Melatonin ameliorates oxidative stress, modulates death receptor pathway proteins, and protects the rat cerebrum against bisphenol-A-induced apoptosis

Journal of the Neurological Sciences

Volumn 347, Issue 1-2, 2014, Pages 251-256

  El Missiry, Mohamed A ^a   Othman, Azza I ^a   Al Abdan, Monera A ^b   El Sayed, Aml A ^a  

^a Mansoura University   (Egypt)

^b PRINCESS NOURAH BINT ABDULRAHMAN UNIVERSITY   (Saudi Arabia)

Author keywords

Antioxidants; Apoptosis; Brain; Caspases 3 and 8; CD95 Fas; Death receptor pathway

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CASPASE 3; CASPASE 8; DEATH RECEPTOR; FAS ANTIGEN; GLUTATHIONE; MALONALDEHYDE; MELATONIN; PROTEIN P53; SUPEROXIDE DISMUTASE; ANTIOXIDANT; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BLOOD LEVEL; BRAIN CELL; BRAIN PROTECTION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; LIPID PEROXIDATION; MALE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; RAT; UPREGULATION; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; BENZHYDRYL COMPOUNDS; CEREBRUM; GLUTATHIONE; MALE; MALONDIALDEHYDE; MELATONIN; OXIDATIVE STRESS; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DEATH DOMAIN; SUPEROXIDE DISMUTASE;

EID: 84920032385     PISSN: 0022510X     EISSN: 18785883     Source Type: Journal    
DOI: 10.1016/j.jns.2014.10.009     Document Type: Article

References (73)

1. K.G. Akbulut, B. Gonul, and H. Akbulut Exogenous melatonin decreases age-induced lipid peroxidation in the brain Brain Res 1238 2008 31 35
2. J.D. Amaral, J.M. Xavier, C.J. Steer, and C.M. Rodrigues The role of p53 in apoptosis Discov Med 9 2010 145 152
3. M. Aydogan, A. Korkmaz, N. Barlas, and D. Kolankaya The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats Toxicology 249 2008 35 39
4. G. Baydas, R.J. Reiter, M. Akbulut, M. Tuzcu, and S. Tamer Melatonin inhibits neural apoptosis induced by homocysteine in hippocampus of rats via inhibition of cytochrome c translocation and caspase-3 activation and by regulating pro- and anti-apoptotic protein levels Neuroscience 135 2005 879 886
5. B.A. Bonsing, W.E. Corver, M.C. Gorsira, M. van Vliet, P.S. Oud, and C.J. Cornelisse Specificity of seven monoclonal antibodies against p53 evaluated with Western blotting, immunohistochemistry, confocal laser scanning microscopy, and flow cytometry Cytometry 28 1997 11 24
6. M. Campanella, C. Sciorati, G. Tarozzo, and M. Beltramo Flow cytometric analysis of inflammatory cells in ischemic rat brain Stroke 33 2002 586 592
7. A. Carpentieri, G. Diaz de Barboza, V. Areco, M. Peralta Lopez, and N. Tolosa de Talamoni New perspectives in melatonin uses Pharmacol Res 65 2012 437 444
8. J. Chen, L. Wang, C. Wu, Q. Hu, C. Gu, and F. Yan Melatonin-enhanced autophagy protects against neural apoptosis via a mitochondrial pathway in early brain injury following a subarachnoid hemorrhage J Pineal Res 56 2014 12 19
9. C.M. Chern, J.F. Liao, Y.H. Wang, and Y.C. Shen Melatonin ameliorates neural function by promoting endogenous neurogenesis through the MT2 melatonin receptor in ischemic-stroke mice Free Radic Biol Med 52 2012 1634 1647
10. S.C. D'Cruz, R. Jubendradass, M. Jayakanthan, S.J. Rani, and P.P. Mathur Bisphenol A impairs insulin signaling and glucose homeostasis and decreases steroidogenesis in rat testis: an in vivo and in silico study Food Chem Toxicol 50 2012 1124 1133
11. W. Dekant, and W. Volkel Human exposure to bisphenol A by biomonitoring: methods, results and assessment of environmental exposures Toxicol Appl Pharmacol 228 2008 114 134
12. O. Eizenberg, A. Faber-Elman, E. Gottlieb, M. Oren, V. Rotter, and M. Schwartz p53 plays a regulatory role in differentiation and apoptosis of central nervous system-associated cells Mol Cell Biol 16 1996 5178 5185
13. M.A. El-Missiry, T.A. Fayed, M.R. El-Sawy, and A.A. El-Sayed Ameliorative effect of melatonin against gamma-irradiation-induced oxidative stress and tissue injury Ecotoxicol Environ Saf 66 2007 278 286
14. Y. Feng, J. Yin, Z. Jiao, J. Shi, M. Li, and B. Shao Bisphenol AF may cause testosterone reduction by directly affecting testis function in adult male rats Toxicol Lett 211 2012 201 209
15. M.F. Fernandez, J.P. Arrebola, J. Taoufiki, A. Navalon, O. Ballesteros, and R. Pulgar Bisphenol-A and chlorinated derivatives in adipose tissue of women Reprod Toxicol 24 2007 259 264
16. T.W. Fischer, K. Kleszczynski, L.H. Hardkop, N. Kruse, and D. Zillikens Melatonin enhances antioxidative enzyme gene expression (CAT, GPx, SOD), prevents their UVR-induced depletion, and protects against the formation of DNA damage (8-hydroxy-2′-deoxyguanosine) in ex vivo human skin J Pineal Res 54 2013 303 312
17. Z.K. Hassan, M.A. Elobeid, P. Virk, S.A. Omer, M. ElAmin, and M.H. Daghestani Bisphenol A induces hepatotoxicity through oxidative stress in rat model Oxid Med Cell Longev 2012 2012 194829
18. H. He, W. Dong, and F. Huang Anti-amyloidogenic and anti-apoptotic role of melatonin in Alzheimer disease Curr Neuropharmacol 8 2010 211 217
19. B. Hoehn, M.A. Yenari, R.M. Sapolsky, and G.K. Steinberg Glutathione peroxidase overexpression inhibits cytochrome C release and proapoptotic mediators to protect neurons from experimental stroke Stroke 34 2003 2489 2494
20. S.B. Hong, Y.C. Hong, J.W. Kim, E.J. Park, M.S. Shin, and B.N. Kim Bisphenol A in relation to behavior and learning of school-age children J Child Psychol Psychiatry 54 2013 890 899
21. H. Iida, K. Maehara, M. Doiguchi, T. Mori, and F. Yamada Bisphenol A-induced apoptosis of cultured rat Sertoli cells Reprod Toxicol 17 2003 457 464
22. S. Jain, C.H. Kumar, U.D. Suranagi, and P.K. Mediratta Protective effect of N-acetylcysteine on bisphenol A-induced cognitive dysfunction and oxidative stress in rats Food Chem Toxicol 49 2011 1404 1409
23. W.S. Juan, H.W. Lin, Y.H. Chen, H.Y. Chen, Y.C. Hung, and S.H. Tai Optimal Percoll concentration facilitates flow cytometric analysis for annexin V/propidium iodine-stained ischemic brain tissues Cytometry A 81 2012 400 408
24. H. Kabuto, S. Hasuike, N. Minagawa, and T. Shishibori Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues Environ Res 93 2003 31 35
25. N. Karageorgos, N. Patsoukis, E. Chroni, D. Konstantinou, S.F. Assimakopoulos, and C. Georgiou Effect of N-acetylcysteine, allopurinol and vitamin E on jaundice-induced brain oxidative stress in rats Brain Res 1111 2006 203 212
26. U. Kilic, E. Kilic, R.J. Reiter, C.L. Bassetti, and D.M. Hermann Signal transduction pathways involved in melatonin-induced neuroprotection after focal cerebral ischemia in mice J Pineal Res 38 2005 67 71
27. U. Kilic, B. Yilmaz, R.J. Reiter, A. Yuksel, and E. Kilic Effects of memantine and melatonin on signal transduction pathways vascular leakage and brain injury after focal cerebral ischemia in mice Neuroscience 237 2013 268 276
28. M.E. Kim, H.R. Park, E.J. Gong, S.Y. Choi, H.S. Kim, and J. Lee Exposure to bisphenol A appears to impair hippocampal neurogenesis and spatial learning and memory Food Chem Toxicol 49 2011 3383 3389
29. P.O. Koh Melatonin prevents the injury-induced decline of Akt/forkhead transcription factors phosphorylation J Pineal Res 45 2008 199 203
30. G. Kroemer, L. Galluzzi, and C. Brenner Mitochondrial membrane permeabilization in cell death Physiol Rev 87 2007 99 163
31. S. Lee, K. Suk, I.K. Kim, I.S. Jang, J.W. Park, and V.J. Johnson Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calcium-induced reactive oxygen species, mitogen-activated protein kinases, and nuclear factor-kappaB J Neurosci Res 86 2008 2932 2942
32. G. Letechipia-Vallejo, I. Gonzalez-Burgos, and M. Cervantes Neuroprotective effect of melatonin on brain damage induced by acute global cerebral ischemia in cats Arch Med Res 32 2001 186 192
33. D. Li, Z. Zhou, D. Qing, Y. He, T. Wu, and M. Miao Occupational exposure to bisphenol-A (BPA) and the risk of self-reported male sexual dysfunction Hum Reprod 25 2010 519 527
34. Y.J. Li, T.B. Song, Y.Y. Cai, J.S. Zhou, X. Song, and X. Zhao Bisphenol A exposure induces apoptosis and upregulation of Fas/FasL and caspase-3 expression in the testes of mice Toxicol Sci 108 2009 427 436
35. H.W. Lin, and E.J. Lee Effects of melatonin in experimental stroke models in acute, sub-acute, and chronic stages Neuropsychiatr Dis Treat 5 2009 157 162
36. R. Liu, L. Xing, D. Kong, J. Jiang, L. Shang, and W. Hao Bisphenol A inhibits proliferation and induces apoptosis in micromass cultures of rat embryonic midbrain cells through the JNK, CREB and p53 signaling pathways Food Chem Toxicol 52 2013 76 82
37. Y. Liu, L. Zhang, H. Zhang, B. Liu, Z. Wu, and W. Zhao Exogenous melatonin modulates apoptosis in the mouse brain induced by high-LET carbon ion irradiation J Pineal Res 52 2012 47 56
38. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
39. F. Luchetti, B. Canonico, M. Betti, M. Arcangeletti, F. Pilolli, and M. Piroddi Melatonin signaling and cell protection function FASEB J 24 2010 3603 3624
40. J.C. Mayo, R.M. Sainz, I. Antolin, and C. Rodriguez Ultrastructural confirmation of neuronal protection by melatonin against the neurotoxin 6-hydroxydopamine cell damage Brain Res 818 2 1999 221 227
41. J.D. Meeker, S. Ehrlich, T.L. Toth, D.L. Wright, A.M. Calafat, and A.T. Trisini Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic Reprod Toxicol 30 2010 532 539
42. A. Menendez-Pelaez, and R.J. Reiter Distribution of melatonin in mammalian tissues: the relative importance of nuclear versus cytosolic localization J Pineal Res 15 1993 59 69
43. D. Nakamura, Y. Yanagiba, Z. Duan, Y. Ito, A. Okamura, and N. Asaeda Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol Toxicol Lett 194 2010 16 25
44. K. Nakamura, K. Itoh, K. Yoshimoto, T. Sugimoto, and S. Fushiki Prenatal and lactational exposure to low-doses of bisphenol A alters brain monoamine concentration in adult mice Neurosci Lett 484 2010 66 70
45. T. Negishi, Y. Ishii, S. Kyuwa, Y. Kuroda, and Y. Yoshikawa Inhibition of staurosporine-induced neuronal cell death by bisphenol A and nonylphenol in primary cultured rat hippocampal and cortical neurons Neurosci Lett 353 2003 99 102
46. M. Nishikimi, N. Appaji, and K. Yagi The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen Biochem Biophys Res Commun 46 1972 849 854
47. T. Obata, and S. Kubota Formation of hydroxy radicals by environmental estrogen-like chemicals in rat striatum Neurosci Lett 296 2000 41 44
48. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal Biochem 95 1979 351 358
49. A.I. Othman, M.A. El-Missiry, M.A. Amer, and M. Arafa Melatonin controls oxidative stress and modulates iron, ferritin, and transferrin levels in adriamycin treated rats Life Sci 83 2008 563 568
50. A. Pedreanez, J. Rincon, M. Romero, N. Viera, and J. Mosquera Melatonin decreases apoptosis and expression of apoptosis-associated proteins in acute puromycin aminonucleoside nephrosis Nephrol Dial Transplant 19 2004 1098 1105
51. F. Radogna, M. Diederich, and L. Ghibelli Melatonin: a pleiotropic molecule regulating inflammation Biochem Pharmacol 80 2010 1844 1852
52. R.J. Reiter Melatonin: clinical relevance Best Pract Res Clin Endocrinol Metab 17 2003 273 285
53. R.J. Reiter, D. Acuna-Castroviejo, D.X. Tan, and S. Burkhardt Free radical-mediated molecular damage. Mechanisms for the protective actions of melatonin in the central nervous system Ann N Y Acad Sci 939 2001 200 215
54. R.J. Reiter, J. Cabrera, R.M. Sainz, J.C. Mayo, L.C. Manchester, and D.X. Tan Melatonin as a pharmacological agent against neuronal loss in experimental models of Huntington's disease, Alzheimer's disease and parkinsonism Ann N Y Acad Sci 890 1999 471 485
55. R.J. Reiter, D.X. Tan, C. Osuna, and E. Gitto Actions of melatonin in the reduction of oxidative stress J Biomed Sci 7 2000 444 458
56. R.M. Sainz, J.C. Mayo, R.J. Reiter, I. Antolin, M.M. Esteban, and C. Rodriguez Melatonin regulates glucocorticoid receptor: an answer to its antiapoptotic action in thymus FASEB J 13 1999 1547 1556
57. J. Sedlak, and R.H. Lindsay Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent Anal Biochem 25 1968 192 205
58. R. Seidl, S. Fang-Kircher, B. Bidmon, N. Cairns, and G. Lubec Apoptosis-associated proteins p53 and APO-1/Fas (CD95) in brains of adult patients with Down syndrome Neurosci Lett 260 1999 9 12
59. N.K. Singhal, G. Srivastava, D.K. Patel, S.K. Jain, and M.P. Singh Melatonin or silymarin reduces maneb- and paraquat-induced Parkinson's disease phenotype in the mouse J Pineal Res 50 2011 97 109
60. D.X. Tan, R.J. Reiter, L.C. Manchester, M.T. Yan, M. El-Sawi, and R.M. Sainz Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger Curr Top Med Chem 2 2002 181 197
61. L.N. Vandenberg, I. Chahoud, V. Padmanabhan, F.J. Paumgartten, and G. Schoenfelder Biomonitoring studies should be used by regulatory agencies to assess human exposure levels and safety of bisphenol A Environ Health Perspect 118 2010 1051 1054
62. L.N. Vandenberg, R. Hauser, M. Marcus, N. Olea, and W.V. Welshons Human exposure to bisphenol A (BPA) Reprod Toxicol 24 2007 139 177
63. H. Viberg, A. Fredriksson, S. Buratovic, and P. Eriksson Dose-dependent behavioral disturbances after a single neonatal bisphenol A dose Toxicology 290 2011 187 194
64. H. Viberg, and I. Lee A single exposure to bisphenol A alters the levels of important neuroproteins in adult male and female mice Neurotoxicology 33 2012 1390 1395
65. Q. Wang, X.F. Zhao, Y.L. Ji, H. Wang, P. Liu, and C. Zhang Mitochondrial signaling pathway is also involved in bisphenol A induced germ cell apoptosis in testes Toxicol Lett 199 2010 129 135
66. X. Wang The antiapoptotic activity of melatonin in neurodegenerative diseases CNS Neurosci Ther 15 2009 345 357
67. X. Wang, B.E. Figueroa, I.G. Stavrovskaya, Y. Zhang, A.C. Sirianni, and S. Zhu Methazolamide and melatonin inhibit mitochondrial cytochrome C release and are neuroprotective in experimental models of ischemic injury Stroke 40 2009 1877 1885
68. Y.B. Wetherill, B.T. Akingbemi, J. Kanno, J.A. McLachlan, A. Nadal, and C. Sonnenschein In vitro molecular mechanisms of bisphenol A action Reprod Toxicol 24 2007 178 198
69. S.J. Won, D.Y. Kim, and B.J. Gwag Cellular and molecular pathways of ischemic neuronal death J Biochem Mol Biol 35 2002 67 86
70. H.J. Wu, C. Liu, W.X. Duan, S.C. Xu, M.D. He, and C.H. Chen Melatonin ameliorates bisphenol A-induced DNA damage in the germ cells of adult male rats Mutat Res 752 2013 57 67
71. C. Yu, F. Tai, Z. Song, R. Wu, X. Zhang, and F. He Pubertal exposure to bisphenol A disrupts behavior in adult C57BL/6 J mice Environ Toxicol Pharmacol 31 2011 88 99
72. C.M. Zehendner, L. Librizzi, M. de Curtis, C.R. Kuhlmann, and H.J. Luhmann Caspase-3 contributes to ZO-1 and Cl-5 tight-junction disruption in rapid anoxic neurovascular unit damage PLoS One 6 2011 e16760
73. Y. Zhang, A. Cook, J. Kim, S.V. Baranov, J. Jiang, and K. Smith Melatonin inhibits the caspase-1/cytochrome c/caspase-3 cell death pathway, inhibits MT1 receptor loss and delays disease progression in a mouse model of amyotrophic lateral sclerosis Neurobiol Dis 55 2013 26 35