Advertisement

Melatonin attenuates bisphenol A-induced toxicity of the adrenal gland of Wistar rats

  • Samuel Gbadebo Olukole
  • Damilare Olaniyi Lanipekun
  • Eunice Olufunke Ola-Davies
  • Bankole Olusiji Oke
Research Article
  • 50 Downloads

Abstract

This study investigated the role of melatonin (MLT) on adrenal gland toxicity induced by bisphenol A (BPA). Adult male rats were divided into four groups of seven animals each: Group I (control) received oral 0.2 ml canola oil; group II received intra-peritoneal 10 mg/kg BW/day MLT; and group III received oral BPA (10 mg/kg BW/day). Group IV rats were treated with same dose of BPA as group III with a concomitant intra-peritoneal 10 mg/kg BW/day MLT. All treatments lasted for 14 days. BPA significantly increased (P < 0.05) adrenal index, circulating levels of corticosterone and adrenocorticotropic hormone (ACTH) in the rats. BPA caused marked vascular congestion, hyperplasia, cellular distortion, increased lipid peroxidation, decreased antioxidant enzymes, and decreased expression of αSmooth muscle actin as well as vimentin proteins. The concomitant treatment with MLT ameliorated these BPA-induced alterations. It is likely that melatonin attenuates BPA-induced alterations of the adrenal gland of rats through the antioxidant defense mechanism.

Keywords

Bisphenol A toxicity Melatonin attenuation Adrenal gland Corticosterone Adrenocorticotropic hormone 

Notes

Acknowledgements

The authors hereby acknowledge the technical assistance received from the Pathology Section, Department of Para-clinical Studies, Faculty of Veterinary Science, University of Pretoria, South Africa. Dr. S.G. Olukole was a Post-Doctoral Fellow, Department of Anatomy and Physiology, Faculty of Veterinary Science, University of Pretoria, South Africa. Dr. Tayo Omobowale of the Department of Veterinary Medicine, Faculty of Veterinary Medicine, University of Ibadan, Nigeria provided the melatonin used in the study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Abdel-Maksoud FM, Leasor KR, Butzen K, Braden TD, Akingbemi BT (2015) Prenatal exposures of male rats to the environmental chemicals bisphenol A and Di(2-Ethylhexyl) phthalate impact the sexual differentiation process. Endocrinology 156:4672–4683CrossRefGoogle Scholar
  2. Abd-Elrazek AM, Ahmed-Farid OAH (2018) Protective effect of L-carnitine and L-arginine against busulfan-induced oligospermia in adult rat. Andrologia 50.  https://doi.org/10.1111/and.12806
  3. Aboul-Ezz HS, Khadrawy YA, Mourad IM (2015) The effect of bisphenol A on some oxidative stress parameters and acetylcholinesterase activity in the heart of male albino rats. Cytotechnology 67:145–155.  https://doi.org/10.1007/s10616-013-9672-1 CrossRefGoogle Scholar
  4. Amaral FG, Turati AO, Barone M, Scialfa JH, Do Carmo Buonfiglio D, Peres R, Peliciari-Garcia RA, Afeche SC, Lima L, Scavone C, Bordin S, Reiter RJ, Menna-Barreto L, Cipolla-Neto J (2014) Melatonin synthesis impairment as a new deleterious outcome of diabetes-derived hyperglycemia. J Pineal Res 57:67–79.  https://doi.org/10.1111/jpi.12144 CrossRefGoogle Scholar
  5. Anjum S, Rahman S, Kaur M, Ahmad F, Rashid H, Ansari RA, Raisuddin S (2011) Melatonin ameliorates bisphenol A-induced biochemical toxicity in testicular mitochondria of mouse. Food Chem Toxicol 49:2849–2854CrossRefGoogle Scholar
  6. Aydogan M, Korkmaz A, Barlas N, Kolankaya D (2008) The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology 249:35–39CrossRefGoogle Scholar
  7. Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888Google Scholar
  8. Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. JAMS 267:1244–1252Google Scholar
  9. Dawood GA (2016) Histological study of Bisphenol-A effect on the adrenal gland in the female rats. J Kerbala University 14, 87–95Google Scholar
  10. Doerge DR, Twaddle NC, Vanlandingham M (2011) Distribution of bisphenol A into tissues of adult, neonatal, and fetal Sprague-Dawley rats. Toxicol Appl Pharmacol 255(3):261–270CrossRefGoogle Scholar
  11. El-Beshbishy H, Ali HAA, El-Shafey M (2012) Lipoic acid mitigates bisphenol A-induced testicular mitochondrial toxicity in rats. Toxicol Ind Health 29:875–887CrossRefGoogle Scholar
  12. El-Ghamrawy TA (2014) The effect of liquid diet on the parotid gland and the protective role of L-carnitine: immunohistochemical and ultrastructural study. Folia Morphol (Warsz) 74:42–49.  https://doi.org/10.5603/FM.2015.0007 CrossRefGoogle Scholar
  13. El-Missiry MA, Abd El-Aziz AF (2000) Influence of melatonin on proliferation and antioxidant system in Ehrlich ascites carcinoma cells. Cancer Lett 151:119–125CrossRefGoogle Scholar
  14. El-Missiry MA, Othman AI, Monera A, Al-Abdan MA, El-Sayed AA (2014) Melatonin ameliorates oxidative stress, modulates death receptor pathway proteins, and protects the rat cerebrum against bisphenol-A-induced apoptosis. J Neurol Sci 347:251–256CrossRefGoogle Scholar
  15. García-Arevalo M, Alonso-Magdalena P, Dos Santos JR, Quesada I, Carneiro EM, Nadal A (2014) Exposure to bisphenol-A during pregnancy partially mimics the effects of a high-fat diet altering glucose homeostasis and gene expression in adult male mice. PLoS One 9:e100214.  https://doi.org/10.1371/journal.pone.0100214 CrossRefGoogle Scholar
  16. Gobbo MG, Dizeyi N, Abrahamsson PA, Bertilsson PA, Masitéli VS, Pytlowanciv EZ, Taboga SR, Goes RM (2015) Influence of melatonin on the proliferative and apoptotic responses of the prostate under normal and hyperglycemic conditions. J Diabetes Res 538529:1–18.  https://doi.org/10.1155/2015/538529 CrossRefGoogle Scholar
  17. Hassan ZK, Elobeid MA, Virk P, Omer SA, El-Amin M, Daghestani MH, Al Olayan EM (2012) Bisphenol A induces hepatotoxicity through oxidative stress in rat model. Oxidative Med Cell Longev 2012:1–6.  https://doi.org/10.1155/2012/194829 CrossRefGoogle Scholar
  18. Hijazi A, Guan H, Cernea M, Yang K (2015) Prenatal exposure to bisphenol A disrupts mouse lung development. FASEB J 29:4968–4977CrossRefGoogle Scholar
  19. Jollow DJ, Mitchell JR, Zampaglione N (1974) Bromobenzene-induced liver necrosis: protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11:151–169CrossRefGoogle Scholar
  20. Lack EE, Graham CW, Azumi N, Bitterman P, Runsnock EJ, O’brien W, Lynch JH (1991) Primary leiomyosarcoma of adrenal gland. Case report with immunohistochemical and ultrastructural study. Am J Surg Pathol 15:899–905CrossRefGoogle Scholar
  21. Marti O, Gavalda A, Gomez F, Armario A (1994) Direct evidence for chronic stress-induced facilitation of the adrenocorticotropin response to a novel stressor. Neuroendocrinology 60:1–7CrossRefGoogle Scholar
  22. Medwid S, Guan H, Yang K (2016) Prenatal exposure to bisphenol A disrupts adrenal steroidogenesis in adult mouse offspring. Environ Toxicol Pharmacol 43:203–208CrossRefGoogle Scholar
  23. Medwid S, Guan H, Yang K (2018) Bisphenol A stimulates adrenal cortical cell proliferation via ERβ-mediated activation of the sonic hedgehog signalling pathway. J Steroid Biochem Mol Biol 178:254–262CrossRefGoogle Scholar
  24. Miller WL, Auchus RJ (2011) The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev 32:81–151CrossRefGoogle Scholar
  25. Mitani F, Mukai K, Miyamoto H, Suematsu M, Ishimura Y (1999) Development of functional zonation in the rat adrenal cortex. Endocrinology 140:3342–3353CrossRefGoogle Scholar
  26. Ola-Davies OE, Olukole SG, Lanipekun DO (2018) Protective effect of gallic acid against bisphenol A-induced morphological alterations of the prostate gland of Wistar rats. Pharm Chem J 5:34–39Google Scholar
  27. Olukole SG, Adeagbo MA, Oke BO (2016) Histology and Histochemistry of the adrenal gland of the African Giant rat (Cricetomys gambianus, Waterhouse). Int J Morphol 34:1455–1460CrossRefGoogle Scholar
  28. Olukole SG, Ajani SO, Ola-Davies OE, Lanipekun DO, Aina OO, Oyeyemi MO, Oke BO (2018) Melatonin ameliorates bisphenol A-induced perturbations of the prostate gland of adult Wistar rats. Biomed Pharmacother 105:73–82CrossRefGoogle Scholar
  29. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767–801CrossRefGoogle Scholar
  30. Panagiotidou E, Zerva S, Mitsiou DJ, Alexis MN, Kitraki E (2014) Perinatal exposure to low-dose bisphenol a affects the neuroendocrine stress responsein rats. J Endocrinol 220:207–218CrossRefGoogle Scholar
  31. Patisaul HB, Adewale HB (2009) Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior. Front Behav Neurosci 3:10.  https://doi.org/10.3389/neuro.08.010.2009 CrossRefGoogle Scholar
  32. Poimenova A, Markaki E, Rahiotis C, Kitraki E (2010) Corticosterone-regulated actions in the rat brain are affected by perinatal exposure to low dose of bisphenol A. Neuroscience 167:741–749CrossRefGoogle Scholar
  33. Reiter RJ, Tan D-X, Gitto E, Sainz RM, Mayo JC, Leon JC, Manchester LC, Vijayalaxmi KE, Kilic U (2004) Pharmacological utility of melatonin in reducing oxidative cellular and molecular damage. Pol J Pharmacol 56:159–170Google Scholar
  34. Reiter RJ, Tan D-X, Terron MP, Flores LJ, Czarnocki Z (2007) Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol 54:1–9Google Scholar
  35. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, vom Saal FS (2007) In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24:199–224CrossRefGoogle Scholar
  36. Rochester JR (2013) Bisphenol A and human health: a review of the literature. Reprod Toxicol 42:132–155CrossRefGoogle Scholar
  37. Rosol TJ, Yarrington JT, Latendresse J, Charles C, Capen CC (2001) Adrenal gland: structure, function, and mechanisms of toxicity. Toxicol Pathol 29:41–48CrossRefGoogle Scholar
  38. Rubin BS, Soto AM (2009) Bisphenol A: perinatal exposure and body weight. Mol Cell Endocrinol 304:55–62.  https://doi.org/10.1016/j.mce.2009.02.023 CrossRefGoogle Scholar
  39. 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 265:56–67CrossRefGoogle Scholar
  40. Sandbo N, Taurin S, Yau DM, Kregel S, Mitchell R, Dulin NO (2007) Downregulation of smooth muscle α-actin expression by bacterial lipopolysaccharide. Cardiovasc Res 74:262–269CrossRefGoogle Scholar
  41. Sartain CV, Hunt PA (2016) An old culprit but a new story: bisphenol A and “NextGen” bisphenols. Fertil Steril 106:0015–0282CrossRefGoogle Scholar
  42. Tabassum H, Parvez S, Raisuddin S (2016) Melatonin abrogates nonylphenol-induced testicular dysfunction in Wistar rats. Andrologia 49.  https://doi.org/10.1111/and.12648
  43. Tan BLL, Kassim NM, Mohd MA (2003) Assessment of pubertal development in juvenile male rats after sub-acute exposure to bisphenol A and nonylphenol. Toxicol Lett 143:261–270CrossRefGoogle Scholar
  44. Tyl RW, Myers CB, Marr MC, Thomas BF, Keimowitz AR, Brine DR, Veselica MM, Fail PA, Chang TY, Seely JC, Joiner RL, Butala JH, Dimond SS, Cagen SZ, Shiotsuka RN, Stropp GD, Waechter JM (2002) Three generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley rats. Toxicol Sci 68:121–146.  https://doi.org/10.1093/toxsci/68.1.121 CrossRefGoogle Scholar
  45. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G (2012) Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Cien Saude Colet 17:407–434CrossRefGoogle Scholar
  46. Varshney R, Kale RK (1990) Effect of calmodulin antagonists on radiation induced lipid peroxidation in microsomes. Int J Radiat Biol 58:733–743CrossRefGoogle Scholar
  47. Wei X, Lee CKF, Yeung WSB, Giesy JP, Wong MH, Zhang X, Hecker M (2011) Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus-pituitary-gonadal axis of CD-1 mice. Reprod Toxicol 31:409–417CrossRefGoogle Scholar
  48. White PC, New MI, Dupont B (1987) Congenital adrenal hyperplasia. N Engl J Med 316(24):1519–1524CrossRefGoogle Scholar
  49. Wolff SF (1994) Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydrogen peroxides. Methods Enzymol 233:182–189CrossRefGoogle Scholar
  50. Yiin S-J, Sheu J-Y, Lin T-H (2000) Lipid peroxidation in rat adrenal glands after administration cadmium and role of essential metals. J Toxicol Environ Health A 62:47–56.  https://doi.org/10.1080/00984100050201668 CrossRefGoogle Scholar
  51. Yu C, Tai F, Song Z, Wu R, Zhang X, He F (2011) Pubertal exposure to bisphenol A disrupts behavior in adult C57BL/6 J mice. Environ Toxicol Pharmacol 31:88–99CrossRefGoogle Scholar
  52. Zhou R, Chen F, Feng X, Zhou L, Li Y, Chen L (2015a) Perinatal exposure to low-dose of bisphenol A causes anxiety-like alteration in adrenal axis regulation and behaviors of rat offspring: a potential role for metabotropicglutamate 2/3 receptors. J Psychiatr Res 64:121–129CrossRefGoogle Scholar
  53. Zhou Y, Tang Y, Tang J, Fei-Deng F, Gong G, Dai Y (2015b) Primary adrenal leiomyosarcoma: a case report and review of literature. Int J Clin Exp Pathol 8:4258–4263Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Veterinary AnatomyUniversity of IbadanIbadanNigeria
  2. 2.Department of Veterinary Physiology and BiochemistryUniversity of IbadanIbadanNigeria

Personalised recommendations