Abstract
Background: Mounting experimental evidence highlights the testicular and neuronal toxicity of environmental/industrial chemicals in experimental animals via the mechanism involving oxidative damage. Nigerian Bonny Light crude oil (BLCO) has been reported to exhibit reproductive and neuronal toxicity in male rats. Studies have shown that vitamin E and quercetin protect rat neuronal and testicular cells from environmental chemical-induced oxidative damage. We investigated the possible protective role of quercetin and vitamin E in BLCO induced-neuronal and testicular toxicity.
Methods: Male rats were administered BLCO at doses of 400 and 800 mg/kg body wt/day p.o. three times/week for 6 weeks. Other groups were co-administered BLCO (400 and 800 mg/kg body wt/day p.o.) with/without vitamin E (50 mg/kg body wt/day p.o.) or quercetin (10 mg/kg body wt/day p.o.) three times/week for 6 weeks, respectively.
Results: Semen quality deteriorated, testosterone and luteinizing hormone (LH) levels were significantly decreased, and follicle stimulating hormone (FSH) increased following BLCO reatment. There was a significant decline in the activities of superoxide dismutase (SOD), catalase (CAT), reduced glutathione (GSH), and glutathione-S-transferase (GST) with concomitant increased levels of lipid peroxidation and activities of xanthine oxidase (XO) in a dose-dependent manner, in testes and brain of rats. Co-administration with vitamin E or quercetin reversed BLCO-induced neuronal and testicular toxicity by preventing oxidative stress, improving sperm quality, and restoring hormonal levels relative to controls.
Conclusions: BLCO altered reproductive indices and induced neuronal toxicity via the mechanism of oxidative stress. Quercetin and vitamin E showed possible chemoprotection against the toxicity.
Acknowledgments
This work was supported by the Senate Research Grant Code No. SRG/Com/2006/34A from the University of Ibadan, Nigeria (E.O.F.) and the University of Ibadan Postgraduate School Research assistantship Scheme 2010/2011 Session.
Authors’ conflict of interest disclosure: The authors stated that there are no conflicts of interest regarding the publication of this article. Research support played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
References
1. Zedeck MS. Polycyclic aromatic hydrocarbon – a review. J Environ Pathol Toxicol 1980;16:357–67.Search in Google Scholar
2. Campbell D, Cox D, Crum J, Foster K, Christie P, Brewster D. Initial effects of the grounding of the tanker Braer on health in Shetland. Br Med J 1993;307:251–5.10.1136/bmj.307.6914.1251Search in Google Scholar
3. Orisakwe OE, Akumka DD, Afonne OJ, Gamanniel KS. Investigation into the pharmacological basis for some of the folkloric uses of bonny light crude oil in Nigeria. Ind J Pharm 2000;32:231–4.Search in Google Scholar
4. Oruambo IF, Jones AB. Alterations in the concentrations of liver mitochondrial DNA, cytoplasmic total hydrocarbon and calcium in guinea pigs after treatment with Nigerian light crude oil. Int J Environ Res Public Health 2007;4:23–7.10.3390/ijerph2007010004Search in Google Scholar
5. Orisakwe OE, Akumka DD, Njan AA, Afonne JO. Testicular toxicity of Nigerian bonny light crude oil in male albino rats. Reprod Toxicol 2004;18:439–42.10.1016/j.reprotox.2004.02.002Search in Google Scholar
6. Farombi EO, Adedara IA, Ebokaiwe AP, Teberen R, Ehwerhemuepha T. Nigerian bonny light crude oil disrupts antioxidant systems in the testes and sperm of rats. Arch Environ Contam Toxicol 2010;59:166–74.10.1007/s00244-009-9443-3Search in Google Scholar
7. Adedara IA, Teberen R, Ebokaiwe AP, Ehwerhemuepha T, Farombi EO. Induction of oxidative stress in liver and kidney of rats exposed to Nigerian Bonny Light crude oil. Environ Toxicol 2012;27:372–9.10.1002/tox.20660Search in Google Scholar
8. Ebokaiwe AP, Adedara IA, Owoeye O, Farombi EO. Neurotoxicity of Nigerian bonny light crude oil in rats. Drug Chem Toxicol 2013;39:187–95.10.3109/01480545.2012.710619Search in Google Scholar
9. Baker HW, Brindle J, Irvine DS, Aitken RJ. Protective effect of antioxidants on the impairment of sperm motility by activated polymorphonuclear leukocytes. Fertil Steril 1996;65:411–9.10.1016/S0015-0282(16)58109-6Search in Google Scholar
10. Yousef MI, Kamil KI, El-Guendi MI, El-Demerdash FM. An in vitro study on reproductive toxicity of aluminium chloride on rabbit sperm: the protective role of some antioxidants. Toxicol 2007;239:213–23.10.1016/j.tox.2007.07.011Search in Google Scholar PubMed
11. Yousef MI, Saad AA, El-Shennawy LK. Protective effect of grape seed proanthocyanidin extract against oxidative stress induced by cisplatin in rats. Food Chem Toxicol 2009;47:1176–83.10.1016/j.fct.2009.02.007Search in Google Scholar PubMed
12. Sharma DR, Wani WY, Sunkaria A, Kandimalla RJ, Verma D, Cameotra SS, et al. Quercetin protects against chronic aluminum-induced oxidative stress and ensuing biochemical, cholinergic, and neurobehavioral impairments in rats. Neurotox Res 2013;23:336–57.Search in Google Scholar
13. Akiyama M. In vivo scavenging effect of ethylcysteine on reactive oxygen species in human semen. Nippon Hinyokika Gakkai Zasshi 1999;90:421–8.Search in Google Scholar
14. Carney JM, Starke-Reed PE, Oliver CN. Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity, and loss in temporal and spatial memory by chronic administration of the spin-trapping compound N-tert-butyl-alpha-phenylnitrone. Proc Natl Acad Sci USA 1991;88:3633–6.10.1073/pnas.88.9.3633Search in Google Scholar PubMed PubMed Central
15. Yousef MI, El-Demerdash FM, Radwan FM. Sodium arsenite-induced biochemical perturbations in rats: ameliorating effect of curcumin. Food Chem Toxicol 2008;46:3506–11.10.1016/j.fct.2008.08.031Search in Google Scholar
16. Sinclair S. Male infertility: nutritional and environmental considerations. Hagerstown MD: Green Valley Health, 2000:21742.Search in Google Scholar
17. Tongoliang BU, Yuling MI, Weidong Z, Caiqiao Z. Protective effect of quercetin on cadmium-induced oxidative toxicity on germ cells in male mice. Ana Rec 2011;294:520–6.10.1002/ar.21317Search in Google Scholar
18. Inal ME, Kahraman A. The protective effect of flavonol quercetin against ultraviolet a induced oxidative stress in rats. Toxicol 2000;154:21–9.10.1016/S0300-483X(00)00268-7Search in Google Scholar
19. Liu CM, Zheng YL, Lu J, Zhang ZF, Fan SH, Wu DM, et al. Quercetin protects rat liver against lead-induced oxidative stress and apoptosis. Environ Toxicol Pharmacol 2010;29:158–66.10.1016/j.etap.2009.12.006Search in Google Scholar PubMed
20. Morales AI, Vicente-Sánchez C, Sandoval JM, Egido J, Mayoral P, Arévalo MA, et al. Protective effect of quercetin on experimental chronic cadmium nephrotoxicity in rats is based on its antioxidant properties. Food Chem Toxicol 2006;44:2092–100.10.1016/j.fct.2006.07.012Search in Google Scholar PubMed
21. Renugadevi J, Prabu SM. Quercetin protects against oxidative stress-related renal dysfunction by cadmium in rats. Exp Toxicol Pathol 2010;62:471–81.10.1016/j.etp.2009.06.006Search in Google Scholar PubMed
22. Farombi EO, Adedara IA, Akinrinde SA, Ojo OO, Eboh AS. Protective effects of kolaviron and quercetin on cadmium-induced testicular damage and endocrine pathology in rats. Androl 2012;44:273–84.10.1111/j.1439-0272.2012.01279.xSearch in Google Scholar PubMed
23. Mi YL, Zhang CQ, Taya K. Quercetin protects spermatogonial cells from 2,4-d-induced oxidative damage in embryonic chickens. J Reprod Dev 2007;53:749–54.10.1262/jrd.19001Search in Google Scholar PubMed
24. Abarikwu SO, Pant AB, Farombi EO. Quercetin decreases steroidogenic enzyme activity, NF-κB expression, and oxidative stress in cultured Leydig cells exposed to atrazine. Mol Cell Biochem 2013;373:19–28.10.1007/s11010-012-1471-zSearch in Google Scholar PubMed
25. Ahmad AK, Hoda M, Raza S, Khan M, Javed H, Ishrat TA, et al. Quercetin protects against oxidative stress associated damages in a rat model of transient focal cerebral ischemia and reperfusion. Neurochem Res 2011;36:1360–71.10.1007/s11064-011-0458-6Search in Google Scholar PubMed
26. Surai P, Kostjuk I, Wishart G, Macpherson A, Speake B, Noble R, et al. Effect of vitamin E and selenium supplementation of cockerel diets on glutathione peroxidase activity and lipid peroxidation susceptibility in sperm, testes, and liver. Biol Trace Elem Res 1998;64:119–32.10.1007/BF02783329Search in Google Scholar
27. Brzezinska-Slebodzinska E, Slebodzinski AB, Pietras B, Wieczorek G. Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma. Biol Trace Elem Res 1995;47:69–74.10.1007/BF02790102Search in Google Scholar
28. Sahoo DK. Testicular protection from thyroid hormone mediated oxidative stress. Reprod 2013;4:4252.Search in Google Scholar
29. Michael G. Vitamin E and Alzheimer disease: the basis for additional clinical trials. Am J Clin Nutr 2000;71:630S–6S.10.1093/ajcn/71.2.630sSearch in Google Scholar
30. Clairborne A. Catalase activity. In: Greenwald AR, editor. Handbook of methods for oxygen radical research. Boca Raton, FL: CRC Press, 1995:237–42.Search in Google Scholar
31. Misra HP, Fridovich I. The role of superoxide anion in the auto-oxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 1972;247:3170–5.10.1016/S0021-9258(19)45228-9Search in Google Scholar
32. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130–9.10.1016/S0021-9258(19)42083-8Search in Google Scholar
33. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with folin phenol reagent. J Biol Chem 1951;193:265–75.10.1016/S0021-9258(19)52451-6Search in Google Scholar
34. Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR. Bromobenzene induced liver necrosis: protective role of glutathione and evidence for 3,4 bromobenzene oxide as the hepatotoxic metabolite. Pharmacol 1974;11:151–69.10.1159/000136485Search in Google Scholar
35. Prajda N, Weber G. malignant transformation-linked imbalance: decreased xanthine oxidase activity in hepatomas. FEBS Lett 1975;59:245–9.10.1016/0014-5793(75)80385-1Search in Google Scholar
36. Farombi EO, Tahnteng JG, Agboola AO, Nwankwo JO, Emerole GO. Chemoprevention of 2-acetylaminofluorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron-a garcinia kola seed extract. Food Chem Toxicol 2000;38:353–541.10.1016/S0278-6915(00)00039-9Search in Google Scholar
37. Zemjanis R. Collection and evaluation of semen. In: Diagnostic and therapeutic technique in animal reproduction, 2nd ed. Baltimore, MD: William and Wilkins, 1970:139–53.Search in Google Scholar
38. Pant N, Srivastava SP. Testicular and spermatotoxic effects of quinalphos in rats. J Appl Toxicol 2003;23:271–4.10.1002/jat.919Search in Google Scholar PubMed
39. Wells ME, Awa OA. New technique for assessing acrosomal characteristics of spermatozoa. J Dairy Sci 1970;53: 227.10.3168/jds.S0022-0302(70)86184-7Search in Google Scholar
40. Kandaswamy S, Senthamilselvan B, Gunasekaran K, Prabhu V, Jagadeesan A. Polychlorinated biphenyls-induced oxidative stress on rat hippocampus: a neuroprotective role of quercetin. ScientificWorldJ 2012, ID 980314.10.1100/2012/980314Search in Google Scholar
41. Hadley ME. Endocrinology, 2nd ed. Englewoods Cliff, NJ: Prentice Hall, 1988.Search in Google Scholar
42. Kordon C, Drouva SV, Martinez de la Escalera G, Weine RI. Role of classic and peptide neuromediators in the neuroendocrine regulation of luteinizing hormone and prolactin. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York: Raven Press, 1994:621–1681.Search in Google Scholar
43. Romão PR, Tovar J, Fonseca SG, Morales RH, Cruz AK, Hothersall JS, et al. Glutathione and the redox control system trypanothione/trypanothione reductase are involved in the protection of Leishmania spp. against nitrosothiol-induced cytotoxicity. Braz J Med Biol Res 2006;39:355–63.10.1590/S0100-879X2006000300006Search in Google Scholar
44. Rashidi MR, Nazemiyeh H. Inhibitory effects of flavonoids on molybdenum hydroxylases activity. Exp Opin Drug Metab Toxicol 2010;6:133–52.10.1517/17425250903426164Search in Google Scholar
45. Pritsos CA. Cellular distribution, metabolism and regulation of the xanthine oxidoreductase enzyme system. Chem Biol Int 2000;129:195–208.10.1016/S0009-2797(00)00203-9Search in Google Scholar
46. Akintonwa A, Ebere AG. Toxicity of Nigerian crude oil and chemical dispersants to Barbus Sp. and Clarias Sp. Bull Environ Contam Toxicol 1990;45:729–33.10.1007/BF01700993Search in Google Scholar
47. Johnson MK, Loo G. Effects of epigallocatechin gallate and quercetin on oxidative damage to cellular DNA. Mut Res 2000;459:211–8.10.1016/S0921-8777(99)00074-9Search in Google Scholar
48. Kawada N, Seki S, Inoue M, Kuroki T. Effect of antioxidants, resveratrol, quercetin, and N-acetylcysteine, on the functions of cultured rat hepatic stellate cells and kupffer cells. Hepatol 1998;27:1265–74.10.1002/hep.510270512Search in Google Scholar PubMed
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