Biotransformation of bisphenol AF to its major glucuronide metabolite reduces estrogenic activity

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Li, Ming ^a   Yang, Yunjia ^a,b   Yang, Yi ^a   Yin, Jie ^a   Zhang, Jing ^a   Feng, Yixing ^a   Shao, Bing ^a,b  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' HEXAFLUOROISOPROPYLIDENE 2 DIPHENOL; 4,4' HEXAFLUOROISOPROPYLIDENE 2 DIPHENOL DIGLUCURONIDE; 4,4' HEXAFLUOROISOPROPYLIDENE 2 DIPHENOL GLUCORONIDE; 4,4' HEXAFLUOROISOPROPYLIDENE 2 DIPHENOL GLUCURONIDE DEHYDRATED; 4,4' HEXAFLUOROISOPROPYLIDENE 2 DIPHENOL SULFATE; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1A1; GLUCURONOSYLTRANSFERASE 1A3; GLUCURONOSYLTRANSFERASE 1A8; GLUCURONOSYLTRANSFERASE 1A9; GLUCURONOSYLTRANSFERASE 2B15; GLUCURONOSYLTRANSFERASE 2B17; GLUCURONOSYLTRANSFERASE 2B4; GLUCURONOSYLTRANSFERASE 2B7; PHENOL DERIVATIVE; UNCLASSIFIED DRUG; 4,4'-HEXAFLUORISOPROPYLIDENE DIPHENOL; BENZHYDRYL DERIVATIVE; ENDOCRINE DISRUPTOR; GLUCURONIDE;

ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL FUNCTIONS; BIOTRANSFORMATION; CANCER CELL; CELL PROLIFERATION; CELL STRAIN T47D; CONCENTRATION RESPONSE; CONTROLLED STUDY; CTSD GENE; ELECTROSPRAY MASS SPECTROMETRY; ESTROGEN ACTIVITY; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; ESTROGEN RESPONSIVE ELEMENT; FRAGMENTATION REACTION; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLUCURONIDATION; GREB1 GENE; HOST RESISTANCE; HYDROXYLATION; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; LIVER MICROSOME; MALE; MCF7 CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; RAT; TFF1 GENE; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; DRUG EFFECTS; FEMALE; HUMAN; METABOLISM; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ANIMALS; BENZHYDRYL COMPOUNDS; BIOTRANSFORMATION; CELL LINE, TUMOR; ENDOCRINE DISRUPTORS; FEMALE; GLUCURONIDES; HUMANS; MALE; MICROSOMES, LIVER; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84892556173     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083170     Document Type: Article

References (44)

1. National Toxicology Program (NTP) (2008). Available: http://ntp.niehs. nih.gov/ntp/htdocs/Chem-Background/ExSumPdf/BisphenolAF-093008-508.pdf#search= BisphenolAF. Accessed 10 July 2013
2. LaFleur AD, Schug KA (2011) A review of separation methods for the determination of estrogens and plastics-derived estrogen mimics from aqueous systems. Anal Chim Acta 696 (1): 6-26. PubMed: 21621029.
3. Song S, Ruan T, Wang T, Liu R, Jiang G (2012) Distribution and preliminary exposure assessment of Bisphenol AF (BPAF) in various environmental matrices around a manufacturing plant in China. Environ Sci Technol 46: 13136-13143. doi:10.1021/es303960k. PubMed: 23151244.
4. Matsushima A, Liu X, Okada H, Shimohigashi M, Shimohigashi Y (2010) Bisphenol AF is a full agonist for the estrogen receptor ERalpha but a highly specific antagonist for ERbeta. Environ Health Perspect 118 (9): 1267-1272. doi:10.1289/ehp.0901819. PubMed: 20427257.
5. Li Y, Luh CJ, Burns KA, Arao Y, Jiang Z et al. (2013) Endocrine-Disrupting Chemicals (EDCs): In Vitro Mechanism of Estrogenic Activation and Differential Effects on ER Target Genes. Environ Health Perspect 121 (4): 459-466. PubMed: 23384675.
6. Li Y, Burns KA, Arao Y, Luh CJ, Korach KS (2012) Differential estrogenic actions of endocrine-disrupting chemicals bisphenol A, bisphenol AF, and zearalenone through estrogen receptor alpha and beta in vitro. Environ Health Perspect 120 (7): 1029-1035. doi:10.1289/ehp.1104689. PubMed: 22494775.
7. Sui Y, Ai N, Park SH, Rios-Pilier J, Perkins JT et al. (2012) Bisphenol A and its analogues activate human pregnane X receptor. Environ Health Perspect 120 (3): 399-405. doi:10.1289/ehp.1104426. PubMed: 22214767.
8. Feng Y, Yin J, Jiao Z, Shi J, Li M et al. (2012) Bisphenol AF may cause testosterone reduction by directly affecting testis function in adult male rats. Toxicol Lett 211 (2): 201-209. doi:10.1016/j.toxlet.2012.03.802. PubMed: 22504055.
9. Ritter JK (2000) Roles of glucuronidation and UDP- glucuronosyltransferases in xenobiotic bioactivation reactions. Chem Biol Interact 129 (1-2): 171-193. doi:10.1016/S0009-2797(00)00198-8. PubMed: 11154740.
10. Sneitz N, Krishnan K, Covey DF, Finel M (2011) Glucuronidation of the steroid enantiomers ent-17beta-estradiol, ent-androsterone and entetiocholanolone by the human UDP-glucuronosyltransferases. J Steroid Biochem Mol Biology 127 (3-5): 282-288. doi:10.1016/j.jsbmb.2011.08.008.
11. Doerge DR, Twaddle NC, Woodling KA, Fisher JW (2010) Pharmacokinetics of bisphenol A in neonatal and adult rhesus monkeys. Toxicol Appl Pharmacol 248 (1): 1-11. doi:10.1016/j.taap.2010.07.009. PubMed: 20655935.
12. Kang JH, Katayama Y, Kondo F (2006) Biodegradation or metabolism of bisphenol A: from microorganisms to mammals. Toxicology 217 (2): 81-90.
13. Pottenger LH, Domoradzki JY, Markham DA, Hansen SC, Cagen SZ et al. (2000) The relative bioavailability and metabolism of bisphenol A in rats is dependent upon the route of administration. Toxicol Sci 54 (1): 3-18. doi:10.1093/toxsci/54.1.3. PubMed: 10746927.
14. Yokota H, Iwano H, Endo M, Kobayashi T, Inoue H et al. (1999) Glucuronidation of the environmental oestrogen bisphenol A by an isoform of UDP-glucuronosyltransferase, UGT2B1, in the rat liver. Biochem J 340 (2): 405-409. doi:10.1042/0264-6021:3400405. PubMed: 10333482.
15. Yoshihara S, Makishima M, Suzuki N, Ohta S (2001) Metabolic activation of bisphenol A by rat liver S9 fraction. Toxicol Sci 62 (2): 221-227. doi:10.1093/toxsci/62.2.221. PubMed: 11452134.
16. Niwa T, Fujimoto M, Kishimoto K, Yabusaki Y, Ishibashi F et al. (2001) Metabolism and interaction of bisphenol A in human hepatic cytochrome P450 and steroidogenic CYP17. Biol Pharm Bull 24 (9): 1064-1067. doi:10.1248/bpb.24.1064. PubMed: 11558570.
17. Yoshihara Si Mizutare T, Makishima M, Suzuki N, Fujimoto N et al. (2004) Potent estrogenic metabolites of bisphenol A and bisphenol B formed by rat liver S9 fraction: their structures and estrogenic potency. Toxicol Sci 78 (1): 50-59. doi:10.1093/toxsci/kfh047. PubMed: 14691209.
18. Schmidt J, Kotnik P, Trontelj J, Knez Z, Mašič LP (2013) Bioactivation of bisphenol A and its analogs (BPF, BPAF, BPZ and DMBPA) in human liver microsomes. Toxicology in Vitro 27 (4): 1267-1276. doi:10.1016/j.tiv. 2013.02.016. PubMed: 23470418.
19. Arewång CJ, Lahmann M, Oscarson S, Tidén AK (2007) Synthesis of urine drug metabolites: glucuronic acid glycosides of phenol intermediates. Carbohydr Res 342 (7): 970-974. doi:10.1016/j.carres.2007.01.014. PubMed: 17324385.
20. Hayasaka T, Katsuhara Y, Kume T, Yamazaki T (2011) HF-mediated equilibrium between fluorinated ketones and the corresponding α-fluoroalcohols. Tetrahedron 67 (12): 2215-2219. doi:10.1016/j.tet.2011. 01.087.
21. Tang L, Ye L, Singh R, Wu B, Lv C et al. (2010) Use of glucuronidation fingerprinting to describe and predict mono-and dihydroxyflavone metabolism by recombinant UGT isoforms and human intestinal and liver microsomes. Mol Pharmaceutics 7 (3): 664-679. doi:10.1021/mp900223c.
22. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38 (11): 1289-1297. doi:10.1038/ng1901. PubMed: 17013392.
23. Deschênes J, Bourdeau V, White JH, Mader S (2007) Regulation of GREB1 transcription by estrogen receptor α through a multipartite enhancer spread over 20 kb of upstream flanking sequences. J Biol Chem 282 (24): 17335-17339. doi:10.1074/jbc.C700030200. PubMed: 17463000.
24. Lee S, Kim YK, Shin T-Y, Kim S-H (2013) Neurotoxic Effects of Bisphenol AF on Calcium-Induced ROS and MAPKs. Neurotox Res 23 (3): 249-259. PubMed: 22996013.
25. Doerge DR, Twaddle NC, Vanlandingham M, Brown RP, Fisher JW (2011) Distribution of bisphenol A into tissues of adult, neonatal, and fetal Sprague-Dawley rats. Toxicol Appl Pharmacol 255 (3): 261-270. doi:10.1016/j.taap.2011.07.009. PubMed: 21820460.
26. Fisher JW, Twaddle NC, Vanlandingham M, Doerge DR (2011) Pharmacokinetic modeling: prediction and evaluation of route dependent dosimetry of bisphenol A in monkeys with extrapolation to humans. Toxicol Appl Pharmacol 257 (1): 122-136. doi:10.1016/j.taap.2011.08.026. PubMed: 21920375.
27. Upmeier A, Degen GH, Diel P, Michna H, Bolt HM (2000) Toxicokinetics of bisphenol A in female DA/Han rats after a single i.v. and oral administration. Arch Toxicol 74 (8): 431-436. doi:10.1007/s002040000144. PubMed: 11097379.
28. Elsby R, Maggs JL, Ashby J, Park BK (2001) Comparison of the modulatory effects of human and rat liver microsomal metabolism on the estrogenicity of bisphenol A: implications for extrapolation to humans. J Pharmacol Exp Ther 297 (1): 103-113. PubMed: 11259533.
29. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM (2009) Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 30 (1): 75-95. PubMed: 19074586.
30. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A (2006) The estrogenic effect of bisphenol A disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environ Health Perspect 114 (1): 106-112. PubMed: 16393666.
31. Ben-Jonathan N, Steinmetz R (1998) Xenoestrogens: the emerging story of bisphenol A. Trends Endocrinol Metab 9 (3): 124-128. doi:10.1016/S1043-2760(98) 00029-0. PubMed: 18406253.
32. Davis DL, Webster P, Stainthorpe H, Chilton J, Jones L et al. (2007) Declines in sex ratio at birth and fetal deaths in Japan, and in US whites but not African Americans. Environ Health Perspect 115 (6): 941-946. doi:10.1289/ehp.9540. PubMed: 17589604.
33. Nadal A, Alonso-Magdalena P, Soriano S, Quesada I, Ropero AB (2009) The pancreatic β-cell as a target of estrogens and xenoestrogens: Implications for blood glucose homeostasis and diabetes. Mol Cell Endocrinol 304 (1): 63-68.
34. Ohno S, Nakajin S (2009) Determination of mRNA expression of human UDP-glucuronosyltransferases and application for localization in various human tissues by real-time reverse transcriptase-polymerase chain reaction. Drug Metab Dispos 37 (1): 32-40. doi:10.1124/dmd.108.023598. PubMed: 18838504.
35. King CD, Rios GR, Assouline JA, Tephly TR (1999) Expression of UDP-glucuronosyltransferases (UGTs) 2B7 and 1A6 in the human brain and identification of 5-hydroxytryptamine as a substrate. Arch Biochem Biophys 365 (1): 156-162. doi:10.1006/abbi.1999.1155. PubMed: 10222050.
36. Mercado-Feliciano M, Bigsby RM (2008) Hydroxylated metabolites of the polybrominated diphenyl ether mixture DE-71 are weak estrogen receptor-α ligands. Environ Health Perspect 116 (10): 1315-1321. doi:10.1289/ehp.11343. PubMed: 18941571.
37. Safe SH (1997) Xenoestrogens and breast cancer. N Engl J Med 337 (18): 1303-1304. doi:10.1056/NEJM199710303371809. PubMed: 9345081.
38. Soto AM, Vandenberg LN, Maffini MV, Sonnenschein C (2008) Does breast cancer start in the womb? Basic Clin Pharmacol Toxicol 102 (2): 125-133. doi:10.1111/j.1742-7843.2007.00165.x. PubMed: 18226065.
39. Weber Lozada K, Keri RA (2011) Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol Reprod 85 (3): 490-497. doi:10.1095/biolreprod.110.090431. PubMed: 21636739.
40. Keri RA, Ho S-M, Hunt PA, Knudsen KE, Soto AM et al. (2007) An evaluation of evidence for the carcinogenic activity of bisphenol A. Reprod Toxicol 24 (2): 240-252. doi:10.1016/j.reprotox.2007.06.008. PubMed: 17706921.
41. Diel P, Olff S, Schmidt S, Michna H (2002) Effects of the environmental estrogens bisphenol A, o,p′-DDT, p-tert-octylphenol and coumestrol on apoptosis induction, cell proliferation and the expression of estrogen sensitive molecular parameters in the human breast cancer cell line MCF-7. J Steroid Biochem Mol Biology 80 (1): 61-70. doi:10.1016/S0960-0760(01)00173-X.
42. Olsen CM, Meussen-Elholm ET, Samuelsen M, Holme JA, Hongslo JK (2003) Effects of the environmental oestrogens bisphenol A, tetrachlorobisphenol A, tetrabromobisphenol A, 4-hydroxybiphenyl and 4, 4′-dihydroxybiphenyl on oestrogen receptor binding, cell proliferation and regulation of oestrogen sensitive proteins in the human breast cancer cell line MCF7. Pharmacol Toxicol 92 (4): 180-188. doi:10.1034/j.1600-0773.2003.920408.x. PubMed: 12753421.
43. Dairkee SH, Seok J, Champion S, Sayeed A, Mindrinos M et al. (2008) Bisphenol A induces a profile of tumor aggressiveness in high-risk cells from breast cancer patients. Cancer Res 68 (7): 2076-2080. doi:10.1158/0008-5472.CAN- 07-6526. PubMed: 18381411.
44. Kitamura S, Suzuki T, Sanoh S, Kohta R, Jinno N et al. (2005) Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol Sci 84 (2): 249-259. doi:10.1093/toxsci/kfi074. PubMed: 15635150.