Bisphenol A and its analogs bisphenol B, bisphenol F, and bisphenol S: Comparative in vitro and in vivo studies on the sperms and testicular tissues of rats

Chemosphere

Volumn 209, Issue , 2018, Pages 508-516

  Ullah, Asad ^a   Pirzada, Madeeha ^a   Jahan, Sarwat ^a   Ullah, Hizb ^a   Shaheen, Ghazala ^a   Rehman, Humaira ^a   Siddiqui, Mariyam Fatima ^a   Butt, Maisra Azhar ^a  

^a QUAID I AZAM UNIVERSITY   (Pakistan)

Author keywords

Antioxidant enzymes; Bisphenol A; Bisphenol B; Bisphenol F; Bisphenol S; Histology; Oxidative stress; Testosterone

Indexed keywords

ANTIOXIDANTS; CONSUMER PRODUCTS; ENZYMES; HISTOLOGY; OXIDATIVE STRESS; RATS; TISSUE;

ANTIOXIDANT ENZYME; BIS-PHENOL A; BISPHENOL F; BISPHENOLS; TESTOSTERONE;

PHENOLS;

4,4' ISOPROPYLIDENEDIPHENOL; ANTIOXIDANT; BISPHENOL B; BISPHENOL F; BISPHENOL S; CATALASE; LIPID; PEROXIDASE; PHENOL DERIVATIVE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TESTOSTERONE; UNCLASSIFIED DRUG; BENZHYDRYL DERIVATIVE; BIS(4-HYDROXYPHENYL)SULFONE; ESTROGEN RECEPTOR; SCAVENGER; SULFONE;

ANTIOXIDANT; CHEMICAL COMPOUND; COMPARATIVE STUDY; CONCENTRATION (COMPOSITION); ENZYME; ENZYME ACTIVITY; OXIDATIVE STRESS; PROTEIN; REACTIVE OXYGEN SPECIES; RODENT; SPERM; TESTOSTERONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; EPIDIDYMIS; EVALUATION STUDY; EXPOSURE; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN CONTENT; PROTEIN EXPRESSION; RAT; SPERM; SPERMATOGENESIS; TESTIS TISSUE; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE RELEASE; ANIMAL; DRUG EFFECT; METABOLISM; PATHOLOGY; SPERMATOZOON; SPRAGUE DAWLEY RAT; TESTIS;

ANIMALIA; RATTUS;

ANIMALS; BENZHYDRYL COMPOUNDS; FREE RADICAL SCAVENGERS; IN VITRO TECHNIQUES; MALE; OXIDATIVE STRESS; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, ESTROGEN; SPERMATOZOA; SULFONES; TESTIS; TESTOSTERONE;

EID: 85049308396     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2018.06.089     Document Type: Article

References (73)

1. Aebi, H., [13] Catalase in vitro. Meth. Enzymol. 105 (1984), 121–126.
2. Ahn, K.C., Zhao, B., Chen, J., Cherednichenko, G., Sanmarti, E., Denison, M.S., Lasley, B., Pessah, I.N., Kültz, D., Chang, D.P., In vitro biologic activities of the antimicrobials triclocarban, its analogs, and triclosan in bioassay screens: receptor-based bioassay screens. Environ. Health Perspect., 116, 2008, 1203.
3. Allard, P., Bisphenol A. Biomarkers in Toxicology. 2014, Elsevier, 459–474.
4. Alonso-Magdalena, P., Ropero, A.B., Soriano, S., García-Arévalo, M., Ripoll, C., Fuentes, E., Quesada, I., Nadal, Á., Bisphenol-A acts as a potent estrogen via non-classical estrogen triggered pathways. Mol. Cell. Endocrinol. 355 (2012), 201–207.
5. Bergmann, O., Zdunek, S., Felker, A., Salehpour, M., Alkass, K., Bernard, S., Sjostrom, S.L., Szewczykowska, M., Jackowska, T., Dos Remedios, C., Dynamics of cell generation and turnover in the human heart. Cell 161 (2015), 1566–1575.
6. Braun, J.M., Kalkbrenner, A.E., Calafat, A.M., Yolton, K., Ye, X., Dietrich, K.N., Lanphear, B.P., Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 128 (2011), 873–882.
7. Cabado, A.G., Aldea, S., Porro, C., Ojea, G., Lago, J., Sobrado, C., Vieites, J.M., Migration of BADGE (bisphenol A diglycidyl-ether) and BFDGE (bisphenol F diglycidyl-ether) in canned seafood. Food Chem. Toxicol. 46 (2008), 1674–1680.
8. Cabaton, N., Chagnon, M.-C., Lhuguenot, J.-C., Cravedi, J.-P., Zalko, D., Disposition and metabolic profiling of bisphenol F in pregnant and nonpregnant rats. J. Agric. Food Chem. 54 (2006), 10307–10314.
9. Calafat, A.M., Weuve, J., Ye, X., Jia, L.T., Hu, H., Ringer, S., Huttner, K., Hauser, R., Exposure to bisphenol A and other phenols in neonatal intensive care unit premature infants. Environ. Health Perspect., 117, 2009, 639.
10. Calafat, A.M., Ye, X., Wong, L.-Y., Reidy, J.A., Needham, L.L., Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ. Health Perspect., 116, 2008, 39.
11. Cano-Nicolau, J., Vaillant, C., Pellegrini, E., Charlier, T.D., Kah, O., Coumailleau, P., Estrogenic effects of several BPA analogs in the developing zebrafish brain. Front. Neurosci., 10, 2016.
12. Carlberg, I., Mannervik, E., Glutathione concentration in rat brain. J. Biol. Chem. 250 (1975), 4475–4480.
13. Chen, M.Y., Ike, M., Fujita, M., Acute toxicity, mutagenicity, and estrogenicity of bisphenol-A and other bisphenols. Environ. Toxicol. 17 (2002), 80–86.
14. Cobellis, L., Colacurci, N., Trabucco, E., Carpentiero, C., Grumetto, L., Measurement of bisphenol A and bisphenol B levels in human blood sera from healthy and endometriotic women. Biomed. Chromatogr. 23 (2009), 1186–1190.
15. Cunha, S., Fernandes, J., Quantification of free and total bisphenol A and bisphenol B in human urine by dispersive liquid–liquid microextraction (DLLME) and heart-cutting multidimensional gas chromatography–mass spectrometry (MD–GC/MS). Talanta 83 (2010), 117–125.
16. Delfosse, V., Grimaldi, M., Pons, J.-L., Boulahtouf, A., Le Maire, A., Cavailles, V., Labesse, G., Bourguet, W., Balaguer, P., Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes. Proc. Natl. Acad. Sci. Unit. States Am. 109 (2012), 14930–14935.
17. Devasagayam, T., Tilak, J., Boloor, K., Sane, K.S., Ghaskadbi, S.S., Lele, R., Free radicals and antioxidants in human health: current status and future prospects. Japi 52 (2004), 794–804.
18. Dodds, E., Lawson, W., Synthetic estrogenic agents without the phenanthrene nucleus. Nature, 137, 1936, 996.
19. Eladak, S., Grisin, T., Moison, D., Guerquin, M.-J., N'Tumba-Byn, T., Pozzi-Gaudin, S., Benachi, A., Livera, G., Rouiller-Fabre, V., Habert, R., A new chapter in the bisphenol A story: bisphenol S and bisphenol F are not safe alternatives to this compound. Fertil. Steril. 103 (2015), 11–21.
20. Feng, Y., Jiao, Z., Shi, J., Li, M., Guo, Q., Shao, B., Effects of bisphenol analogues on steroidogenic gene expression and hormone synthesis in H295R cells. Chemosphere 147 (2016), 9–19.
21. Feng, Y., Yin, J., Jiao, Z., Shi, J., Li, M., Shao, B., Bisphenol AF may cause testosterone reduction by directly affecting testis function in adult male rats. Toxicol. Lett. 211 (2012), 201–209.
22. Fic, A., Žegura, B., Sollner Dolenc, M., Filipič, M., Peterlin Mašič, L., Mutagenicity and DNA damage of bisphenol A and its structural analogues in HepG2 cells. Arh. Hig. Rada. Toksikol. 64 (2013), 189–200.
23. Gallart-Ayala, H., Moyano, E., Galceran, M., Fast liquid chromatography–tandem mass spectrometry for the analysis of bisphenol A-diglycidyl ether, bisphenol F-diglycidyl ether and their derivatives in canned food and beverages. J. Chromatogr. A 1218 (2011), 1603–1610.
24. García, M.M.S., Acquier, A., Suarez, G., Gomez, N.V., Gorostizaga, A., Mendez, C.F., Paz, C., Cisplatin inhibits testosterone synthesis by a mechanism that includes the action of reactive oxygen species (ROS) at the level of P450scc. Chem. Biol. Interact. 199 (2012), 185–191.
25. Glausiusz, J., The plastics puzzle. Nature, 508, 2014, 306.
26. Grignard, E., Lapenna, S., Bremer, S., Weak estrogenic transcriptional activities of Bisphenol A and Bisphenol S. Toxicol. Vitro 26 (2012), 727–731.
27. Hayashi, I., Morishita, Y., Imai, K., Nakamura, M., Nakachi, K., Hayashi, T., High-throughput spectrophotometric assay of reactive oxygen species in serum. Mutat. Res. Genet. Toxicol. Environ. Mutagen 631 (2007), 55–61.
28. Huang, Y., Wong, C., Zheng, J., Bouwman, H., Barra, R., Wahlström, B., Neretin, L., Wong, M., Bisphenol A (BPA) in China: a review of sources, environmental levels, and potential human health impacts. Environ. Int. 42 (2012), 91–99.
29. Hulak, M., Gazo, I., Shaliutina, A., Linhartova, P., In vitro effects of bisphenol A on the quality parameters, oxidative stress, DNA integrity and adenosine triphosphate content in sterlet (Acipenser ruthenus) spermatozoa. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 158 (2013), 64–71.
30. Ike, M., Chen, M., Danzl, E., Sei, K., Fujita, M., Biodegradation of a variety of bisphenols under aerobic and anaerobic conditions. Water Sci. Technol. 53 (2006), 153–159.
31. Iqbal, M., Sharma, S., Rezazadeh, H., Hasan, N., Abdulla, M., Athar, M., Glutathione metabolizing enzymes and oxidative stress in ferric nitrilotriacetate mediated hepatic injury. Redox Rep. 2 (1996), 385–391.
32. Jambor, T., Jana, B., Hana, G., Eva, T., Norbert, L., Male Reproduction: One of the Primary Targets of Bisphenol. Bisphenol A Exposure and Health Risks. 2017, InTech.
33. Jensen, E.C., Quantitative analysis of histological staining and fluorescence using ImageJ. Anat. Rec. 296 (2013), 378–381.
34. Ji, K., Hong, S., Kho, Y., Choi, K., Effects of bisphenol S exposure on endocrine functions and reproduction of zebrafish. Environ. Sci. Technol. 47 (2013), 8793–8800.
35. Kakkar, P., Das, B., Viswanathan, P., A Modified Spectrophotometric Assay of Superoxide Dismutase. 1984.
36. Kaul, N., Forman, H.J., 16 Reactive Oxygen Species in Physiology and Toxicology. Toxicology of the Human Environment: the Critical Role of Free Radicals. 2000, 311.
37. Kinch, C.D., Ibhazehiebo, K., Jeong, J.-H., Habibi, H.R., Kurrasch, D.M., Low-dose exposure to bisphenol A and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish. Proc. Natl. Acad. Sci. Unit. States Am. 112 (2015), 1475–1480.
38. Kitamura, S., Suzuki, T., Sanoh, S., Kohta, R., Jinno, N., Sugihara, K., Yoshihara, S.i., Fujimoto, N., Watanabe, H., Ohta, S., Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol. Sci. 84 (2005), 249–259.
39. Korkmaz, A., Ahbab, M.A., Kolankaya, D., Barlas, N., Influence of vitamin C on bisphenol A, nonylphenol and octylphenol induced oxidative damages in liver of male rats. Food Chem. Toxicol. 48 (2010), 2865–2871.
40. Kuiper, G.G., Lemmen, J.G., Carlsson, B., Corton, J.C., Safe, S.H., Van Der Saag, P.T., Van Der Burg, B., Gustafsson, J.-A.k., Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139 (1998), 4252–4263.
41. Lee, H.J., Chattopadhyay, S., Gong, E.-Y., Ahn, R.S., Lee, K., Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol. Sci. 75 (2003), 40–46.
42. Lee, J., Park, N.-Y., Kho, Y., Ji, K., Effects of 4-hydroxyphenyl 4-isoprooxyphenylsulfone (BPSIP) exposure on reproduction and endocrine system of zebrafish. Environ. Sci. Technol. 52 (2018), 1506–1513.
43. Lee, S., Liu, X., Takeda, S., Choi, K., Genotoxic potentials and related mechanisms of bisphenol A and other bisphenol compounds: a comparison study employing chicken DT40 cells. Chemosphere 93 (2013), 434–440.
44. Li, G., Chang, H., Xia, W., Mao, Z., Li, Y., Xu, S., F0 maternal BPA exposure induced glucose intolerance of F2 generation through DNA methylation change in Gck. Toxicol. Lett. 228 (2014), 192–199.
45. Liao, C., Kannan, K., Concentrations and profiles of bisphenol A and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure. J. Agric. Food Chem. 61 (2013), 4655–4662.
46. Liao, C., Kannan, K., A survey of bisphenol A and other bisphenol analogues in foodstuffs from nine cities in China. Food Addit. Contam. 31 (2014), 319–329.
47. Liao, C., Liu, F., Guo, Y., Moon, H.-B., Nakata, H., Wu, Q., Kannan, K., Occurrence of eight bisphenol analogues in indoor dust from the United States and several Asian countries: implications for human exposure. Environ. Sci. Technol. 46 (2012), 9138–9145.
48. Liao, C., Liu, F., Kannan, K., Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol A residues. Environ. Sci. Technol. 46 (2012), 6515–6522.
49. Liao, C., Liu, F., Moon, H.-B., Yamashita, N., Yun, S., Kannan, K., Bisphenol analogues in sediments from industrialized areas in the United States, Japan, and Korea: spatial and temporal distributions. Environ. Sci. Technol. 46 (2012), 11558–11565.
50. Maćczak, A., Cyrkler, M., Bukowska, B., Michałowicz, J., Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study). Toxicol. Vitro 41 (2017), 143–149.
51. Manfo, F.P.T., Jubendradass, R., Nantia, E.A., Moundipa, P.F., Mathur, P.P., Adverse Effects of Bisphenol A on Male Reproductive Function. Reviews of Environmental Contamination and Toxicology, vol. 228, 2014, Springer, 57–82.
52. Michałowicz, J., Bisphenol A–sources, toxicity and biotransformation. Environ. Toxicol. Pharmacol. 37 (2014), 738–758.
53. Michałowicz, J., Duda, W., Phenols–Sources and toxicity. Pol. J. Environ. Stud., 16, 2007.
54. Michałowicz, J., Mokra, K., Bąk, A., Bisphenol A and its analogs induce morphological and biochemical alterations in human peripheral blood mononuclear cells (in vitro study). Toxicol. Vitro 29 (2015), 1464–1472.
55. Mokra, K., Kocia, M., Michałowicz, J., Bisphenol A and its analogs exhibit different apoptotic potential in peripheral blood mononuclear cells (in vitro study). Food Chem. Toxicol. 84 (2015), 79–88.
56. Molina-Molina, J.-M., Amaya, E., Grimaldi, M., Sáenz, J.-M., Real, M., Fernández, M.F., Balaguer, P., Olea, N., In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-A congeners and derivatives via nuclear receptors. Toxicol. Appl. Pharmacol. 272 (2013), 127–136.
57. Naderi, M., Wong, M.Y., Gholami, F., Developmental exposure of zebrafish (Danio rerio) to bisphenol-S impairs subsequent reproduction potential and hormonal balance in adults. Aquat. Toxicol. 148 (2014), 195–203.
58. Nunez, A., Kannan, K., Giesy, J., Fang, J., Clemens, L., Effects of bisphenol A on energy balance and accumulation in brown adipose tissue in rats. Chemosphere 42 (2001), 917–922.
59. Pandey, K.B., Rizvi, S.I., Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxidative Med. Cell. Longev. 3 (2010), 2–12.
60. Pérez, V.I., Bokov, A., Van Remmen, H., Mele, J., Ran, Q., Ikeno, Y., Richardson, A., Is the oxidative stress theory of aging dead?. Biochim. Biophys. Acta Gen. Subj. 1790 (2009), 1005–1014.
61. Radák, Z., Kaneko, T., Tahara, S., Nakamoto, H., Ohno, H., Sasvári, M., Nyakas, C., Goto, S., The effect of exercise training on oxidative damage of lipids, proteins, and DNA in rat skeletal muscle: evidence for beneficial outcomes. Free Radic. Biol. Med. 27 (1999), 69–74.
62. Rejitha, J., Karthiayini, K., Physiological effects of oxidative stress and antioxidant Supplementation. 23rd Swadeshi Science Congress, 2013.
63. Richter, C.A., Birnbaum, L.S., Farabollini, F., Newbold, R.R., Rubin, B.S., Talsness, C.E., Vandenbergh, J.G., Walser-Kuntz, D.R., vom Saal, F.S., In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24 (2007), 199–224.
64. Rochester, J.R., Bolden, A.L., Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ. Health Perspect., 123, 2015, 643.
65. Rosenmai, A.K., Dybdahl, M., Pedersen, M., Alice van Vugt-Lussenburg, B.M., Wedebye, E.B., Taxvig, C., Vinggaard, A.M., Are structural analogues to bisphenol a safe alternatives?. Toxicol. Sci. 139 (2014), 35–47.
66. Rotroff, D.M., Dix, D.J., Houck, K.A., Knudsen, T.B., Martin, M.T., McLaurin, K.W., Reif, D.M., Crofton, K.M., Singh, A.V., Xia, M., Using in vitro high throughput screening assays to identify potential endocrine-disrupting chemicals. Environ. Health Perspect., 121, 2013, 7.
67. Scippo, M.-L., Bisphenol A in our food: same toxicological studies but different risk assessment and risk management decisions around the world. Food Sci. Law 5 (2011), 5–9.
68. Ullah, H., Jahan, S., Ain, Q.U., Shaheen, G., Ahsan, N., Effect of bisphenol S exposure on male reproductive system of rats: a histological and biochemical study. Chemosphere 152 (2016), 383–391.
69. Usman, A., Ahmad, M., From BPA to its analogues: is it a safe journey?. Chemosphere 158 (2016), 131–142.
70. Van Landuyt, K., Nawrot, T., Geebelen, B., De Munck, J., Snauwaert, J., Yoshihara, K., Scheers, H., Godderis, L., Hoet, P., Van Meerbeek, B., How much do resin-based dental materials release? A meta-analytical approach. Dent. Mater. 27 (2011), 723–747.
71. Wetherill, Y.B., Akingbemi, B.T., Kanno, J., McLachlan, J.A., Nadal, A., Sonnenschein, C., Watson, C.S., Zoeller, R.T., Belcher, S.M., In vitro molecular mechanisms of bisphenol A action. Reprod. Toxicol. 24 (2007), 178–198.
72. Zhan, M., Yang, X., Xian, Q., Kong, L., Photosensitized degradation of bisphenol A involving reactive oxygen species in the presence of humic substances. Chemosphere 63 (2006), 378–386.
73. Zou, Y., Lin, S., Chen, S., Zhang, H., Determination of bisphenol A diglycidyl ether, novolac glycidyl ether and their derivatives migrated from can coatings into foodstuff by UPLC-MS/MS. Eur. Food Res. Technol. 235 (2012), 231–244.