In vitro and in silico assessment of the structure-dependent binding of bisphenol analogues to glucocorticoid receptor

Analytical and Bioanalytical Chemistry

Volumn 409, Issue 8, 2017, Pages 2239-2246

  Zhang, Jie ^a   Zhang, Tiehua ^b   Guan, Tianzhu ^b   Yu, Hansong ^a   Li, Tiezhu ^a  

^a JILIN AGRICULTURAL UNIVERSITY   (China)

^b JILIN UNIVERSITY   (China)

Author keywords

Bisphenol analogues; Fluorescence polarization; Glucocorticoid receptor; Molecular docking

Indexed keywords

BINS; ENDOCRINE DISRUPTERS; ENDOCRINOLOGY; FLUORESCENCE; HORMONES; MOLECULAR DYNAMICS; MOLECULAR MODELING; PHENOLS; POLARIZATION; RECOMBINANT PROTEINS;

BISPHENOLS; ENDOCRINE DISRUPTING COMPOUND; ENVIRONMENTALLY BENIGN; FLUORESCENCE POLARIZATION; GLUCOCORTICOID RECEPTOR; MOLECULAR DOCKING; MOLECULAR DYNAMICS SIMULATIONS; STRUCTURAL VARIATIONS;

BINDING ENERGY;

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; GLUCOCORTICOID RECEPTOR; PHENOL DERIVATIVE;

COMPUTER SIMULATION; FLUORESCENCE POLARIZATION; IN VITRO STUDY; METABOLISM; MOLECULAR DOCKING; MOLECULAR DYNAMICS;

BENZHYDRYL COMPOUNDS; COMPUTER SIMULATION; FLUORESCENCE POLARIZATION; IN VITRO TECHNIQUES; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; PHENOLS; RECEPTORS, GLUCOCORTICOID;

EID: 85009282307     PISSN: 16182642     EISSN: 16182650     Source Type: Journal    
DOI: 10.1007/s00216-016-0168-7     Document Type: Article

References (47)

1. Stossi F, Bolt Michael J, Ashcroft Felicity J, Lamerdin Jane E, Melnick Jonathan S, Powell Reid T, et al. Defining estrogenic mechanisms of bisphenol A analogs through high throughput microscopy-based contextual assays. J Biol Chem. 2014;21(6):743–53. doi:10.1016/j.chembiol.2014.03.013.
2. Staples CA, Dome PB, Klecka GM, Oblock ST, Harris LR. A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere. 1998;36(10):2149–73. doi:10.1016/S0045-6535(97)10133-3.
3. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect. 2010;118(8):1055–70. doi:10.1289/ehp.0901716.
4. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007;24(2):139–77. doi:10.1016/j.reprotox.2007.07.010.
5. Rubin BS. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011;127(1-2):27–34. doi:10.1016/j.jsbmb.2011.05.002.
6. Vogel SA. The politics of plastics: the making and unmaking of bisphenol a “safety”. Am J Public Health. 2009;99 Suppl 3:S559–66. doi:10.2105/ajph.2008.159228.
7. Jing P, Zhang X, Wu Z, Bao L, Xu Y, Liang C, et al. Electrochemical sensing of bisphenol A by graphene-1-butyl-3-methylimidazolium hexafluorophosphate modified electrode. Talanta. 2015;141:41–6. doi:10.1016/j.talanta.2015.03.042.
8. Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect. 2015;123(7):643–50. doi:10.1289/ehp.1408989.
9. Chen D, Kannan K, Tan H, Zheng Z, Feng Y-L, Wu Y, et al. Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity-a review. Environ Sci Technol. 2016;50(11):5438–53. doi:10.1021/acs.est.5b05387.
10. Usman A, Ahmad M. From BPA to its analogues: is it a safe journey? Chemosphere. 2016;158:131–42. doi:10.1016/j.chemosphere.2016.05.070.
11. Matthews JB, Twomey K, Zacharewski TR. In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors α and β. Chem Res Toxicol. 2001;14(2):149–57. doi:10.1021/tx0001833.
12. Takayanagi S, Tokunaga T, Liu X, Okada H, Matsushima A, Shimohigashi Y. Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor γ (ERRγ) with high constitutive activity. Toxicol Lett. 2006;167(2):95–105. doi:10.1016/j.toxlet.2006.08.012.
13. Riu A, Grimaldi M, le Maire A, Bey G, Phillips K, Boulahtouf A, et al. Peroxisome proliferator-activated receptor γ is a target for halogenated analogs of bisphenol A. Environ Health Perspect. 2011;119(9):1227–32. doi:10.1289/ehp.1003328.
14. Sui Y, Ai N, Park S-H, Rios-Pilier J, Perkins JT, Welsh WJ, et al. Bisphenol A and its analogues activate human pregnane X receptor. Environ Health Perspect. 2012;120(3):399–405. doi:10.1289/ehp.1104426.
15. Sargis RM, Johnson DN, Choudhury RA, Brady MJ. Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (Silver Spring, Md). 2010;18(7):1283–8. doi:10.1038/oby.2009.419.
16. Lee HJ, Chattopadhyay S, Gong E-Y, Ahn RS, Lee K. Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol Sci. 2003;75(1):40–6. doi:10.1093/toxsci/kfg150.
17. Zoeller RT, Bansal R, Parris C. Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology. 2005;146(2):607–12. doi:10.1210/en.2004-1018.
18. Liao C, Liu F, Moon HB, 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. 2012;46(21):11558–65. doi:10.1021/es303191g.
19. Song S, Song M, Zeng L, Wang T, Liu R, Ruan T, et al. Occurrence and profiles of bisphenol analogues in municipal sewage sludge in China. Environ Pollut. 2014;186:14–9. doi:10.1016/j.envpol.2013.11.023.
20. Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PKS, Moon H-B, et al. Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China. Korea India Ecotox Environ Saf. 2015;122:565–72. doi:10.1016/j.ecoenv.2015.09.029.
21. Zang X, Chang Q, Hou M, Wang C, Wang Z. Graphene grafted magnetic microspheres for solid phase extraction of bisphenol A and triclosan from water samples followed by gas chromatography-mass spectrometric analysis. Anal Methods. 2015;7(20):8793–800. doi:10.1039/c5ay01578b.
22. Li Y, Jiao Y, Guo Y, Yang Y. Determination of bisphenol-A, 2,4-dichlorophenol, bisphenol-AF and tetrabromobisphenol-A in liquid foods and their packaging materials by vortex-assisted supramolecular solvent microextraction/high-performance liquid chromatography. Anal Methods. 2013;5(19):5037. doi:10.1039/c3ay40586a.
23. Khedr A. Optimized extraction method for LC-MS determination of bisphenol A, melamine and di(2-ethylhexyl) phthalate in selected soft drinks, syringes, and milk powder. J Chromatogr B. 2013;930:98–103. doi:10.1016/j.jchromb.2013.04.040.
24. Inoue K, Murayama S, Takeba K, Yoshimura Y, Nakazawa H. Contamination of xenoestrogens bisphenol A and F in honey: safety assessment and analytical method of these compounds in honey. J Food Compos Anal. 2003;16(4):497–506. doi:10.1016/S0889-1575(03)00018-8.
25. D’Antuono A, Dall’Orto VC, Balbo AL, Sobral S, Rezzano I. Determination of bisphenol A in food-simulating liquids using LCED with a chemically modified electrode. J Agr Food Chem. 2001;49(3):1098–101. doi:10.1021/jf000660n.
26. Marchesini GR, Meulenberg E, Haasnoot W, Irth H. Biosensor immunoassays for the detection of bisphenol A. Anal Chim Acta. 2005;528(1):37–45. doi:10.1016/j.aca.2004.06.066.
27. Moreno MJ, D’Arienzo P, Manclus JJ, Montoya A. Development of monoclonal antibody-based immunoassays for the analysis of bisphenol A in canned vegetables. J Environ Sci Heal B. 2011;46(6):509–17. doi:10.1080/03601234.2011.583871.
28. Zhang J, Zhao S-Q, Zhang K, Zhou J-Q. Cd-doped ZnO quantum dots-based immunoassay for the quantitative determination of bisphenol A. Chemosphere. 2014;95:105–10. doi:10.1016/j.chemosphere.2013.08.039.
29. Kuruto-Niwa R, Tateoka Y, Usuki Y, Nozawa R. Measurement of bisphenol A concentrations in human colostrum. Chemosphere. 2007;66(6):1160–4. doi:10.1016/j.chemosphere.2006.06.073.
30. Bledsoe RK, Montana VG, Stanley TB, Delves CJ, Apolito CJ, McKee DD, et al. Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell. 2002;110(1):93–105. doi:10.1016/s0092-8674(02)00817-6.
31. Roelofs MJ, van den Berg M, Bovee TF, Piersma AH, van Duursen MB. Structural bisphenol analogues differentially target steroidogenesis in murine MA-10 Leydig cells as well as the glucocorticoid receptor. Toxicol. 2015;329:10–20. doi:10.1016/j.tox.2015.01.003.
32. Prasanth GK, Divya LM, Sadasivan C. Bisphenol-A can bind to human glucocorticoid receptor as an agonist: an in silico study. J Appl Toxicol. 2010;30(8):769–74. doi:10.1002/jat.1570.
33. Kroe RR, Baker MA, Brown MP, Farrow NA, Gautschi E, Hopkins JL, et al. Agonist versus antagonist induce distinct thermodynamic modes of co-factor binding to the glucocorticoid receptor. Biophys Chem. 2007;128(2-3):156–64. doi:10.1016/j.bpc.2007.03.013.
34. Simmons CA, Bledsoe RK, Guex N, Pearce KH. Expression, purification, and characterization of multiple, multifunctional human glucocorticoid receptor proteins. Protein Express Purif. 2008;62(1):29–35. doi:10.1016/j.pep.2008.07.008.
35. Roehrl MH, Wang JY, Wagner G. A general framework for development and data analysis of competitive high-throughput screens for small-molecule inhibitors of protein-protein interactions by fluorescence polarization. Biochemistry. 2004;43(51):16056–66. doi:10.1021/bi048233g.
36. Scherrer LC, Dalman FC, Massa E, Meshinchi S, Pratt WB. Structural and functional reconstitution of the glucocorticoid receptor-hsp90 complex. J Biol Chem. 1990;265(35):21397–400.
37. Pratt WB, Toft DO. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev. 1997;18(3):306–60. doi:10.1210/edrv.18.3.0303.
38. Kwon Y-U, Kodadek T. Quantitative comparison of the relative cell permeability of cyclic and linear peptides. Chem Biol. 2007;14(6):671–7. doi:10.1016/j.chembiol.2007.05.006.
39. Yu P, Liu B, Kodadek T. A convenient, high-throughput assay for measuring the relative cell permeability of synthetic compounds. Nat Protoc. 2007;2(1):23–30.
40. Kaya T, Mohr SC, Waxman DJ, Vajda S. Computational screening of phthalate monoesters for binding to PPARγ. Chem Res Toxicol. 2006;19(8):999–1009. doi:10.1021/tx050301s.
41. Zhang J, Xing X, Sun Y, Li Z, Xue P, Wang T, et al. Characterization of the binding between phthalate esters and mouse PPARα for the development of a fluorescence polarization-based competitive binding assay. Anal Methods. 2016;8(4):880–5. doi:10.1039/c5ay03053f.
42. Lind U, Greenidge P, Gillner M, Koehler KF, Wright A, Carlstedt-Duke J. Functional probing of the human glucocorticoid receptor steroid-interacting surface by site-directed mutagenesis. Gln-642 plays an important role in steroid recognition and binding. J Biol Chem. 2000;275(25):19041–9. doi:10.1074/jbc.M000228200.
43. Kauppi B, Jakob C, Farnegardh M, Yang J, Ahola H, Alarcon M, et al. The three-dimensional structures of antagonistic and agonistic forms of the glucocorticoid receptor ligand-binding domain: RU-486 induces a transconformation that leads to active antagonism. J Biol Chem. 2003;278(25):22748–54. doi:10.1074/jbc.M212711200.
44. Wang H, Aslanian R, Madison VS. Induced-fit docking of mometasone furoate and further evidence for glucocorticoid receptor 17α pocket flexibility. J Mol Graph Model. 2008;27(4):512–21. doi:10.1016/j.jmgm.2008.09.002.
45. Onnis V, Kinsella GK, Carta G, Fayne D, Lloyd DG. Rational structure-based drug design and optimization in the ligand-binding domain of the glucocorticoid receptor-α. Future Med Chem. 2009;1(2):345–59. doi:10.4155/fmc.09.21.
46. Veleiro AS, Alvarez LD, Eduardo SL, Burton G. Structure of the glucocorticoid receptor, a flexible protein that can adapt to different ligands. ChemMedChem. 2010;5(5):649–59. doi:10.1002/cmdc.201000014.
47. Zhuang S, Zhang C, Liu W. Atomic insights into distinct hormonal activities of bisphenol A analogues toward PPARγ and ERα receptors. Chem Res Toxicol. 2014;27(10):1769–79. doi:10.1021/tx500232b.