Protective Role of Naringenin on Oxidative Stress Caused by Fenamiphos in Rat Blood and Spleen Tissue

Year 2024, Volume: 14 Issue: 2, 625 - 635, 01.06.2024

Hatice Karaboduk , Çağlar Adıgüzel , Fatma Gökçe Apaydın , Suna Kalender , Meltem Uzunhisarcikli , Yusuf Kalender

https://doi.org/10.21597/jist.1381156

Abstract

Fenamiphos, an organophosphate insecticide, is frequently used in agricultural areas and causes various problems in terms of environment and public health. Naringenin is a flavonone with anticancer, anti-inflammatory, antioxidant and antiproliferative activities. The aim of this study is to investigate the protective role of naringenin on fenamiphos-induced oxidative stress in the blood and spleen tissue of rats. In this study, rats were divided into 4 groups, with 6 in each group. 1st group: control group, 2nd group: fenamifos (0.76 mg/kg b.w.) treated group, 3rd group: naringenin (50 mg/kg b.w.) treated group 4th group: fenamifos (0.76 mg/kg b.w.) v.a.) plus naringenin (50 mg/kg b.a.) treated group. The substances were given to experimental animals via gavage for 28 days. When the fenamiphos treated group was compared with the control group, a statistically significant increase was observed in MDA, IL-17 and 8-OHdG levels compared to the control group (p <0.05), while a statistically significant decrease was observed in SOD, CAT, GPx and GST enzyme activities (p<0.05). When the naringenin-treated group was compared with the fenamiphos-treated group, a significant improvement in the parameters was observed. In this study, it was observed that the administration of naringenin, which has strong antioxidant properties, significantly reduced oxidative damage against the toxicity caused by fenamiphos in the blood and spleen tissue of rats.

Keywords

Blood, Spleen, Fenamiphos, Naringenin, Oxidative stress

Ethical Statement

Bu çalışma için Gazi Üniversitesi Hayvan Deneyleri Yerel Etik Kurulundan (Protokol no: G.Ü.ET-22.011 ) onay alınmıştır.

Fenamifos’un Sıçan Kan ve Dalak Dokusunda Sebep Olduğu Oksidatif Stres Üzerine Naringenin’in Koruyucu Rolü

Abstract

Organofosfatlı bir insektisit olan fenamifos, tarım alanlarında sıklıkla kullanılmakta, çevre ve halk sağlığı açısından çeşitli sorunlar meydana getirmektedir. Naringenin, antikanser, antiinflamatuvar, antioksidan ve antiproliferatif aktivitelere sahip bir flavonondur. Bu çalışmanın amacı sıçanların kan ve dalak dokusunda fenamifos kaynaklı oksidatif stres üzerine naringeninin koruyucu rolünü araştırmaktır. Bu çalışmada sıçanlar her grupta 6 adet olacak şekilde 4 gruba ayrılmıştır. 1. grup: kontrol grubu, 2. grup: fenamifos (0.76 mg/kg v.a.) muameleli grup, 3. grup: naringenin (50 mg/kg v.a.) muameleli grup 4. grup: fenamifos (0.76 mg/kg v.a.) ve naringenin (50 mg/kg v.a.) muameleli grup. Maddeler deney hayvanlarına 28 gün boyunca gavaj yolu ile verilmiştir. Fenamifos muameleli grup, kontrol grubu ile karşılaştırıldığında MDA, IL-17 ve 8-OHdG düzeylerinde kontrol grubuna göre istatistiksel olarak anlamlı bir artış gözlenirken (p<0.05), SOD, CAT, GPx ve GST enzim aktivitelerinde ise istatiksel olarak anlamlı bir azalma gözlenmiştir (p<0.05). Naringenin muameleli grup, fenamifos muameleli grup ile karşılaştırıldığında, parametrelerde anlamlı bir iyileşme gözlenmiştir. Bu çalışmada fenamifosun sıçanların kan ve dalak dokusunda oluşturduğu toksisiteye karşı, antioksidan özellikleri güçlü naringenin uygulamasının oksidatif hasarı önemli ölçüde azalttığı gözlenmiştir.

Keywords

Kan, Dalak, Fenamifos, Naringenin, Oksidatif stres

References

• Adiguzel, C. & Kalender, Y. (2020). Bendiocarb-induced nephrotoxicity in rats and the protective role of vitamins C and E. Environmental Science and Pollution Research, 27, 6449-6458. https://doi.org/10.1007/s11356-019-07260-x
• Adiguzel, C., Karaboduk, H., Apaydin, F. G., Kalender, S. & Kalender, Y. (2023). Comparison of nickel oxide nano and microparticles toxicity in rat liver: molecular, biochemical, and histopathological study. Toxicology Research, tfad062. https://doi.org/10.1093/toxres/tfad062
• Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3
• Altamura, M., Caradonna, L., Amati, L., Pellegrino, N. M., Urgesi, G. & Miniello S. (2001). Splenectomy and sepsis: the role of the spleen in the immunemediated bacterial clearance. Immunopharmacology and Immunotoxicology, 23, 153-161. https://doi.org/10.1081/IPH-100103856
• Ameer, B., Weintraub, R. A., Johnson, J. V., Yost, R. A. & Rouseff, R. L. (1996). Flavanone absorption after naringin, hesperidin, and citrus administration. Clinical Pharmacology & Therapeutics, 60(1), 34-40. https://doi.org/10.1016/S0009-9236(96)90164-2
• Apaydın, F., Uzunhisarcıklı, M., Aslantürk, A. & Kalender, S. (2018). Bisphenol a-induced histopathological alterations on small intestine tissues of rats: The protective role of taurine and curcumin. Iğdır University Journal of the Institute of Science and Technology, 8(2), 43-47. https://doi.org/10.21597/jist.427870
• Banerjee, B. D., Seth, V. & Ahmed, R. S. (2001). Pesticide-induced oxidative stress: perspective and trends. Reviews on environmental health, 16(1), 1-40. https://doi.org/10.1515/REVEH.2001.16.1.1
• Baş, H. & Kalender, Y. (2011). Chlorpyrifos induced cardiotoxicity in rats and the protective role of quercetin and catechin. Gazi University Journal of Science, 24(3), 387-395.
• Baş, H., Kalender, Y., Pandir, D. & Kalender, S. (2015). Effects of lead nitrate and sodium selenite on DNA damage and oxidative stress in diabetic and non-diabetic rat erythrocytes and leucocytes. Environmental Toxicology and Pharmacology, 39(3), 1019-1026. https://doi.org/10.1016/j.etap.2015.03.012
• Baş, H. & Kalender, Y. (2016). Nephrotoxic effects of lead nitrate exposure in diabetic and nondiabetic rats: Involvement of oxidative stress and the protective role of sodium selenite. Environmental Toxicology, 31(10), 1229-1240. https://doi.org/10.1002/tox.22130
• Baş, H., Apaydın, F. G., Kalender, S., Aydoğdu, G., Adıgüzel, Ç., Taştan, H. & Kalender, Y. (2022). Dimethoate-induced oxidative stress and DNA damage in rat blood cells: preventive effects of ferulic acid. Turkish Bulletin of Hygiene and Experimental Biology, 79(2), 243-254. https://doi.org/10.5505/TurkHijyen.2022.09734
• Bojarski, B. & Witeska, M. (2020). Blood biomarkers of herbicide, insecticide, and fungicide toxicity to fish-a review. Environmental Science and Pollution Research, 27, 19236-19250. https://doi.org/10.1007/s11356-020-08248-8
• Caceres, T., Megharaj, M., Venkateswarlu, K., Sethunathan, N. & Naidu, R. (2010). Fenamiphos and related organophosphorus pesticides: environmental fate and toxicology (pp. 117-162). Springer New York. https://doi.org/10.1007/978-1-4419-5623-1_3
• Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193(1), 265-75. https://doi.org/10.1016/S0021-9258(19)52451-6
• Demir, F., Uzun, F. G., Durak, D. & Kalender, Y. (2011). Subacute chlorpyrifos-induced oxidative stress in rat erythrocytes and the protective effects of catechin and quercetin. Pesticide Biochemistry and Physiology, 99(1), 77-81. https://doi.org/10.1016/j.pestbp.2010.11.002
• Durak, D., Kalender, S., Uzun, F. G. & Kalender, Y. (2010). Mercury chloride-induced oxidative stress in human erythrocytes and the effect of vitamins C and E in vitro. African Journal of Biotechnology, 9(4), 488-495.
• Djuric, A., Begic, A., Gobeljic, B., Stanojevic, I., Ninkovic, M., Vojvodic, D., Pantelic, A., Zebic, G., Prokic, V., Dejanovic, B., Stojanovic, I., Pavlica, M., Djukic, D., Saso, L., Djurdjevic, D., Pavlovii, M., Topic, A., Vujanovic, D., Stevnovic, I. & Djukic, M. (2015). Oxidative stress, bioelements and androgen status in testes of rats subacutely exposed to cadmium. Food Chemical Toxicology, 86, 25-33. https://doi.org/10.1016/j.fct.2015.09.004
• Dosumu, O. A., Rotimi, S. O., Adeleye, O. O., Akamo, A. J., Osinuga, K. T., Taiwo, O. A., Omotosho, O.O. & Sani, L. O. (2021). Vitamin K protects against 7, 12‐dimethylbenz (A) anthracene induced hepatotoxicity in Wistar rats. Environmental Toxicology, 36(3), 362-373. https://doi.org/10.1002/tox.23042
• Eraslan, G., Saygi, S., Essiz, D., Aksoy, A., Gul, H. & Macit, E. (2007). Evaluation of aspect of some oxidative stress parameters using vitamin E, proanthocyanidin and nacetylcysteine against exposure to cyfluthrin in mice. Pesticide Biochemistry and Physiology, 88, 43-49. https://doi.org/10.1016/j.pestbp.2006.08.010
• Habig, W. H., Pabst, M. J. & Jakoby, W. B. (1974). Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8
• Geyik, S., Altunısık, E., Neyal, A.M. &Taysi, S. (2016). Oxidative stress and DNA damage in patients with migraine. The Journal Headache and Pain, 17(10), 1-6. https://doi.org/10.1186/s10194-016-0606-0
• Kalender, S., Apaydin, F. G., Baş, H. & Kalender, Y. (2015). Protective effects of sodium selenite on lead nitrate‐induced hepatotoxicity in diabetic and non‐diabetic rats. Environmental Toxicology and Pharmacology, 40. 568-574. https://doi.org/10.1016/j.etap.2015.08.011
• Karaboduk, H. & Kalender, Y. (2021). The effects of lead nitrate and mercury chloride on rat liver tissue. Fresenius Environmental Bulletin, 30(3), 2368-2379.
• Kiran, S. D. V. S., Rohini, P. & Bhagyasree, P. (2017). Flavonoid: A review on Naringenin. Journal of Pharmacognosy and Phytochemistry, 6(5), 2778-2783.
• Kucukler, S., Darendelioğlu, E., Caglayan, C., Ayna, A., Yıldırım, S. & Kandemir, F.M. (2020). Zingerone attenuates vancomycin-induced hepatotoxicity in rats through regulation of oxidative stress, inflammation and apoptosis. Life Sciences, 259, 118382. https://doi.org/10.1016/j.lfs.2020.118382
• Marklund, S. & Marklund, G. (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry, 47(3), 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
• Miljkovic, D., Cvetkovic, I., Momcilovic, M., Maksimovic-Ivanic, D., Stosic-Grujicic, S. & Trajkovic, V. (2005). Interleukin-17 stimulates inducible nitric oxide synthase-dependent toxicity in mouse beta cells. Cellular and Molecular Life Sciences, 62, 2658-2668. https://doi.org/10.1007/s00018-005-5259-0
• Ohkawa, H., Ohishi, N. & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95(2), 351-358. https://doi.org/10.1016/0003-2697(79)90738-3
• Ojha, A., Yaduvanshi, S. K. & Srivastava, N. (2011). Effect of combined exposure of commonly used organophosphate pesticides on lipid peroxidation and antioxidant enzymes in rat tissues. Pesticide Biochemistry and Physiology, 99(2), 148-156. https://doi.org/10.1016/j.pestbp.2010.11.011
• Paglia, D.E. & Valentine, W.N. (1987). Studies on the quantative and qualitative characterization of glutathione peroxidase. Journal of Laboratory and Clinical Medicine, 70. 158-165.
• Rai, R., Jat, D. & Mishra, S. K. (2023). Naringenin ameliorates aluminum toxicity-induced testicular dysfunctions in mice by suppressing oxidative stress and histopathological alterations. Systems Biology in Reproductive Medicine, 1-7. https://doi.org/10.1080/19396368.2023.2203794
• Rashmi, R., Magesh, S. B., Ramkumar, K. M., Suryanarayanan, S. & SubbaRao, M. V. (2018). Antioxidant potential of naringenin helps to protect liver tissue from streptozotocin-induced damage. Reports of Biochemistry & Molecular Biology, 7(1), 76.
• Romeh, A. A. & Hendawi, M. Y. (2017). Biochemical interactions between Glycine max L. silicon dioxide (SiO2) and plant growth-promoting bacteria (PGPR) for improving phytoremediation of soil contaminated with fenamiphos and its degradation products. Pesticide Biochemistry and Physiology, 142, 32-43. https://doi.org/10.1016/j.pestbp.2017.01.001
• Qader, B., Baron, M. G., Hussain, I., Johnson, R. P. & Gonzalez-Rodriguez, J. (2019). Electrochemical determination of the organophosphate compound Fenamiphos and its main metabolite, Fenamiphos sulfoxide. Monatshefte Für Chemie-Chemical Monthly,150. 411-417. https://doi.org/10.1007/s00706-018-2334-4
• Quintana, M. M., Osimani, V. R., Magnarelli, G., Rovedatti, M. G. & Guiñazú, N. (2018). The insecticides chlorpyrifos and acetamiprid induce redox imbalance in umbilical cord blood erythrocytes in vitro. Pesticide Biochemistry and Physiology, 148, 87-92. https://doi.org/10.1016/j.pestbp.2018.04.001
• Singh, B. K., Walker, A. & Wright, D. J. (2006). Bioremedial potential of fenamiphos and chlorpyrifos degrading isolates: influence of different environmental conditions. Soil Biology and Biochemistry, 38(9), 2682-2693. https://doi.org/10.1016/j.soilbio.2006.04.019
• Thiermann, H., Mast, U., Klimmek, R., Eyer, P., Hibler, A., Pfab, R., Felgenhauer, N. & Zilker, T. (1997). Cholinesterase status, pharmacokinetics and laboratory findings during obidoxime therapy in organophosphate poisoned patients. Human & Experimental Toxicology, 16(8), 473-480. https://doi.org/10.1177/096032719701600809
• Wang, J., Yang, Z., Lin, L., Zhao, Z., Liu, Z. & Liu, X. (2012). Protective effect of naringenin against lead-induced oxidative stress in rats. Biological Trace Element Research, 146, 354-359. https://doi.org/10.1007/s12011-011-9268-6
• Wang, Y. S., Tai, K. T. & Yen, J. H. (2004). Separation, bioactivity, and dissipation of enantiomers of the organophosphorus insecticide fenamiphos. Ecotoxicology and Environmental Safety, 57(3), 346-353. https://doi.org/10.1016/j.ecoenv.2003.08.012
• Wang., J., Zhu, H., Lin, S., Wang, K., Wang, H. & Liu, Z. (2021). Protective effect of naringenin against cadmium-induced testicular toxicity in male SD rats. Journal of Inorganic Biochemistry. 214, 111310. https://doi.org/10.1016/j.jinorgbio.2020.111310
• Wilcox, L. J., Borradaile, N. M. & Huff, M. W. (1999). Antiatherogenic properties of naringenin, a citrus flavonoid. Cardiovascular Drug Reviews, 17(2), 160-178. https://doi.org/10.1111/j.1527-3466.1999.tb00011.x
• Yıldız, M.O., Çelik, H., Caglayan, C., Genç, A., Doğan, T. & Satıcı, E. (2022). Neuroprotective effects of carvacrol against cadmium-induced neurotoxicity in rats: role of oxidative stress, inflammation and apoptosis. Metabolic Brain Disease, 37, 1259-1269. https://doi.org/10.1007/s11011-022-00945-2
• Zaidun, N. H., Thent, Z. C. & Abd Latiff, A. (2018). Combating oxidative stress disorders with citrus flavonoid: Naringenin. Life Sciences, 208, 111-122. https://doi.org/10.1016/j.lfs.2018.07.017