The effect of pre- and postnatal exposure to a mixture daidzein and genistein on the reproductive system of male rats

Mariola Marchlewicz, Dagmara Szypulska-Koziarska, Irena Baranowska-Bosiacka, Ewa Duchnik, Barbara Wiszniewska, Joanna Kruk

Abstract


Introduction: There is growing interest in the risk or benefits soybean food known as rich in isoflavones, due to their interactions with endogenous estrogen signal transduction pathway. Recent studies provide evidence that isoflavones can affect the reproductive and endocrine system under regular diet.

The aim of this study was to determine how the long-lasting administration of the key isoflavones, genistein and daidzein, may change morphology of the testis and the function of the epididymal antioxidant system of male rats.

Materials and methods: Male rats were treated by genistein and daidzein, in combination 2 (S2) or 20 (S20) mg/kg body weight per day for 5 days weekly mixed with regular rat chow from prenatal life until to sexual maturity. The control groups were fed without isoflavones.

Results: The findings show that the body, testis and cauda epididymis weights, testosterone level in blood plasma were significantly lower than controls in the S20 group (p < 0.05). Also, superoxide dismutase activity in the epididymis, catalase activity in the testis, and glutathione peroxidase activity in the caput epididymis were significantly decreased (p < 0.05). Treating with these isoflavones significantly suppressed lipid peroxides levels in the epididymis (p < 0.05). Furthermore, presence of prematurely exfoliated gametogenic cells was observed in seminiferous tubules as well as the architectural disorganization of the seminiferous epithelium.

Conclusions: These findings suggest that isoflavones, if consumed chronically at a dose as for the S20 group may act not only as antioxidants, but they can be a risk for the male rats reproductive system dysfunction.

 


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References


Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. Oxidative stress and male reproductive health. Asian J Androl 2014;16(1):31-8.

Aitken RJ, De Iuliis GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod 2010;16(1):3-13.

Hermo L, Pelletier RM, Cyr DG, Smith CE. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech 2010;73(4):241-78.

Ko EY, Sabanehg ES Jr, Agarwal A. Male infertility testing: reactive oxygen species and antioxidant capacity. Fertil Steril 2014;102(6):1518-27.

Walczak-Jędrzejowska R. Stres oksydacyjny a niepłodność męska. Część I: czynniki wywołujące stres oksydacyjny w nasieniu. Post Androl Online 2015;2(1):5-15.

Sharpe RM, Irvine DS. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health? BMJ 2004;328(7437):447-51.

Cederroth CR, Zimmermann C, Nef S. Soy, phytoestrogens and their impact on reproductive health. Mol Cell Endocrinol 2012;355(2):192-200.

Smoliga JM, Baur JA, Hausenblas HA. Resveratrol and health – a comprehensive review of human clinical trials. Mol Nutr Food Res 2011;55(8):1129-41.

Sharpe RM, Skakkebaek NE. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet 1993;341(8857):1392-5.

Caceres S, Silvan G, Martinez-Fernandez L, Illera MJ, Millan P, Monsalve B, et al. The effects of isoflavones on androgens and glucocorticoids during puberty on male Wistar rats. Reprod Domest Anim 2014;49(4):611-7.

Cederroth CR, Auger J, Zimmermann C, Eustache F, Nef S. Soy, phyto-oestrogens and male reproductive function: a review. Int J Androl 2010;33(2):304-16.

Sirotkin AV, Harrath AH. Phytoestrogens and their effects. Eur J Pharmacol 2014;741:230-6.

Li L, Chen X, Luo Q, Huang C, Liu W, Chen Z. Effects of soy isoflavones on testosterone synthetase in diet-induced obesity male rats. Int J Clin Exp Pathol 2017;10(9):9202-12.

Agarwal A, Sekhon LH. The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb) 2010;13(4):217-25.

Eustache F, Mondon F, Canivenc-Lavier MC, Lesaffre C, Fulla Y, Berges R, et al. Chronic dietary exposure to a low-dose mixture of genistein and vinclozolin modifies the reproductive axis, testis transcriptome, and fertility. Environ Health Perspect 2009;117(8):1272-9.

Napier ID, Simon L, Perry D, Cooke PS, Stocco DM, Sepehr E, et al. Testicular development in male rats is sensitive to a soy-based diet in the neonatal period. Biol Reprod 2014;90(2):40. doi: 10.1095/biolreprod.113.113787.

Lazari MFM, Lucas TFG, Yasuhara F, Gomes GRO, Siu ER, Royer C, et al. Estrogen receptors and function in the male reproductive system. Arq Bras Endocrinol Metab 2009;53(8):923-33.

Sherrill JD, Sparks M, Dennis J, Mansour M, Kemppainen BW, Bartol FF, et al. Develompental exposures of male rats to soy isoflavones impact Leydig cell differentiation. Biol Reprod 2010;83(3):488-501.

Carreau S, Hess RA. Oestrogens and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010;365(1546):1517-35.

McLachlan JA. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev 2001;22(3):319-41.

Weber KS, Setchell KDR, Stocco DM, Lephart ED. Dietary soy-phytoestrogens decrease testosterone levels and prostate weight without altering LH, prostate 5α-reductase or testicular steroidogenic acute regulatory peptide levels in adult male Sprague–Dawley rats. J Endocrinol 2001;170(3):591-9.

Eumkeb G, Tanphonkrang S, Sirichaiwetchakoon K, Hengpratom T, Naknarong W. The synergy effect of daidzein and genistein isolated from Butea superba Roxb. on the reproductive system of male mice. Nat Prod Res 2017;31(6):672-5.

Mitchell JH, Cawood EW, Kinniburgh D, Provan A, Collins AR, Irvine DS. Effect of a phytoestrogen food supplement on reproductive health in normal males. Clin Sci (Lond) 2001;100(6):613-8.

Doerge DR. Bioavailability of soy isoflavones through placental/lactational transfer and soy food. Toxicol Appl Pharmacol 2011;254(2):145-7.

Faqi AS, Johnson WD, Morrissey RL, McCormick DL. Reproductive toxicity assessment of chronic dietary exposure to soy isoflavones in male rats. Reprod Toxicol 2004;18(4):605-11.

Piotrowska K, Baranowska-Bosiacka I, Marchlewicz M, Gutowska I, Noceń I, Zawiślak M, et al. Changes in male reproductive system and mineral metabolism induced by soy isoflavones administrated to rats from prenatal life until sexual maturity. Nutrition 2011;27(3):372-9.

Neumann F, Schenck B. Formal genesis of giant cells in the germinal epithelium in the rat thioglucose model. Andrologia 1997;9(4):323-8.

Hwang KA, Kang NH, Yi BR, Lee HR, Park MA, Choi KC. Genistein, a soy phytoestrogen, prevents the growth of BG-1 ovarian cancer cells induced by 17β-estradiol or bisphenol A via the inhibition of cell cycle progression. Int J Oncol 2013;42(2):733-40.

Prietsch RF, Monte LG, da Silva FA, Beira FT, Del Pino FA, Campos VF, et al. Genistein induces apoptosis and autophagy in human breast MCF-7 cells by modulating the expression of proapoptotic factors and oxidative stress enzymes. Mol Cell Biochem 2014;390(1-2):235-42.

Brown NM, Lindley SLL, Witte DP, Setchell KDR. Impact of perinatal exposure to equol enantiomers on reproductive development in rodents. Reprod Toxicol 2011;32(1):33-42.

Kolasa A, Marchlewicz M, Świder M, Sikorski A, Wenda-Różewicka L, Wiszniewska B. Najądrze. In: Piasecka M, editor. Układ płciowy męski. Badania kliniczne i doświadczalne. Szczecin: Wydawnictwo Pomorskiego Uniwersytetu Medycznego w Szczecinie; 2013. p. 419-31.

Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014;32(1):1-17.

Azenabor A, Ekun AO, Akinloye O. Impact of inflammation on male reproductive tract. J Reprod Infertil 2015;16(3):123-9.

Nikolopoulou M, Soucek DA, Vary JV. Changes in the lipid content of boar sperm plasma membranes during epididymal maturation. Biochim Biophys Acta 1985;815(3):486-98.

Quideau S, Deffieux D, Douat-Casassus C, Pouységu L. Plant polyphenols: chemical properties biological activities, and synthesis. Angew Chem Int Ed Engl 2011;50(3):586-621.

Singh P, Sharma S, Rath SK. Genistein induces deleterious effects during its acute exposure in Swiss mice. Biomed Res Int 2014;2014:619617. doi: 10.1155/2014/619617.

Park K, Jeon S, Song YJ, Yi LSH. Proteomic analysis of boar spermatozoa and quantity changes of superoxide dismutase 1, glutathione peroxidase, and peroxiredoxin 5 during epididymal maturation. Anim Reprod Sci 2012;135(1-4):53-61.

Mahmoud AM, Yang W, Bosland MC. Soy isoflavones and prostate cancer: a review of molecular mechanism. J Steroid Biochem Mol Biol 2014;140:116-32.

Abarikwu SO, Otuechere CA, Ekor M, Monwuba K, Osobu D. Rutin ameliorates cyclophosphamide-induced reproductive toxicity in male rats. Toxicol Int 2012;19(2):207-14.

Bouayed J, Bohn T. Exogenous antioxidants – Double-edged swords in cellular redox state: Health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid Med Cell Longev 2010;3(4):228-37.

Barbosa AC, Lajolo FM, Genovese MI. Effect of free or protein-associated soy isoflavones on the antioxidant status in rats. J Sci Food Agric 2011;91(4):721-31.

Borrás C, Gambini J, Gómez-Cabrera MC, Sastre J, Pallardó FV, Mann GE, et al. Genistein, a soy isoflavone, up-regulates expression of antioxidant genes: involvement of estrogen receptors, ERK1/2, and NFκB. FASEB J 2006;20(12):2136-8.

Kładna A, Berczyński P, Kruk I, Piechowska T, Aboul-Enein HY. Studies on the antioxidant properties of some phytoestrogens. Luminescence 2016;31(6):1201-6.

Bedford JM. The epididymis re-visited: a personal view. Asian J Androl 2015;17(5):693-8.

Zhao E, Mu Q. Phytoestrogen biological actions on Mammalian reproductive system and cancer growth. Sci Pharm 2011;79(1):1-20.




DOI: https://doi.org/10.21164/pomjlifesci.550

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