Effects of co-administered melatonin, fructose and bisphenol A (BPA) on rat epididymis and sperm characteristics

References

• Abdel Gawad FA, El-Shaarawy EA, Rizk AA, Sayed WM, Emam RA. 2015. Efficiency of selenium in attenuating epididymal histopathological changes in hypercholesterolaemic adult rat. Fol Morphol (Warsz). 74:295–302. doi:10.5603/FM.2015.0045.
   PubMed Web of Science ®Google Scholar
• Agbaje IM, Rogers DA, Mcvicar CM, McClure N, Atkinson AB, Mallidis C, Lewis SE. 2007. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod. 22:1871–1877. doi:10.1093/humrep/dem077.
   PubMed Web of Science ®Google Scholar
• Al-Hiyasat AS, Darmani H, Elbetieha AM. 2002. Effects of bisphenol A on adult male mouse fertility. Eur J Oral Sci. 110:163–167.
   PubMed Web of Science ®Google Scholar
• Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. 2006. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Env Health Perspect. 114:106–112. doi:10.1289/ehp.8451.
   PubMed Web of Science ®Google Scholar
• Ambe AK, Mondragon EC, Gonzales SE. 2008. Impact of spermatozoid head anomalies as predictor factor of nondetermined infertility. Ginecol Obstet Mex. 76:151–155.
   PubMedGoogle Scholar
• Beu CCL, Orsi AM, Domeniconi RF. 2009. Structure of the lining epithelium of the cauda epididymis of the golden hamster. J Vet Med C Anat Histol Embryol. 38:49–57. doi:10.1111/j.1439-0264.2008.00891.x.
   PubMed Web of Science ®Google Scholar
• Cai J, Wang C, Huang L, Chen M, Zuo Z. 2013. A novel effect of polychlorinated biphenyls: impairment of the tight junctions in the mouse epididymis. Toxicol Sci. 134:382–390. doi:10.1093/toxsci/kft106.
   PubMed Web of Science ®Google Scholar
• Caserta D, Di Segni N, Mallozzi M, Giovanale V, Mantovani A, Marci R, Moscarini M. 2014. Bisphenol A and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies. Reprod Biol Endocrinol. 12. doi:10.1186/1477-7827-12-37.
   PubMed Web of Science ®Google Scholar
• Chengmin W, Wenjuan F, Chao Q, Maosheng Y, Changjiang L, Suqin Q, Kedi Y. 2014. The pole of Pten/Akt signaling pathway ınvolved in BPA-ınduced apoptosis of rat Sertoli cells. Env Toxicol. 30:793–802.
   PubMed Web of Science ®Google Scholar
• Chitra KC, Rao KR, Mathur PP. 2003. Effect of bisphenol A and co-administration of bisphenol A and vitamin C on epididymis of adult rats: a histological and biochemical study. Asian J Androl. 5:203–208.
   PubMed Web of Science ®Google Scholar
• Clegg ED, Perreault SD, Klinefelter GR. 2001. Assessment of male reproductive toxicity. In: Hayes AW(ed.), Principles and methods of toxicology. 4th ed. Taylor & Francis; Philadelphia (PA); p. 11263–11300.
   Google Scholar
• Cyr DG, Hermo L, Egenberger N, Mertineit C, Trasler JM, Laird DW. 1999. Cellular immunolocalization of occludin during embryonic and postnatal development of the mouse testis and epididymis. Endocrinology. 140:3815–3825. doi:10.1210/endo.140.8.6903.
   PubMed Web of Science ®Google Scholar
• Cyr DG, Gregory M, Dube E, Dufresne J, Chan PT. 2007. Orchestration of occludins, claudins, catenins and cadherins as players involved in maintenance of the blood-epididymal barrier in animals and humans. Asian J Androl. 9:463–475. doi:10.1111/j.1745-7262.2007.00308.x.
   PubMed Web of Science ®Google Scholar
• Dernek D, Ömeroğlu S, Akçay NC, Kartal B, Dizakar SÖA, Türkoğlu İ, Aydin V. 2017. Possible effects of melatonin against rat uterus exposure to bisphenol A during neonatal period. Env Sci Pollut Res Int. 24:26829–26838. doi:10.1007/s11356-017-0187-8.
   PubMed Web of Science ®Google Scholar
• Dube E, Hermo L, Chan PT, Cyr DG. 2008. Alterations in gene expression in the caput epididymides of nonobstructive azoospermic men. Biol Reprod. 78:342–351. doi:10.1095/biolreprod.107.062760.
   PubMed Web of Science ®Google Scholar
• Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, Munoz-de-Toro M. 2007. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Env Health Perspect. 115:80–86. doi:10.1289/ehp.9282.
   PubMed Web of Science ®Google Scholar
• El Ghazzawy IF, Meleis AE, Farghaly EF, Solaiman A. 2011. Histological study of the possible protective effect of pomegranate juice on bisphenol-A induced changes of the caput epididymal epithelium and sperms of adult albino rats. Alexandr J Med. 2:125–137. doi:10.1016/j.ajme.2011.06.006.
   Google Scholar
• Furuse M. 2010. Molecular basis of the core structure of tight junctions. C S Harb Perspect Biol. 2:a002907.
   PubMed Web of Science ®Google Scholar
• Gitto E, Marseglia L, Manti S, D’Angelo G, Barberi I, Salpietro C, Reiter RJ. 2013. Protective role of melatonin in neonatal diseases. Oxid Med Cell Longev. 2013:980374. doi:10.1155/2013/980374.
   PubMed Web of Science ®Google Scholar
• Gomori G. 1939. The effect of certain factors on the results of silver impregnation for reticulum fibers. Am J Pathol. 15:493–495.
   PubMedGoogle Scholar
• Gregory M, Cyr DG. 2014. The blood-epididymis barrier and inflammation. Spermatogenesis. 31(4(2)):e979619.
   Google Scholar
• Gregory M, Dufresne J, Hermo L, Cyr D. 2001. Claudin-1 is not restricted to tight junctions in the rat epididymis. Endocrinology. 142:854–863. doi:10.1210/endo.142.2.7975.
   PubMed Web of Science ®Google Scholar
• Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ. 2003. Bisphenol A exposure causes meiotic aneuploidy in the female mouse. Curr Biol. 13:546–553.
   PubMed Web of Science ®Google Scholar
• Isomaa B. 2001. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 24:683–689. doi:10.2337/diacare.24.4.683.
   PubMed Web of Science ®Google Scholar
• Kasturi SS, Tannir J, Brannigan RE. 2008. The metabolic syndrome and male infertility. J Androl. 29:251–259. doi:10.2164/jandrol.107.003731.
   PubMedGoogle Scholar
• Konduracka E, Krzemieniecki K, Gajos G. 2014. Relationship between everyday use cosmetics and female breast cancer. Pol Arch Int Med. 124:264–269.
   Google Scholar
• Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller R, Perera FP, Champagne FA. 2013. Sex-specific epi-genetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci USA. 110:9956–9961. doi:10.1073/pnas.1214056110.
   PubMed Web of Science ®Google Scholar
• Levy S, Robaire B. 1999. Segment-specific changes with age in the expression of junctional proteins and the permeability of the blood-epididymis barrier in rats. Biol Reprod. 60:1392–1401. doi:10.1095/biolreprod60.6.1392.
   PubMed Web of Science ®Google Scholar
• Li C, Zhou X. 2015. Melatonin and male reproduction. Clin Chim Acta. 15:175–180.
   Google Scholar
• Lizarraga D, Vinardell MP, Noé V, van Delft JH, Alcarraz-Vizán G, van Breda SG, Staal Y, Günther UL, Reed MA, Ciudad CJ, Torres JL, Cascante M. 2011. A lyophilized red grape pomace containing proanthocyanidin-rich dietary fiber induces genetic and metabolic alterations in colon mucosa of female C57BL/6J mice. J Nutr. 141:1597–1604. doi:10.3945/jn.110.133199.
   PubMed Web of Science ®Google Scholar
• Manchester LC, Coto-Montes A, Boga JA, Andersen LPH, Zhou Z, Galano A, Vriend J, Tan DX, Reiter RJ. 2015. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 59:403–419. doi:10.1111/jpi.12267.
   PubMed Web of Science ®Google Scholar
• Mazroa Shireen A. 2011. Effect of bisphenol A on the cauda epididymis of adult male albino rats and the possible protective role of quercetin: a histological and immunohistochemical study. Egypt J Histol. 34:377–390. doi:10.1097/01.EHX.0000397468.63291.0c.
   Google Scholar
• Menale C, Mita DG, Diano N, Diano S. 2016. Adverse effects of bisphenol A exposure on glucose metabolism regulation. Biotechnol J. 10:122–130.
   Google Scholar
• Morgante G, Tosti C, Orvieto R, Musacchio MC, Piomboni P, De Leo V. 2011. Metformin improves semen characteristics of oligo-terato-asthenozoospermic men with metabolic syndrome. Fertil Steril. 95:2150–2152. doi:10.1016/j.fertnstert.2010.12.009.
   PubMed Web of Science ®Google Scholar
• Morrison CD, Brannigan RE. 2015. Metabolic syndrome and infertility in men. Best Pract Res Clin Obstet Gynaecol. 29:507–515. doi:10.1016/j.bpobgyn.2014.10.006.
   PubMed Web of Science ®Google Scholar
• Mota PC, Ramalho-Santos J. 2006. Comparison between different markers for sperm quality in the cat: diff-Quik as a simple optical technique to assess changes in the DNA of feline epididymal sperm. Theriogenology. 65:1360–1375. doi:10.1016/j.theriogenology.2005.08.012.
   PubMed Web of Science ®Google Scholar
• Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B. 2000. Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc Natl Acad Sci USA. 97:11603–11608. doi:10.1073/pnas.97.21.11603.
   PubMed Web of Science ®Google Scholar
• Oehninger S, Kruger T. 1995. The diagnosis of male infertility by semen quality: clinical signifinance of sperm morphology assesment. Hum Reprod. 10:1037–1038. doi:10.1093/oxfordjournals.humrep.a136088.
   PubMed Web of Science ®Google Scholar
• Othman A, Edrees GM, El-Missiry MA, Ali DA, Aboel-Nour M, Dabdoub BR. 2016. Melatonin controlled apoptosis and protected the testes and sperm quality against bisphenol A-induced oxidative toxicity. Toxicol Indust Health. 32:1537–1549. doi:10.1177/0748233714561286.
   PubMed Web of Science ®Google Scholar
• Ozan G, Kaya N, Yılmaz OF, Erdem E, Ozan E. 2014. Yüksek fruktoz diyeti ile metabolik sendrom oluşturulan ratların testis dokusunda ghrelin dağılımına oleuropeinin etkisi. Firat Üniv Saglik Bilimleri Vet Derg. 28:127–133.
   Google Scholar
• Prins GS, Hu WY, Shi GB, Hu DP, Majumdar S, Li G, Huang K, Nelles JL, Ho SM, Walker CL, Kajdacsy-Balla A, van Breemen RB. 2014. Bisphenol A promotes human prostate stem-progenitor cell self-renewal and increases in vivo carcinogenesis in human prostate epithelium. Endocrinology. 155:805–817. doi:10.1210/en.2013-1955.
   PubMed Web of Science ®Google Scholar
• Quitmeyer A, Roberts R. 2007. Babies, bottles, and bisphenol A: the story of a scientist mother. PLoS Biol. 5(7):e200. doi:10.1371/journal.pbio.0050200.
   PubMed Web of Science ®Google Scholar
• Rosenfeld CS. 2015. Bisphenol A and phthalate endocrine disruption of parental and social behaviors. Front Nutr. 9:57.
   Google Scholar
• Routledge EJ, White R, Parker MG, Sumpter JP. 2000. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ER beta. J Biol Chem. 275:35986–35993. doi:10.1074/jbc.M006777200.
   PubMed Web of Science ®Google Scholar
• Salian S, Doshi T, Vanage G. 2009. Neonatal exposure of male rats to bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis. Toxicology. 265:56–67. doi:10.1016/j.tox.2009.09.012.
   PubMed Web of Science ®Google Scholar
• Sanchez-Lozada LG, Tapia E, Jimenez A, Bautista P, Cristóbal M, Nepomuceno T, Soto V, Avila-Casado C, Nakagawa T, Johnson RJ, Herrera-Acosta J, Franco M. 2007. Fructose-induced metabolic syndrome is associated with glomerular hypertension and renal microvascular damage in rats. Am J Physiol Ren Physiol. 292:423–429. doi:10.1152/ajprenal.00124.2006.
   PubMed Web of Science ®Google Scholar
• Sato EF, Kobuchi H, Edashige K, Takahashi M, Yoshioka T, Utsumi K, Inoue M. 1992. Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat. FEBS Lett. 303:121–125.
   PubMed Web of Science ®Google Scholar
• Sullivan R, Mieusset R. 2016. The human epididymis: its function in sperm maturation. Hum Reprod Update. 22:574–587. doi:10.1093/humupd/dmw015.
   PubMed Web of Science ®Google Scholar
• Tiwari D, Vanage G. 2013. Mutagenic effect of bisphenol A on adult rat male germ cells and their fertility. Reprod Toxicol. 40:60–68. doi:10.1016/j.reprotox.2013.05.013.
   PubMed Web of Science ®Google Scholar
• Turner TT. 2008. De Graaf’s thread: the human epididymis. J Androl. 29:237–250. doi:10.2164/jandrol.107.004119.
   PubMedGoogle Scholar
• van der Merwe FH, Kruger TF, Oehninger SC, Lombard CJ. 2005. The use of semen parameters to identify the subfertile male in the general population. Gynecol Obstet Invest. 59:86–91. doi:10.1159/000082368.
   PubMed Web of Science ®Google Scholar
• Vandenberg L, Hauser R, Marcus M, Olea N, Welshons W. 2007. Human exposure to bisphenol A (BPA). Reprod Toxicol. 24:139–177. doi:10.1016/j.reprotox.2007.07.010.
   PubMed Web of Science ®Google Scholar
• Vriend J, Reiter RJ. 2015. Melatonin feedback on clock genes: a theory involving the proteasome. J Pineal Res. 58:1–11. doi:10.1111/jpi.12189.
   PubMed Web of Science ®Google Scholar
• Weissgerber P, Kriebs U, Tsvilovskyy V, Olausson J, Kretz O, Stoerger C, Vennekens R, Wissenbach U, Middendorff R, Flockerzi V, Freichel M. 2011. Male fertility depends on Ca2+ absorption by TRPV6 in epididymal epithelia. Sci Sign. 3(4(171)):ra27.
   Google Scholar
• WHO. 2010. World health organization department of reproductive health and research. WHO laboratory manual for the examination and processing of human semen. 5th editon. Switzerland: WHO.
   Google Scholar
• Wisniewski P, Romano RM, Kizys MML, Oliveira KC, Kasamatsu T, Giannocco G, Chiamolera MI, Dias-da-Silva MR, Romano MA. 2015. Adult exposure to bisphenol A (BPA) in Wistar rats reduces sperm quality with disruption of the hypothalamic-pituitary-testicular axis. Toxicology. 329:1–9. doi:10.1016/j.tox.2015.01.002.
   PubMed Web of Science ®Google Scholar
• Wong SK, Chin KY, Suhaimi FH, Fairus A, Ima-Nirwana S. 2016. Animal models of metabolic syndrome: a review. Nutr Metab. 13:65. doi:10.1186/s12986-016-0123-9.
   Google Scholar
• Zhang M, Dai X, Lu Y, Miao Y, Zhou C, Cui Z, Liu H, Xiong B. 2017. Melatonin protects oocyte quality from bisphenol A-induced deterioration in the mouse. J Pineal Res. 62:3. doi:10.1111/jpi.12396
   Web of Science ®Google Scholar