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Research Article

Naringenin; a bioflavonoid, impairs the reproductive potential of male mice

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Pages 417-427 | Received 21 Sep 2016, Accepted 11 Feb 2017, Published online: 10 Apr 2017

References

  • Aitken RJ, De Iuliis GN. (2006). Value of DNA integrity assays for fertility evaluation. Soc Reprod Fertil Suppl 65:81–92.
  • Annadurai T, Muralidharan AR, Joseph T, et al. (2012). Antihyperglycemic and antioxidant effects of a flavanone, naringenin, in streptozotocin–nicotinamide-induced experimental diabetic rats. J Physiol Biochem 68:307–18.
  • Azoulay-Zohar H, Israelson A, Salah AH, Shoshan-Barmatz V. (2004). In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem J 377:347–55.
  • Bergelson S, Pinkus R, Daniel V. (1994). Intracellular glutathione levels regulate Fos/Jun induction and activation of glutathione S-transferase gene expression. Cancer Res 54:36–40.
  • Bu T, Mi Y, Zeng W, Zhang C. (2011). Protective effect of quercetin on cadmium‐induced oxidative toxicity on germ cells in male mice. Anat Rec 294:520–6. p
  • Celeghini ECC, Nascimento J, Raphael CF, et al. (2010). Simultaneous assessment of plasmatic, acrosomal, and mitochondrial membranes in ram sperm by fluorescent probes. ARQ Bras Med Vet Zoo 62:536–43.
  • Collodel G, Federico MG, Geminiani M, et al. (2011). Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reprod Toxicol 31:239–46.
  • de Lamirande E, Jiang H, Zini A, et al. (1997). Reactive oxygen species and sperm physiology. Rev Reprod 2:48–54.
  • Evenson DP, LARSON KL, Jost LK. (2002). Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 23:25–43.
  • Fallahi F, Roghani M, Moghadami S. (2012). Citrus flavonoid naringenin improves aortic reactivity in streptozotocin-diabetic rats. Indian J Pharmacol 44:382.
  • Galati G, Chan T, Wu B, O'Brien PJ. (1999). Glutathione-dependent generation of reactive oxygen species by the peroxidase-catalyzed redox cycling of flavonoids. Chem Res Toxicol 12:521–5.
  • Galati G, Moridani MY, Chan TS, O’Brien PJ. (2001). Peroxidative metabolism of apigenin and naringenin versus luteolin and quercetin: glutathione oxidation and conjugation. Free Radic Biol Med 30:370–82.
  • Gaspar J, Rodrigues A, Laires A, et al. (1994). On the mechanisms of genotoxicity and metabolism of quercetin. Mutagenesis 9:445–9.
  • Girotti AW. (1990). Photodynamic lipid peroxidation in biological systems. Photochem Photobiol 51:497–509.
  • Griswold MD. (1998). The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol 9:411–16.
  • Halliwell B. (1996). Antioxidants in human health and disease. Annu Rev Nutr 16:33–50.
  • Hermenean A, Ardelean A, Stan M, et al. (2013). Protective effects of naringenin on carbon tetrachloride-induced acute nephrotoxicity in mouse kidney. Chem Biol Interact 205:138–47.
  • Hissin PJ, Hilf R. (1976). A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74:214–26.
  • Holstein AF, Eckmann C. (1986). Multinucleated spermatocytes and spermatids in human seminiferous tubules. Andrologia 18:5–16.
  • Iwamura C, Shinoda K, Yoshimura M, et al. (2010). Naringenin chalcone suppresses allergic asthma by inhibiting the type-2 function of CD4 T cells. Allergol Int 59:67–73.
  • Iwasaki A, Gagnon C. (1992). Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril 57:409–16.
  • Jain A, Yadav A, Bozhkov AI, et al. (2011). Therapeutic efficacy of silymarin and naringenin in reducing arsenic-induced hepatic damage in young rats. Ecotoxicol Environ Safe 74:607–14.
  • Jang M, Cai L, Udeani GO, et al. (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275:218–20.
  • Jiang YG, Peng T, Luo Y, et al. (2008). Resveratrol reestablishes spermatogenesis after testicular injury in rats caused by 2, 5-hexanedione. Chin Med J 121:1204–9.
  • Juan ME, González-Pons E, Munuera T, et al. (2005). Trans-resveratrol, a natural antioxidant from grapes, increases sperm output in healthy rats. J Nutr 135:757–60.
  • Khaki A, Fathiazad F, Nouri M, et al. (2010). Beneficial effects of quercetin on sperm parameters in streptozotocin‐induced diabetic male rats. Phytother Res 24:1285–91.
  • Khanduja KL, Verma A, Bhardwaj A. (2001). Impairment of human sperm motility and viability by quercetin is independent of lipid peroxidation. Andrologia 33:277–81.
  • Kono Y. (1978). Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189–95.
  • Kris-Etherton PM, Lefevre M, Beecher GR, et al. (2004). Bioactive compounds in nutrition and health-research methodologies for establishing biological function: the antioxidant and anti-inflammatory effects of flavonoids on atherosclerosis. Annu Rev Nutr 24:511–38.
  • Li G, Ma A, Shi W, Zhong XH. (2010). Quercetin protects hamster spermatogenic cells from oxidative damage induced by diethylstilboestrol. Andrologia 42:285–90.
  • Liu CM, Zheng YL, Lu J, et al. (2010). Quercetin protects rat liver against lead-induced oxidative stress and apoptosis. Environ Toxicol Pharmacol 29:158–66.
  • Liu RH, Finley J. (2005). Potential cell culture models for antioxidant research. J Agric Food Chem 53:4311–4.
  • Liu RH. (2004). Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 134:3479S–85S.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. (1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–75.
  • McLean DJ, Friel PJ, Pouchnik D, Griswold MD. (2002). Oligonucleotide microarray analysis of gene expression in follicle-stimulating hormone-treated rat Sertoli cells. Mol Endocrinol 16:2780–92.
  • Mi Y, Zhang C, Li C, et al. (2010). Quercetin attenuates oxidative damage induced by treatment of embryonic chicken spermatogonial cells with 4-nitro-3-phenylphenol in diesel exhaust particles. Biosci Biotechnol Biochem 74:934–8.
  • Moustafa MH, Sharma RK, Thornton J, et al. (2004). Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod 19:129–38.
  • Mulvihill EE, Assini JM, Sutherland BG, et al. (2010). Naringenin decreases progression of atherosclerosis by improving dyslipidemia in high-fat-fed low-density lipoprotein receptor–null mice. Arterioscler Thromb Vasc Biol 30:742–8.
  • Muthaiah VPK, Venkitasamy L, Michael FM, et al. (2013). Neuroprotective role of naringenin on carbaryl induced neurotoxicity in mouse neuroblastoma cells. J Pharmacol Pharmacother 4:192.
  • Nass‐Arden L, Breitbart H. (1990). Modulation of mammalian sperm motility by quercetin. Mol Reprod Dev 25:369–73.
  • Oguro T, Hayashi M, Nakajo S, et al. (1998). The expression of heme oxygenase-1 gene responded to oxidative stress produced by phorone, a glutathione depletor, in the rat liver; the relevance to activation of c-jun n-terminal kinase. J Pharm Exp Ther 287:773–8.
  • Paglia DE, Valentine WN. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–69.
  • Ranawat P, Kaushik G, Saikia UN, et al. (2013). Quercetin impairs the reproductive potential of male mice. Andrologia 45:56–65.
  • Ranawat P, Khanduja KL, Pathak CM. (2014). Resveratrol – an ingredient of red wine abrogates the reproductive capacity in male mice. Andrologia 46:650–8.
  • Revel A, Raanani H, Younglai E, et al. (2003). Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects lung from DNA damage and apoptosis caused by benzo [a] pyrene. J Appl Toxicol 23:255–61.
  • Ruchko M, Gorodnya O, LeDoux SP, et al. (2005). Mitochondrial DNA damage triggers mitochondrial dysfunction and apoptosis in oxidant-challenged lung endothelial cells. Am J Physiol Lung Cell Mol Physiol 288:L530–5.
  • Shin S, Jeon JH, Park D, et al. (2008). Trans-resveratrol relaxes the corpus cavernosum ex vivo and enhances testosterone levels and sperm quality in vivo. Arch Pharm Res 31:83–7.
  • Sikka SC. (2001). Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–62.
  • Surai P, Kostjuk I, Wishart G, et al. (1998). 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 64:119–32.
  • Svechnikov K, Spatafora C, Svechnikova I, et al. (2009). Effects of resveratrol analogs on steroidogenesis and mitochondrial function in rat Leydig cells in vitro. J Appl Toxicol 29:673–80.
  • Taepongsorat L, Tangpraprutgul P, Kitana N, Malaivijitnond S. (2008). Stimulating effects of quercetin on sperm quality and reproductive organs in adult male rats. Asian J Androl 10:249–58.
  • Tapanainen JS, Tilly JL, Vihko KK, Hsueh AJ. (1993). Hormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors. Mol Endocrinol 7:p643–50.
  • Testai L, Martelli A, Marino A, et al. (2013). The activation of mitochondrial BK potassium channels contributes to the protective effects of naringenin against myocardial ischemia/reperfusion injury. Biochem Pharmacol 85:1634–43.
  • Tormos C, Chaves FJ, Garcia MJ, et al. (2004). Role of glutathione in the induction of apoptosis and c-fos and c-jun mRNAs by oxidative stress in tumor cells. Cancer Lett 208:103–13.
  • Trush MA, Mimnaugh EG, Ginsburg E, Gram TE. (1981). In vitro stimulation by paraquat of reactive oxygen-mediated lipid peroxidation in rat lung microsomes. Toxicol Appl Pharmacol 60:p279–86.
  • Uguralp S, Usta U, Mizrak B. (2005). Resveratrol may reduce apoptosis of rat testicular germ cells after experimental testicular torsion. Eur J Pediatr Surg 15:333–6.
  • Williams RJ, Spencer JP, Rice-Evans C. (2004). Flavonoids: antioxidants or signalling molecules? Free Radic Biol Med 36:838–49.
  • Xia XY, Wu YM, Hou BS, et al. (2008). Evaluation of sperm mitochondrial membrane potential by JC-1 fluorescent staining and flow cytometry. Zhonghua Nan Ke Xue 14:135–8.

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