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ORIGINAL ARTICLE

Coenzyme Q10 and fish oil synergistically alleviate aluminum chloride-induced suppression of testicular steroidogenesis and antioxidant defense

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Pages 1319-1334 | Received 03 Apr 2015, Accepted 30 Jun 2015, Published online: 11 Aug 2015

References

  • Yokel RA, McNamara PJ. Aluminium toxicokinetics: an updated mini review. Pharmacol Toxicol 2001;88: 159–167.
  • Fernandez-Lorenzo JR, Cocho JA, Rey-Goldar ML, Couce M, Fraga JM. Aluminum contents of human milk, cow's milk, and infant formulas. J Pediatr Gastroenterol Nutr 1999;28:270–275.
  • Popinska K, Kierku´s J, Lyszkowska M, Socha J, Pietraszek E, Kmiotek W, Ksiazyk J. Aluminum contamination of parenteral nutrition additives, amino acid solutions, and lipid emulsions. Nutrition 1999;15:683–686.
  • Abbasali KM, Zhila T, Farshad N. Developmental toxicity of aluminium from high doses of AlCl3 in mice. J Appl Res 2005;5:575–579.
  • Lin JL, Yang YJ, Yang SS, Leu ML. Aluminum utensile contribute to aluminum accumulation in patients with renal disease. Am J Kidney Dis 1997;30:653–658.
  • Sharma P, Mishra K. Amelioration of fumonisin B1 hepatotoxicity in mice by depletion of T cells with anti-Thy-1.2. Reprod Toxicol 2006;21:313–321.
  • Suwalsky M, Norris B, Villena F, Cuevas F, Sotomayor P, Zatta P. Aluminum fluoride affects the structure and functions of cell membranes. Food Chem Toxicol 2004;42:925–933.
  • Domingo JL. Aluminum and other metals in Alzheimer's disease: a review of potential therapy with chelating agents. J Alzheimer's Dis 2006;10:331–341.
  • Hovatta O, Venalainen ER, Kuusimaki L, Heikkila J, Hirvi T, Reima I. Aluminum, lead and cadmium concentrations in seminal plasma and spermatozoa, and semen quality in Finnish men. Hum Reprod 1998;13:115–119.
  • Dawson EB, Evans DR, Harris WA, Powell LC. Seminal plasma trace metal levels in industrial workers. Biol Trace Elem Res 2000;74:97–105.
  • Chinoy NJ, Bhattacharya S. Effect of single dose of aluminum chloride on some reproductive organs and fertility in male mice. Indian J Environ Toxicol 1996;6:10–13.
  • Chinoy NJ, Momin R, Jhala DD. Fluoride and aluminium induced toxicity in mice epididymis and its mitigation by vitamin C. Fluoride 2005;38:115–121.
  • Chinoy NJ, Momin R, Sorathia HP, Jhala DD. Recovery from fluoride plus aluminium toxicity in vas deferens, seminal vesicle, and ventral prostate of mice by vitamin C. Fluoride 2005;38:122–126.
  • Bonakdar RA, Guarneri E. Coenzyme Q10. Am Fam Physician 2005;72:1065–1070.
  • Lenaz G, Fato R, Formiggini G, Genova ML. The role of coenzyme Q in mitochondrial electron transport. Mitochondrion 2007;7:S8–S33.
  • Crane FL. Biochemical functions of coenzyme Q10. J Am Coll Nutr 2001;20:591–598.
  • El-Sheikh AA, Morsy MA, Mahmoud MM, Rifaai RA, Abdelrahman AM. Effect of coenzyme-Q10 on doxorubicin-induced nephrotoxicity in rats. Adv Pharmacol Sci 2012;2012:981461.
  • Sohet FM, Neyrinck AM, Pachikian BD, de Backer FC, Bindels LB, Niklowitz P, et al. Coenzyme Q10 supplementation lowers hepatic oxidative stress and inflammation associated with diet-induced obesity in mice. Biochem Pharmacol 2009;78:1391–1400.
  • Balercia G, Mancini A, Paggi F, Tiano L, Pontecorvi A, Boscaro M, et al. Coenzyme Q10 and male infertility. J Endocrinol Invest 2009;32:626–632.
  • Pan HC, Kao TK, Ou YC, Yang DY, Yen YJ, Wang CC, et al. Protective effect of docosahexaenoicacid against brain injury in ischemic rats. J Nutr Biochem 2009;20:715–725.
  • Priyamvada S, Khan SA, Khan MW, Khan S, Farooq N, Khan F, Yusufi AN. Studies on the protective effect of dietary fish oil on uranyl-nitrate-induced nephrotoxicity and oxidative damage in rat kidney. Prostaglandins Leukot Essent Fatty Acids 2010;82:35–44.
  • Wathes DC, Abayasekara DR, Aitken RJ. Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 2007;77:190–201.
  • Gliozzi TM, Zaniboni L, Maldjian A, Luzi F, Maertens L, Cerolini S. Quality and lipid composition of spermatozoa in rabbits fed DHA and vitamin E rich diets. Theriogenology 2009;71:910–919.
  • Nissen HP, Kreysel HW. Polyunsaturated fatty acids in relation to sperm motility. Andrologia 1983;15:264–269.
  • Zalata AA, Christophe AB, Depuydt CE, Schoonjans F, Comhaire FH. The fatty acid composition of phospholipids of spermatozoa from infertile patients. Mol Hum Reprod 1998;4:111–118.
  • Barcelos RC, Benvegnú DM, Boufleur N, Reckziegel P, Muller LG, Pase C, et al. Effects of omega-3 essential fatty acids (omega-3 EFAs) on motor disorders and memory dysfunction typical neuroleptic-induced: behavioral and biochemical parameter. Neurotox Res 2010;17:228–237.
  • Ashtiyani SC, Najafi H, Kabirinia K, Vahedi E, Jamebozorky L. Oral omega-3 fatty acid for reduction of kidney dysfunction induced by reperfusion injury in rats. Iran J Kidney Dis 2012;6:275–283.
  • Ozen OA, Cosar M, Sahin O, Fidan H, Eser O, Mollaoglu H, et al. The protective effect of fish n-3 fatty acids on cerebral ischemia in rat prefrontal cortex. Neurol Sci 2008;29:147–152.
  • Yousef MI, Salama AF. Propolis protection from reproductive toxicity caused by aluminium chloride in male rats. Food Chem Toxicol 2009;47:1168–1175.
  • Moselhy WA, Helmy NA, Abdel-Halim BR, Nabil TM, Abdel-Hamid MI. Role of ginger against the reproductive toxicity of aluminium chloride in albino male rats. Reprod Domest Anim 2012;47:335–343.
  • Zararsız İ, Kuş Davarcı M, Kuş MA, Kaman D, Sarsılmaz M. The protective effects of omega-3 fatty acids on rat testicular tissue. Dicle Med J 2011;38:382–386.
  • Uygur R, Aktas C, Tulubas F, Uygur E, Kanter M, Erboga M, et al. Protective effects of fish omega-3 fatty acids on doxorubicin-induced testicular apoptosis and oxidative damage in rats. Andrologia 2014;46:917–926.
  • Uygur R, Yagmurca M, Alkoc OA, Genc A, Songur A, Ucok K, Ozen OA. Effects of quercetin and fish n-3 fatty acids on testicular injury induced by ethanol in rats. Andrologia 2014;46:356–369.
  • El-Sheikh AA, Morsy MA, Mahmoud MM, Rifaai RA. Protective mechanisms of coenzyme-Q10 may involve up-regulation of testicular P-glycoprotein in doxorubicin-induced toxicity. Environ Toxicol Pharmacol 2014;37: 772–781.
  • Ghanbarzadeh S, Garjani A, Ziaee M, Khorrami A. Effects of L-carnitine and coenzyme q10 on impaired spermatogenesis caused by isoproterenol in male rats. Drug Res (Stuttg) 2014;64:449–453.
  • Ghanbarzadeh S, Garjani A, Ziaee M, Khorrami A. CoQ10 and L-Carnitine Attenuate the Effect of High LDL and Oxidized LDL on Spermatogenesis in Male Rats. Drug Res (Stuttg) 2014;64:510–515.
  • Zhu YZ, Li XW, Chen CX, Wang F, Li J, Hu CW, et al. Effects of aluminum trichloride on the trace elements and cytokines in the spleen of rats. Food Chem Toxicol 2012;50:2911–2915.
  • Liu FT, Li YF, Jin SM. Effects of aluminum intoxication on immune function in chickens. Asian J Ecotoxicol 2007; 2:445–449.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951;193:265–275.
  • Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351–358.
  • Tarafder PK, Rathore DP. Spectrophotometric determination of nitrite in water. Analyst 1988;113:1073–1076.
  • Beutler E, Duron O, Kelly MB. Improved method for the determination of blood glutathione. J Lab Clin Med 1963;61:882–888.
  • Aebi H. Catalase in vitro. Enzymol 1984;105:121–126.
  • Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158–169.
  • Nishikimi M, Roa NA, Yogi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 1972;46:849–854.
  • Tsugawa M, Iida S, Fujii H, Moriwaki K, Tarui S, Sugi M, et al. An enzyme-linked immunosorbent assay (ELISA) for adenosine 3′,5′-cyclic monophosphate (cAMP) in human plasma and urine using monoclonal antibody. J Immunoassay 1990;11:49–61.
  • Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc 2008;3: 1101–1108.
  • Bancroft JD, Stevens A. Theory and Practice of Histological Techniques, Fourth Edition, Queen's Medical Center, Notingham, University Hospital NHS Trust2002.
  • Hardy MP, Zirkin BR, Ewing LL. Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 1989;124:762–770.
  • LD Russell, RA Ettlin, AP Sinha Hikim, ED Clegg. Histological and Histopathological Evaluation of the Testis. Clearwater: Cache River Press. 1990;119–161.
  • Rebourcet D, O’Shaughnessy PJ, Monteiro A, Milne L, Cruickshanks L, Jeffrey N, et al. Sertoli Cells Maintain Leydig Cell Number and Peritubular Myoid Cell Activity in the Adult Mouse Testis. PLoS One 2014;9:e105687.
  • Ebokaiwe AP, Ramesh P, Mathur PP, Farombi EO. Transient effect of single dose exposure of Nigerian Bonny-light crude oil on testicular steroidogenesis in Wistar rats is accompanied by oxidative stress. Drug Chem Toxicol 2014;12:1–8.
  • Kokilavani P, Suriyakalaa U, Elumalai P, Abirami B, Ramachandran R, Sankarganesh A, Achiraman S. Antioxidant mediated ameliorative steroidogenesis by Commelina benghalensis L. and Cissus quadrangularis L. against quinalphos induced male reproductive toxicity. Pestic Biochem Physiol 2014;109:18–33.
  • Sun H, Hu C, Jia L, Zhu Y, Zhao H, Shao B, et al. Effect of aluminium exposure on serum sex hormones and androgen receptors expression in male rats. Biol Trace Elem Res 2011;144:1050–1058.
  • Rawi SM, Seif Al Nassr FM. Zinc sulphate and vitamin E alleviate reproductive toxicity caused by aluminium sulphate in male albino rats. Toxicol Ind Health 2015;31:221–234.
  • Kumar V, Bal A, Gill K. Susceptibility of mitochondrial superoxide dismutase to aluminium induced oxidative damage. Toxicology 2009;255:117–123.
  • Verstraeten SV, Oteiza PI. Effects of Al(3+) and related metals on membrane phase state and hydration: correlation with lipid oxidation. Arch Biochem Biophys 2000;375:340–346.
  • Kong S, Liochev S, Fridovich I. Aluminum(III) facilitates the oxidation of NADH by the superoxide anion. Free Radic Biol Med 1992;13:79–81.
  • Mendez-Alvarez E, Soto-Otero R, Hermida-Ameijeiras A, Lopez-Real AM, Labandeira-Garcia JL. Effects of aluminum and zinc on the oxidative stress caused by 6-hydroxydopamine autoxidation: relevance for the pathogenesis of Parkinson's disease. Biochim Biophys Acta 2002;1586:155–168.
  • Exley C. The pro-oxidant activity of aluminum. Free Radic Biol Med 2004;36:380–387.
  • Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen derivative stress: a review. Ann Bot 2003;91:179–194.
  • Aitken RJ, Clarkson JS, Fishel S. Generation of reactive oxygen species, lipid peroxidation and human sperm function. Biol Reprod 1989;40:183–197.
  • Turner TT, Lysiak JL. Oxidative stress: a common factor in testicular dysfunction. J Androl 2008;29:488–498.
  • Nehru B, Anand P. Oxidative damage following chronic aluminum exposure in adult and pup rat brains. J Trace Elem Med Biol 2005;19:203–208.
  • Bouasla I, Bouasla A, Boumendjel A, Messarah M, Abdennour C, Boulakoud MS, et al. Nigella sativa Oil Reduces Aluminium Chloride-Induced Oxidative Injury in Liver and Erythrocytes of Rats. Biol Trace Elem Res 2014;162:252–261.
  • Orihuela D, Meichtry V, Pregi N, Pizarro M. Short-term oral exposure to aluminum decreases glutathione intestinal levels and changes enzyme activities involved in its metabolism. J Inorg Biochem 2005;99:1871–1878.
  • Zhu YZ, Sun H, Fu Y, Wang J, Song M, Li M, et alEffects of sub-chronic aluminum chloride on spermatogenesis and testicular enzymatic activity in male rats. Life Sci 2014;102:36–40.
  • Chia SE, Ong CN, Chua LH, Ho LM, Tay KS. Comparison of Zinc concentrations in blood and seminal plasma and the various sperm parameters between fertile and infertile men. J Androl 2000;21:53–57.
  • Ebisch IM, van Heerde WL, Thomas CM, van der Put N, Wong WY, Steegers-Theunissen RP. C677T methylene tetrahydrofolate reductase polymorphism interferes with effect of folic acid and zinc sulphate on sperm concentration. Fertil Steril 2003;80:1190–1194.
  • El-Masry K, Alnasr AS, Kamal TH. Influences of season and dietary supplementation with selenium and vitamin E or zinc on some blood constituents and semen quality of New Zealand white rabbits males. World Rabbit Science 1994;2:79–86.
  • Colagar AH, Marzony ET, Chaichi MJ. Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 2009;29:82–88.
  • Martin GB, White CL, Markey CM, Blackberry MA. Effects of dietary zinc deficiency on the reproductive system of young male sheep: testicular growth and the secretion of inhibin and testosterone. J Reprod Fertil 1994;101:87–96.
  • Hamdi SA, Nassif OI, Ardawi MS. Effect of marginal or severe dietary zinc deficiency on testicular development and functions of the rat. Arch Androl 1997;38:243–253.
  • El-Ashmawy IM, Saleh A, Salama OM. Effects of marjoram volatile oil and grape seed extract on ethanol toxicity in male rats. Basic Clin Pharmacol Toxicol 2007;101:320–327.
  • Katyal R, Desigan B, Sodhi CP, Ojha S. Oral aluminum administration and oxidative injury. Biol Trace Elem Res 1997;57:125–130.
  • Bhasin P, Singla N, Dhawan DK. Protective role of zinc during aluminum-induced hepatotoxicity. Environ Toxicol 2014;29:320–327.
  • Kaur R, Dhanju CK, Kaur K. Effects of dietary selenium on biochemical composition of rat testis. Indian J Exp Biol 1999;37:509–511.
  • Guo CH, Hsu GS, Chuang CJ, Chen PC. Aluminum accumulation induced testicular oxidative stress and altered selenium metabolism in mice. Environ Toxicol Pharmacol 2009;27:176–181.
  • Nirmala RN, Shankarbhat K, Urban D. Effect of long term administration of aluminum chloride on oxidative stress and acetylcholinesterase activity in rat brains. IJPBS 2013; 3:616–622.
  • Gonzalez-Muñoz MJ, Meseguer I, Sanchez-Reus MI, Schultz A, Olivero R, Benedí J, Sánchez-Muniz FJ. Beer consumption reduces cerebral oxidation caused by aluminum toxicity by normalizing gene expression of tumor necrotic factor alpha and several antioxidant enzymes. Food Chem Toxicol 2008;46:1111–1118.
  • Ali HA, Afifi M, Abdelazim AM, Mosleh YY. Quercetin and Omega 3 Ameliorate Oxidative Stress Induced by Aluminium Chloride in the Brain. J Mol Neurosci 2014;53: 654–660.
  • Kono Y, Fridovich I. Superoxide radical inhibits catalase. J Biol Chem 1982;257:5751–5754.
  • Jayaraj R, Anand T, Rao PVL. Activity and gene expression profile of certain antioxidant enzymes to microcystin- LR induced oxidative stress in mice. Toxicology 2006; 220:136–146.
  • Xiong Q, Xie P, Li H, Hao L, Li G, Qiu T, Liu Y. Acute Effects of Microcystins Exposure on the Transcription of Antioxidant Enzyme Genes in Three Organs (Liver, Kidney, and Testis) of Male Wistar Rats. J Biochem Mol Toxicol 2010;24:361–367.
  • Nidhi G, Pant SC, Vijayaraghavan R, Rao PVL. Comparative toxicity evaluation of cyanobacterial peptide toxin microcystin variants (LR, RR YR) in mice. Toxicology 2003;188:285–296.
  • Rao PVL, Nidhi G, Jayaraj R, Bhaskar ASB, Jatav PC. Age dependent effects on biochemical variables and toxicity induced by cyclic peptide toxin microcystin-LR in mice. Comp Biochem Physiol C 2005;140:11–19.
  • Becaria A, Campbell A, Bondy SC. Aluminum as a toxicant. Toxicol Ind Health 2002;18:309–320.
  • Mahieu S, Calvo ML. Effect of chronic poisoning with aluminium on the renal handling of phosphate in the rat. Toxicol Lett 1998;94:47–56.
  • Guo C, Huang C, Chen S, Wang Hsu G. Serum and testicular testosterone and nitric oxide products in aluminum-treated mice. Environ Toxicol Pharmacol 2001;10:53–60.
  • Asahi M, Fujii J, Suzuki K, Seo HG, Kuzuya T, Hori M, et al. Inactivation of glutathione peroxidase by nitric oxide. Implication for cytotoxicity. J Biol Chem 1995;270: 21035–21039.
  • Kremser K, Stangl H, Pahan K, Singh I. Nitric oxide regulates peroxisomal enzyme activities. Eur J Clin Chem Clin Biochem 1995;33:763–774.
  • Hornsby PJ, Crivello JF. The role of lipid peroxidation and biological antioxidants in the function of the adrenal cortex II. Mol Cell Endocrinol 1983;30:123–147.
  • Guo CH, Lin CY, Yeh MS, Hsu GS. Aluminum-induced suppression of testosterone through nitric oxide production in male mice. Environ Toxicol Pharmacol 2005;19:33–40.
  • Dobashi M, Fujisawa M, Yamazaki T, Okuda Y, Kanzaki M, Tatsumi N, et al. Inhibition of steroidogenesis in Leydig cells by exogenous nitric oxide occurs independently of steroidogenic acute regulatory protein (star) mRNA. Arch Androl 2001;47:203–209.
  • Kostic TS, Andric SA, Maric D, Kovacevic RZ. Inhibitory effects of stress-activated nitric oxide on antioxidant enzymes and testicular steroidogenesis. J Steroid Biochem Mol Biol 2000;75:299–306.
  • Stocco DM. StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 2001;63:193–213.
  • Mansour MM, Hafiez AA, el-Kirdassy ZH, el-Malkh MN, Halawa FA, el-Zayat EM. Role of zinc in regulating the testicular function. Part 2. Effect of dietary zinc deficiency on gonadotropins, prolactin and testosterone levels as well as 3 beta-hydroxysteroid dehydrogenase activity in testes of male albino rats. Nahrung 1989;33:941–947.
  • Ascoli M, Fanelli F, Segaloff DL. The lutropin/choriogonadotropin receptor, a perspective. Endocr Rev 2002;23:141–174.
  • Stocco DM, Wang X, Jo Y, Manna PR. Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol Endocrinol 2005;19:2647–2659.
  • Anakwe OO, Payne AH. Noncoordinate regulation of de novo synthesis of cytochrome P-450 cholesterol side-chain cleavage and cytochrome P-450 17 alpha-hydroxylase/C17-20 lyase in mouse Leydig cell cultures: relation to steroid production. Mol Endocrinol 1987;1:595–603.
  • Mathur PP, Huang L, Kashou A, Vaithinathan S, Agarwal A. Environmental toxicants and testicular apoptosis. Reprod Sci J 2011;3:114–124.
  • Chen H, Cangello D, Benson S, Folmer J, Zhu H, Trush MA, Zirkin BR. Age-related increase in mitochondrial superoxide generation in the testosterone-producing cells of brown Norway rat testes: relationship to reduced steroidogenic function?. Exp Gerontol 2001;36:1361–1373.
  • Endo T, Aten RF, Leykin L, Behrman HR. Hydrogen peroxide evokes antisteroidogenic and antigonadotropic actions in human granulosa luteal cells. J Clin Endocrinol Metab 1993;76:337–342.
  • Stocco DM, Wells J, Clark BJ. The effects of hydrogen peroxide on steroidogenesis in mouse Leydig tumor cells. Endocrinology 1993;133:2827–2832.
  • Georgiou M, Prekins LM, Payne AH. Steroid synthesis dependent oxygen-mediated damage of mitochondrial and microsomal Cytochrome P-450 enzymes in rat Leydig cell cultures. Endocrinology 1987;121:1390–1399.
  • Walsh LP, McCormick C, Stocco DM. Roundup inhibits steroidogenesis by distrupting StAR expression. Environ Health Persp 2000;108:769–776.
  • Shi Z, Feng Y, Wang J, Zhang H, Ding L, Dai J. Perfluorododecanoic acid-induced steroidogenic inhibition is associated with steroidogenic acute regulatory protein and reactive oxygen species in cAMP-stimulated Leydig cells. Toxicol Sci 2010;114:285–294.
  • Mathur PP, D’Cruz SC. The effect of environmental contaminants on testicular function. Asian J Androl 2011;13: 585–591.
  • Behrman HR, Aten RF. Evidence that hydrogen peroxide blocks hormone-sensitive cholesterol transport into mitochondria of rat luteal cells. Endocrinology 1991;128: 2566–2958.
  • Reddy MM, Mahipal SV, Subhashini J, Reddy MC, Roy KR, Reddy GV, Reddy et al. Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod Toxicol 2006;22:493–500.
  • Artemenko IP, Zhao D, Hales DB, Hales KH, Jefcoate CR. Mitochondrial processing of newly synthesized steroidogenic acute regulatory protein (StAR), but not total StAR, mediates cholesterol transfer to cytochrome P450 side chain cleavage enzyme in adrenal cells. J Biol Chem 2001;276:46583–46596.
  • Diemer T, Allen JA, Hales KH, Hales DB. Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology 2003;144:2882–2891.
  • Tsai SC, Lu CC, Lin CS, Wang PS. Antisteroidogenic actions of hydrogen peroxide on rat Leydig cells. J Cell Biochem 2003;90:1276–1286.
  • Quinn PG, Payne AH. Steroid product-induced, oxygen-mediated damage of microsomal cytochrome P-450 enzymes in Leydig cell cultures. Relationship to desensitization. J Biol Chem 1985;260:2092–2099.
  • Yeap BB. Testosterone and ill-health in aging men. Nat Clin Pract Endocrinol Metab 2009;5:113–121.
  • Shahraki MR, Palan Mony EY, Zahed Asl S, Sarkaki AR, Shahraki AR. Effect of aluminium chloride injection in lateral ventricle on serum gonadotropines, testosterone and spermatogenesis in rats. J Med Sci 2008;8:410–414.
  • Reza SM, Palan MJ. Effect of Aluminium on Testosterone Hormones in Male Rat. J Med Sci 2006;6:296–299.
  • Platt B, Busselberg D. Actions of aluminium on voltage-activated calcium channel currents. Cell Mol Neurobiol 1994;14:819–829.
  • Clark BJ, Soo SC, Caron KM, Ikeda Y, Parker KL, Stocco DM. Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol Endocrinol 1995;9:1346–1355.
  • Murugesan P, Muthusamy T, Balasubramanian K, Arunakaran J. Effects of vitamins C and E on steroidogenic enzymes mRNA expression in polychlorinated biphenyl (Aroclor 1254) exposed adult rat Leydig cells. Toxicol 2007;232:170–182.
  • Omura T, Morohashi K. Gene regulation of steroidogenesis. J Steroid Biochem Mol Biol 1995;53:19–25.
  • Ihsan A, Wang X, Liu Z, Wang Y, Huang X, Liu Y, et al. Long-term mequindox treatment induced endocrine and reproductive toxicity via oxidative stress in male Wistar rats. Toxicol Appl Pharmacol 2011;252:281–288.
  • Barlow NJ, Phillips SI, Wallace DC, Gaido WK, Foster PMD. Qunatitative changes in gene expression in fetal rat testis following exposure to di(n-butyl) phathalate. Toxicol Sci 2003;73:431–451.
  • Bentinger M, Brismar K, Dallner G. The antioxidant role of coenzyme Q. Mitochondrion 2007;7:S41–S50.
  • Majumdar AS, Nirwane A, Kamble R. Coenzyme q10 abrogated the 28 days aluminium chloride induced oxidative changes in rat cerebral cortex. Toxicol Int 2014;21: 214–221.
  • Fouad AA, Al-Sultan AI, Yacoubi MT. Coenzyme Q10 counteracts testicular injury induced by sodium arsenite in rats. Eur J Pharmacol 2011;655:91–98.
  • Erol B, Bozlu M, Hanci V, Tokgoz H, Bektas S, Mungan G. Coenzyme Q10 treatment reduces lipid peroxidation, inducible and endothelial nitric oxide synthases, and germ cell-specific apoptosis in a rat model of testicular ischemia/reperfusion injury. Fertil Steril 2010;93:280–282.
  • Ramadan LA, Abd-Allah AR, Aly HA, Saad-el-Din AA. Testicular toxicity effects of magnetic field exposure andprophylactic role of coenzyme Q10 and L-carnitine in mice. Pharmacol Res 2002;46:363–370.
  • Ognjanovic BI, Markovic SD, Dordevic NZ, Trbojevi IS, Stajn AS, Saicic ZS. Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: Protective role of coenzyme Q10 and Vitamin E. Reprod Toxicol 2010;29:191–197.
  • Fouad AA, Jresat I, Hepatoprotective effect of coenzyme Q10 in rats with acetaminophen toxicity. Environ Toxicol Pharmacol 2012;33:158–167.
  • Nadjarzadeh A, Shidfar F, Amirjannati N, Vafa MR, Motevalian SA, Gohari MR, et al. Effect of Coenzyme Q10 supplementation on antioxidant enzymes activityand oxidative stress of seminal plasma: a double-blind randomised clinical trial. Andrologia 2014;46:177–183.
  • Safarinejad MR. The effect of coenzyme Q10 supplementation on partner pregnancy rate in infertile men with idiopathic oligoasthenoteratozoospermia: an open-label prospective study. Int Urol Nephrol 2012;44:689–700.
  • Mancini A, Leone E, Festa R, Grande G, Silvestrini A, de Marinis L, et al. Effects of testosterone on antioxidant systems in male secondary hypogonadism. J Androl 2008; 29:622–629.
  • Demirbag R, Yilmaz R, Erel O. The association of total antioxidant capacity with sex hormones. Scand Cardiovasc J 2005;39:172–176.
  • Abdel-Hady ESK, Abdel-Rahman GH. Protective effect of coenzyme q10 on cadmium-induced testicular damage in male rabbits. Am Eurasian J Toxicol Sci 2011;3:153–160.
  • Belardinelli R, Tiano L, Littarru GP. Oxidative stress, endothelial function and coenzyme Q10. Biofactors 2008; 32:129–133.
  • Jung HJ, Park EH, Lim CJ. Evaluation of anti-angiogenic, anti-inflammatory and antinociceptive activity of coenzyme Q(10) in experimental animals. J Pharm Pharmacol 2009; 61:1391–1395.
  • Rooney JP. The role of thiols, dithiols, nutritional factors and interacting ligands in the toxicology of mercury. Toxicology 2007;234:145–156.
  • Kelso KA, Redpath A, Noble RC, Speake BK. Lipid and antioxidant changes in spermatozoa and seminal plasma throughout the reproductive period of bulls. J Reprod Fertil 1997;109:1–6.
  • Lourenço ACS, Gomes C, Boareto AC, Mueller RP, Nihi F, Andrade LF, et al. Influence of oily vehicles on fetal testis and lipid profile of rats exposed to di-butyl phthalate. Hum Exp Toxicol 2014;33:54–63.
  • Hodge WG, Schachter HM, Barnes D, Pan Y, Lowcock EC, Zhang L, et al. Efficacy of omega-3 fatty acids in preventing age-related macular degeneration: a systematic review. Ophthalmology 2006;113:1165–1172.
  • Safarinejad MR. Effect of omega-3 polyunsaturated fatty acid supplementation on semen profile and enzymatic anti-oxidant capacity of seminal plasma in infertile men with idiopathic oligoasthenoteratospermia: a double-blind, placebo-controlled, randomised study. Andrologia 2010;43: 38–47.
  • Sarsilmaz M, Songur A, Ozyurt H, Kus I, Ozen OA, Ozyurt B, et al. Potential role of dietary omega-3 essential fatty acids on some oxidant/antioxidant parameters in rats’ corpus striatum. Prostaglandins Leukot Essent Fatty Acids 2003; 69:253–259.
  • Chaudhary M, Joshi DK, Tripathi S, Kulshrestha S, Mahdi AA. Docosahexaenoic acid ameliorates aluminum induced biochemical and morphological alteration in rat cerebellum. Ann Neurosci 2014;21:5–9.
  • Ciftci O, Cetin A, Aydin M, Kaya K, Oguz F. Fish oil, contained in eicosapentaenoic acid and docosahexaenoic acid, attenuates testicular and spermatological damage induced by cisplatin in rats. Andrologia 2014;46:1161–1168.
  • Castillo RL, Zepeda AB, Short SE, Figueroa E, Bustos-Obregon E, Farías JG. Protective effects of polyunsatutared fatty acids supplementation against testicular damage induced by intermittent hypobaric hypoxia in rats. J Biomed Sci 2015;22:8.
  • Li Y, Liu L, Wang B, Xiong J, Li Q, Wang J, Chen D. Impairment of reproductive function in a male rat model of non-alcoholic fatty liver disease and beneficial effect of N-3 fatty acid supplementation. Toxicol Lett 2013;222:224–232.
  • Sebokova E, Garg ML, Wierzbicki A, Thomson AB, Clandinin MT. Alteration of the lipid composition of rat testicular plasma membranes by dietary (n-3) fatty acids changes the responsiveness of Leydig cells and testosterone synthesis. J Nutr 1990;120:610–618.
  • Esmaeili V, Shahverdi AH, Alizadeh AR, Alipour H, Chehrazi M. Saturated, omega-6 and omega-3 dietary fatty acid effects on the characteristics of fresh, frozen–thawed semen and blood parameters in rams. Andrologia 2014;46: 42–49.
  • Latini G, Massaro M, De Felice C. Prenatal exposure to phthalates and intrauterine inflammation: a unifying hypothesis. Toxicol Sci 2005;85:743.
  • Kielar ML, Jeyarajah DR, Zhou XJ, Lu CY. Docosahexaenoic acid ameliorates murine ischemic acute renal failure and prevents increases in mRNA abundance for both TNF-alpha and inducible nitric oxide synthase. J Am Soc Nephrol 2003;14:389–396.
  • Li CC, Yang HT, Hou YC, Chiu YS, Chiu WC. Dietary fish oil reduces systemic inflammation and ameliorates sepsis-induced liver injury by up-regulating the peroxisome proliferator-activated receptor gamma-mediated pathway in septic mice. J Nutr Biochem 2014;25:19–25.

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