development of ischemia and reperfusion tissue injury compared to those of other groups (p=0.001). The significant higher values of SOD, tGSH, GPO, GSHRd and GST were observed in I/R/NC animals compared to those of other groups (p=0.001). Damage indicators (NOS, MDA, MPO and DNA damage level) were significantly lower in I/R/NC animal compared to those of other groups (p=0.001). Conclusion: Intraperitoneal administration of TNP could be helpful in minimizing ischemia-reperfusion injury in ovarian tissue exposed to ischemia.

Keywords

Ischemia-reperfusion; α-tocopherol nanoparticles; Intraperitoneal; Ovary

Full Text:

PDF XML HTML FIGS

References

Oelsner G, Shashar D. Adnexal torsion. Clin Obstet Gynecol. 2006;49(3):459-63.

Geimanaite L, Trainavicius K. Ovarian torsion in children: management and outcomes. J Pediatr Surg. 2013;48(9):1946-53.

Celik A, Ergün O, Aldemir H, Ozcan C, Ozok G, Erdener A, et al. Long-term results of conservative management of adnexal torsion in children. J Pediatr Surg. 2005;40(4):704-8.

Carden DL, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J Pathol. 2000;190(3):255-66.

Zimmerman BJ, Granger DN. Reperfusion injury. Surg Clin North Am. 1992;72(1):65-83.

Nakagiri A, Sunamoto M, Takeuchi K, Murakami M. Evidence for the involvement of NADPH oxidase in ischemia/reperfusion-induced gastric damage via angiotensin II. J Physiol Pharmacol 2010;61(2):171-9.

Javanmardi S, Khordadmehr M. Benidipine reduces ischemia/reperfusion injury following testicular torsion/detorsion in rats. Iranian Journal of Veterinary Surgery. 2017;12(2):21-30.

Ingec M, Isaoglu U, Yilmaz M, Calik M, Polat B, Alp HH, et al. Prevention of ischemia-reperfusion injury in rat ovarian tissue with the on-off method. J Physiol Pharmacol. 2011;62(5):575-82.

Filho DW, Torres MA, Bordin AL, Crezcynski-Pasa TB, Boveris A. Spermatic cord torsion, reactive oxygen and nitrogen species and ischemia- reperfusion injury. Mol Aspects Med. 2004;25(1-2):199-210.

Girotti AW. Lipid hydroperoxide generation, turnover, and effector action in biological systems. J Lipid Res. 1998;39(8):1529-42.

Huang HY, Helzlsouer KJ, Appel LJ. The effects of vitamin C and vitamin E on oxidative DNA damage: results from a randomized controlled trial. Cancer Epidemiol Biomarkers Prev. 2000;9(7):647-52.

Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA.1993;90(17):7915-22.

Oral A, Odabasoglu F, Halici Z, Keles ON, Unal B, Coskun AK, et al. Protective effects of montelukast on ischemia-reperfusion injury in rat ovaries subjected to torsion and detorsion: biochemical and histopathologic evaluation. Fertil Steril. 2011;95(4):1360-6.

Mogilner JG, Lurie M, CoranAG, Nativ O, Shiloni E, Sukhotnik I. Effect of diclofenac on germ cell apoptosis following testicular ischemia-reperfusion injury in a rat. Pediatr Surg Int. 2006;22(1):99-105.

Halici Z, Karaca M, Keles ON, Borekci B, Odabasoglu F, Suleyman H, et al. Protective effects of amlodipine on ischemiareperfusion injury of rat ovary: biochemical and histopathologic evaluation. Fertil Steril. 2008;90(6):2408-15.

Anderson AM, Mitchell MS, Mohan RS. Isolation of curcumin from turmeric. Journal of chemical education. 2000;77(3):359.

Bramley PM, Elmadfa I, Kafatos A, Kelly FJ, Manios Y, Roxborough HE, et al. Vitamin E. J Sci Food Agric. 2000;80(7):913-38.

Farias MC, Moura ML, Andrade L, Leão MHMR. Encapsulation of the alpha-tocopherol in a glassy food model matrix. Materials Research. 2007;10(1):57-62.

Hategekimana J, Masamba KG, Ma J, Zhong F. Encapsulation of vitamin E: effect of physicochemical properties of wall material on retention and stability. Carbohydr Polym. 2015;124:172-179.

Trombino S, Cassano R, Muzzalupo R, Pingitore A, Cione E, Picci N. Stearyl ferulate-based solid lipid nanoparticles for the encapsulation and stabilization of β-carotene and α-tocopherol. Colloids Surf B Biointerfaces. 2009;72(2):181-7.

Duclairoir C, Orecchioni AM, Depraetere P, Nakache E. Alpha-tocopherol encapsulation and in vitro release from wheat gliadin nanoparticles. J Microencapsul. 2002;19(1):53-60.

Quiñones JP, Gothelf KV, Kjems J, Yang C, Caballero AMH, Schmidt C, et al. Self-assembled nanoparticles of modified-chitosan conjugates for the sustained release of dl-α-tocopherol. Carbohydr Polym. 2013;92(1):856-864.

Luo Y, Zhang B, Whent M, Yu L, Wang Q. Preparation and characterization of zein/chitosan complex for encapsulation of α-tocopherol, and its in vitro controlled release study. Colloids Surf B Biointerfaces. 2011;85(2):145-52.

Cortés-Sanabria L, Paredes-Ceseña CA, Herrera-Llamas RM, Cruz-Bueno Y, Soto-Molina H, Pazarín L, et al.Comparison of cost-utility between automated peritoneal dialysis and continuous ambulatory peritoneal dialysis. Arch Med Res. 2013;44(8):655-61.

Chaudhary K, Haddadin S, Nistala R, Papageorgio C. Intraperitoneal Drug Therapy: an Advantage. Curr Clin Pharmacol. 2010;5(2):82-88.

Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16(2):109-10.

Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem. 1988;34(3):497-500.

Feelisch M, Noack EA. Correlation between nitric oxide formation during degradation of organic nitrates and activation of guanylate cyclase. Eur J Pharmacol. 1987;139(1):19-30.

Knowles RG, Merrett M, Salter M, Moncada S. Differential induction of brain, lung and liver nitric oxide synthase by endotoxin in the rat. Biochem J. 1990;270(3):833-6.

Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351-8.

Wei H, Frenkel K. In vivo formation of oxidized DNA bases in tumor promoter-treated mouse skin. Cancer Res. 1991;51(16):4443-9.

Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem. 1968;25(1):192-205.

Lawrence RA, Burk RF. Glutathione peroxidase activity in selenium-deficient rat liver. 1976. Biochem Biophys Res Commun.2012;425(3):503-9.

Carlberg I, Mannervik B. Glutathione reductase. Methods Enzymol. 1985;113:484-90.

Habig WH, Jakoby WB. Assays for differentiation of glutathione S-transferases. Methods Enzymol. 1981;77:398-405.

Celik O, Turkoz Y, Hascalik S, Hascalik M, Cigremis Y, Mizrak B, et al. The protective effect of caffeic acid phenethyl ester on ischemia-reperfusion injury in rat ovary. Eur J Obstet Gynecol Reprod Biol. 2004;117(2):183-88.

Arosio B, Gagliano N, Fusaro LM, Parmeggiani L, Tagliabue J, Galetti P, et al. Aloe-Emodin quinone pretreatment reduces acute liver injury induced by carbon tetrachloride. Pharmacol Toxicol. 2000;87(5):229-33.

Chatterjee PK, Patel NS, Kvale EO, Cuzzocrea S, Brown PA, Stewart KN, et al. Inhibition of inducible nitric oxide synthase reduces renal ischemia/reperfusion injury. Kidney Int. 2002;61(3):862-71.

Jeddi S, Zaman J, Zadeh-Vakili A, Zarkesh M, Ghasemi A. Involvement of inducible nitric oxide synthase in the loss of cardioprotection by ischemic postconditioning in hypothyroid rats. Gene. 2016;580(2):169-76

Ferdinandy P, Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol. 2003;138(4):532-43.

Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr Med Chem. 2005;12(10):1161-208.

Niki E, Yoshida Y, Saito Y, Noguchi N. Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun. 2005;338(1):668-76.

Ximenes VF, Paino IM, Faria-Oliveira OM, Fonseca LM, Brunetti IL. Indole ring oxidation by activated leukocytes prevents the production of hypochlorous acid. Braz J Med Biol Res. 2005;38(11):1575-83.

Van Antwerpen P, Boudjeltia KZ, Babar S, Legssyer I, Moreau P, Moguilevsky N, et al. Thiol-containing molecules interact with the myeloperoxidase/H2O2/chloride system to inhibit LDL oxidation. Biochem Biophys Res Commun. 2005;337(1):82-8.

Isaoglu U, Yilmaz M, Sener E, Cetin N, Altuner D, Bilen H, et al. The impaired balances of oxidant/antioxidant and COX-1/COX-2 in ovarian ischemia-reperfusion injury and prevention by nimesulide. Latin American Journal of Pharmacy. 2012;31(10):1481-8.

Meister A. Glutathione deficiency produced by inhibition of its synthesis, and its reversal; applications in research and therapy. Pharmacol Ther. 1991;51(2):155-94.

Celebi F, Akbas A, Saglam MB, Kisaoglu A, Alp HH. Effect of sertraline in indomethacin-induced gastric mucosal damage. Asian Journal of Chemistry. 2012;24(5):1966.

Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160(1):1-40.

Sharma H, Zhang X, Dwivedi C. The effect of ghee (clarified butter) on serum lipid levels and microsomal lipid peroxidation. Ayu .2010;31(2):134-40.

Polat B, Suleyman H, Alp HH. Adaptation of rat gastric tissue against indomethacin toxicity. Chem Biol Interact. 2010;186(1):82-9.

Shi HY, Li ZH, Zhang YX, Chen L, Xiang DY, Zhang YF. Two pear glutathione S-transferases genes are regulated during fruit development and involved in response to salicylic acid, auxin, and glucose signaling. PLoS One. 2014;9(2):e89926.

Mansoorali KP, Prakash T, Kotresha D, Prabhu K, Rama Rao N. Cerebroprotective effect of Eclipta alba against global model of cerebral ischemia induced oxidative stress in rats. Phytomedicine. 2012;19(12):1108-16.

Milligan JR, Aguilera JA, Nguyen TT, Ward JF, Kow YW, He B, et al. Yield of DNA strand breaks after base oxidation of plasmid DNA. Radiat Res. 1999;151(3):334-42.

Grollman AP, Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet. 1993;9(7):246-9.

Aksoy A. Ovarian ischemia–reperfusion injury: a brief review. SM J Gynecol Obstet. 2015;1(2):1008.

Srivastava G, Mehta JL. Currying the heart: curcumin and cardioprotection. Journal of cardiovascular pharmacology and therapeutics. 2009;14(1):22-7.

Uguralp S, Bay Karabulut A, Mizrak B. Effects of pentoxifylline and vitamin E on the bilateral ovary after experimental ovarian ischemia. Eur J Pediatr Surg. 2005;15(2):107-13.

Nugent D, Newton H, Gallivan L, Gosden RG. Protective effect of vitamin E on ischaemia-reperfusion injury in ovarian grafts. J Reprod Fertil. 1998;114(2):341-6.

Turner PV, Brabb T, Pekow C, Vasbinder MA. Administration of Substances to Laboratory Animals: Routes of Administration and Factors to Consider. J Am Assoc Lab Anim Sci. 2011;50(5):600-13.

Petros R A, DeSimone JM. Strategies in the design of nanoparticles for therapeutic applications. Nat Rev Drug Discov. 2010;9(8):615-27.