Beneficial role of naringin against methotrexate-induced injury to rat testes: biochemical and ultrastructural analyses

References

• Vardi N, Parlakpinar H, Cetin A, et al. Protective effect of beta-carotene on methotrexate-induced oxidative liver damage. Toxicol Pathol. 2010;38(4):592–597.
   PubMed Web of Science ®Google Scholar
• El-Sheikh AA, Morsy MA, Hamouda AH. Protective mechanisms of thymoquinone on methotrexate-induced intestinal toxicity in rats. Pharmacogn Mag. 2016;12(Suppl 1):S76–S81.
   PubMed Web of Science ®Google Scholar
• Sener G, Eksioglu-Demiralp E, Cetiner M, et al. L-Carnitine ameliorates methotrexate-induced oxidative organ injury and inhibits leukocyte death. Cell Biol Toxicol. 2006;22:47–60.
   PubMed Web of Science ®Google Scholar
• Wang G, Peng X. A review of clinical applications and side effects of methotrexate in ophthalmology. J Ophthalmol. 2020;2020:1537689.
   PubMed Web of Science ®Google Scholar
• Armagan A, Uzar E, Uz E, et al. Caffeic acid phenethyl ester modulates methotrexate-induced oxidative stress in testes of rat. Hum Exp Toxicol. 2008;27(7):547–552.
   PubMed Web of Science ®Google Scholar
• Padmanabhan S, Tripathi DN, Vikram A, et al. Methotrexate-induced cytotoxicity and genotoxicity in germ cells of mice: intervention of folic and folinic acid. Mutat Res. 2009;673(1):43–52.
   PubMed Web of Science ®Google Scholar
• Gulgun M, Erdem O, Oztas E, et al. Proanthocyanidin prevents methotrexate-induced intestinal damage and oxidative stress. Exp Toxicol Pathol. 2010;62(2):109–115.
   PubMedGoogle Scholar
• Daggulli M, Dede O, Utangac MM, et al. Protective effects of carvacrol against methotrexate-induced testicular toxicity in rats. Int J Clin Exp Med. 2014;7(12):5511–5516.
   PubMed Web of Science ®Google Scholar
• Najafi G, Atashfaraz E, Farokhi F. Attenuation of methotrexate-induced embryotoxicity and oxidative stress by ethyl pyruvate. Int J Fertil Steril. 2016;10(2):232–238.
   PubMedGoogle Scholar
• Nouri HS, Azarmi Y, Movahedin M. Effect of growth hormone on testicular dysfunction induced by methotrexate in rats. Andrologia. 2009;41(2):105–110.
   PubMed Web of Science ®Google Scholar
• Singh K, Bhori M, Kasu YA, et al. Antioxidants as precision weapons in war against cancer chemotherapy induced toxicity – Exploring the armoury of obscurity. Saudi Pharm J. 2018;26(2):177–190.
   PubMed Web of Science ®Google Scholar
• Watjen W, Michels G, Steffan B, et al. Low concentrations of flavonoids are protective in rat H4IIE cells whereas high concentrations cause DNA damage and apoptosis. J Nutr. 2005;135(3):525–531.
   PubMed Web of Science ®Google Scholar
• Peterson JJ, Beecher GR, Bhagwat SA, et al. Flavanones in grapefruit, lemons, and limes: A compilation and review of the data from the analytical literature. J Food Composit Anal. 2006;19:S74–S80.
   Web of Science ®Google Scholar
• Wang MJ, Chao PD, Hou YC, et al. Pharmacokinetics and conjugation metabolism of naringin and naringenin in rats after single dose and multiple dose administrations. J Food Drug Anal. 2006;14:247–253.
   Web of Science ®Google Scholar
• Jung UJ, Kim HJ, Lee JS, et al. Naringin supplementation lowers plasma lipids and enhances erythrocyte antioxidant enzyme activities in hypercholesterolemic subjects. Clin Nutr (Edinburgh, Scotland). 2003;22(6):561–568.
   PubMed Web of Science ®Google Scholar
• Pari L, Amudha K. Hepatoprotective role of naringin on nickel-induced toxicity in male Wistar rats. Eur J Pharmacol. 2011;650(1):364–370.
   PubMed Web of Science ®Google Scholar
• Deenonpoe R, Prayong P, Thippamom N, et al. Anti-inflammatory effect of naringin and sericin combination on human peripheral blood mononuclear cells (hPBMCs) from patient with psoriasis. BMC Complement Altern Med. 2019;19(1):168.
   PubMedGoogle Scholar
• Elsawy H, Alzahrani AM, Alfwuaires M, et al. Nephroprotective effect of naringin in methotrexate induced renal toxicity in male rats. Biomed Pharmacother. 2021;143:112180.
   PubMed Web of Science ®Google Scholar
• Ghanbari-Movahed M, Jackson G, Farzaei MH, et al. A systematic review of the preventive and therapeutic effects of naringin against human malignancies. Front Pharmacol. 2021;12:639840.
   PubMed Web of Science ®Google Scholar
• Liu W, Zheng W, Cheng L, et al. Citrus fruits are rich in flavonoids for immunoregulation and potential targeting ACE2. Nat Prod Bioprospect. 2022;12(1):4.
   PubMed Web of Science ®Google Scholar
• Jagetia GC, Reddy TK. The grapefruit flavanone naringin protects against the radiation-induced genomic instability in the mice bone marrow: a micronucleus study. Mutat Res. 2002;519(1-2):37–48.
   PubMed Web of Science ®Google Scholar
• Jagetia GC, Venkatesha VA, Reddy TK. Naringin, a citrus flavonone, protects against radiation-induced chromosome damage in mouse bone marrow. Mutagenesis. 2003;18(4):337–343.
   PubMed Web of Science ®Google Scholar
• Butchi Akondi R, Kumar P, Annapurna A, et al. Protective effect of rutin and naringin on sperm quality in streptozotocin (STZ) induced type 1 diabetic rats. Iran J Pharm Res. 2011;10(3):585–596.
   PubMed Web of Science ®Google Scholar
• Alboghobeish S, Mahdavinia M, Zeidooni L, et al. Efficiency of naringin against reproductive toxicity and testicular damages induced by bisphenol A in rats. Iran J Basic Med Sci. 2019;22(3):315–523.
   PubMed Web of Science ®Google Scholar
• Sherif IO, Al-Mutabagani LA, Sarhan OM. Ginkgo biloba extract attenuates methotrexate-induced testicular injury in rats: cross-talk between oxidative stress, inflammation, apoptosis, and miRNA-29a expression. Integr Cancer Ther. 2020;19:1534735420969814.
   Web of Science ®Google Scholar
• Golechha M, Sarangal V, Bhatia J, et al. Naringin ameliorates pentylenetetrazol-induced seizures and associated oxidative stress, inflammation, and cognitive impairment in rats: possible mechanisms of neuroprotection. Epilepsy Behav. 2014;41:98–102.
   PubMed Web of Science ®Google Scholar
• Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–126.
   PubMed Web of Science ®Google Scholar
• Nishikimi M, Appaji N, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun. 1972;46(2):849–854.
   PubMed Web of Science ®Google Scholar
• Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70(1):158–169.
   PubMed Web of Science ®Google Scholar
• Goldberg DM, Spooner JR. In: HU Bergmeyer, editor. Methods of enzymatic analysis. Weinheim: Verlag Chemie; 1987. p. 258.
   Google Scholar
• Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963;61:882–888.
   PubMed Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.
   PubMed Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–358.
   PubMed Web of Science ®Google Scholar
• Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963;17(1):208–212.
   PubMed Web of Science ®Google Scholar
• Tracey WR, Linden J, Peach MJ, et al. Comparison of spectrophotometric and biological assays for nitric oxide (NO) and endothelium-derived relaxing factor (EDRF): nonspecificity of the diazotization reaction for NO and failure to detect EDRF. J Pharmacol Exp Ther. 1990;252(3):922–928.
   PubMed Web of Science ®Google Scholar
• Owumi SE, Ochaoga SE, Odunola OA, et al. Protocatechuic acid inhibits testicular and epididymal toxicity associated with methotrexate in rats. Andrologia. 2019;51(9):e13350.
   PubMed Web of Science ®Google Scholar
• Kavram Sarihan K, Yilmaz M Y, Eraldemir FC, et al. Protective effects of apocynin on damaged testes of rats exposed to methotrexate. Turk J Med Sci. 2020;50(5):1409–1420.
   PubMed Web of Science ®Google Scholar
• Allen JA, Shankara T, Janus P, et al. Energized, polarized, and actively respiring mitochondria are required for acute Leydig cell steroidogenesis. Endocrinology. 2006;147(8):3924–3935.
   PubMed Web of Science ®Google Scholar
• Heidari R, Ahmadi A, Mohammadi H, et al. Mitochondrial dysfunction and oxidative stress are involved in the mechanism of methotrexate-induced renal injury and electrolytes imbalance. Biomed Pharmacother. 2018;107:834–840.
   PubMed Web of Science ®Google Scholar
• Morsy MA, Abdel-Aziz AM, Abdel-Hafez SMN, et al. The possible contribution of P-glycoprotein in the protective effect of paeonol against methotrexate-induced testicular injury in rats. Pharmaceuticals (Basel). 2020;13(9):223.
   PubMedGoogle Scholar
• Kostic TS, Andric SA, Maric D, et al. Inhibitory effects of stress-activated nitric oxide on antioxidant enzymes and testicular steroidogenesis. J Steroid Biochem Mol Biol. 2000;75(4-5):299–306.
   PubMed Web of Science ®Google Scholar
• Asadi N, Bahmani M, Kheradmand A, et al. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: A review. J Clin Diagn Res. 2017;11(5):IE01–IIE5.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Prabakaran SA, Said TM. Prevention of oxidative stress injury to sperm. J Androl. 2005;26(6):654–660.
   PubMedGoogle Scholar
• Sikka SC. Oxidative stress and role of antioxidants in normal and abnormal sperm function. Front Biosci. 1996;1:e78–e86.
   PubMedGoogle Scholar
• Hadwan MH, Almashhedy LA, Alsalman ARS. Study of the effects of oral zinc supplementation on peroxynitrite levels, arginase activity and NO synthase activity in seminal plasma of Iraqi asthenospermic patients. Reprod Biol Endocrinol. 2014;12(1).
   PubMedGoogle Scholar
• Kutlubay R, Oguz EO, Can B, et al. Vitamin E protection from testicular damage caused by intraperitoneal aluminium. Int J Toxicol. 2007;26(4):297–306.
   PubMed Web of Science ®Google Scholar
• Kono Y, Fridovich I. Superoxide radical inhibits catalase. J Biol Chem. 1982;257(10):5751–5754.
   PubMed Web of Science ®Google Scholar
• Aitken RJ, Baker MA. Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol. 2006;250(1-2):66–69.
   PubMed Web of Science ®Google Scholar
• Peltola V, Huhtaniemi I, Ahotupa M. Antioxidant enzyme activity in the maturing rat testis. J Androl. 1992;13(5):450–455.
   PubMedGoogle Scholar
• Belhan S, Comakli S, Kucukler S, et al. Effect of chrysin on methotrexate-induced testicular damage in rats. Andrologia. 2019;51(1):e13145.
   PubMed Web of Science ®Google Scholar
• Maher P. The effects of stress and aging on glutathione metabolism. Ageing Res Rev. 2005;4(2):288–314.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhao TT, Zhao HY, et al. Melatonin protects methotrexate-induced testicular injury in rats. Eur Rev Med Pharmacol Sci. 2018;22(21):7517–7525.
   PubMed Web of Science ®Google Scholar
• Aldhahrani A, Soliman MM, Althobaiti F, et al. The modulatory impacts of glycyrrhiza glabra extract against methotrexate-induced testicular dysfunction and oxidative stress. Toxicol Res (Camb). 2021;10(4):677–686.
   PubMed Web of Science ®Google Scholar
• Chen RC, Sun GB, Wang J, et al. Naringin protects against anoxia/reoxygenation-induced apoptosis in H9c2 cells via the Nrf2 signaling pathway. Food Funct. 2015;6(4):1331–1344.
   PubMed Web of Science ®Google Scholar
• Zhang T, Liu T, Shao J, et al. Antioxidant protects blood-testis barrier against synchrotron radiation X-ray-induced disruption. Spermatogenesis. 2015;5(1):e1009313.
   PubMedGoogle Scholar
• Ye J, Luo D, Xu X, et al. Metformin improves fertility in obese males by alleviating oxidative stress-induced blood-testis barrier damage. Oxid Med Cell Longev. 2019;2019:9151067.
   PubMed Web of Science ®Google Scholar
• Dolati P, Khodabandeh Z, Zamiri MJ, et al. The effect of lead acetate and quercetin on the tight and gap junctions in the mouse testis. Biol Trace Elem Res. 2020;198(2):535–543.
   PubMed Web of Science ®Google Scholar