Inverse antagonist activities of parabens on human oestrogen-related receptor γ (ERRγ): In vitro and in silico studies

Toxicology and Applied Pharmacology

Volumn 270, Issue 1, 2013, Pages 16-22

  Zhang, Zhaobin ^a   Sun, Libei ^a   Hu, Ying ^a   Jiao, Jian ^a   Hu, Jianying ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

Breast cancer; Endocrine disrupting chemicals; Ethylparaben; Methylparaben; Oestrogen related receptor ; Parabens

Indexed keywords

4 HYDROXYBENZOIC ACID ESTER; ARGININE; BENZOIC ACID DERIVATIVE; BENZYL PARABEN; BIOLOGICAL MARKER; BUTYL PARABEN; ESTROGEN RELATED RECEPTOR GAMMA; ETHYL PARABEN; GLUTAMIC ACID; METHYL PARABEN; NUCLEAR RECEPTOR COACTIVATOR; PROPYL PARABEN; SALICYLIC ACID DERIVATIVE; STEROID RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BREAST CANCER; BREAST CARCINOGENESIS; COMPUTER MODEL; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROGEN BOND; IN VITRO STUDY; MOLECULAR DOCKING; PROTEIN EXPRESSION; RECEPTOR BINDING;

COMPUTER SIMULATION; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; PARABENS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, ESTROGEN;

EID: 84877073515     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.03.030     Document Type: Article

References (47)

1. Abad M.C., Askari H., O'Neill J., Klinger A.L., Milligan C., Lewandowski F., Springer B., Spurlino J., Rentzeperis D. Structural determination of estrogen-related receptor gamma in the presence of phenol derivative compounds. J. Steroid Biochem. Mol. Biol. 2008, 108:44-54.
2. Ariazi E.A., Clark G.M., Mertz J.E. Estrogen-related receptor alpha and estrogen-related receptor gamma associate with unfavorable and favorable biomarkers, respectively, in human breast cancer. Cancer Res. 2002, 62:6510-6518.
3. Barr L., Metaxas G., Harbach C.A.J., Savoy L.A., Darbre P.D. Measurement of paraben concentrations in human breast tissue at serial locations across the breast from axilla to sternum. J. Appl. Toxicol. 2012, 32:219-232.
4. Calafat A.M., Ye X., Wong L.Y., Bishop A.M., Needham L.L. Urinary concentrations of four parabens in the U.S. population: NHANES 2005-2006. Environ. Health Perspect. 2010, 118:679-685.
5. Casas L., Fernandez M.F., Llop S., Guxens M., Ballester F., Olea N., Irurzun M.B., Rodriguez L.S.M., Riano I., Tardon A., Vrijheid M., Calafat A.M., Sunyer J. Urinary concentrations of phthalates and phenols in a population of Spanish pregnant women and children. Environ. Int. 2011, 37:858-866.
6. Charles A.K., Darbre P.D. Combinations of parabens at concentrations measured in human breast tissue can increase proliferation of MCF-7 human breast cancer cells. J. Appl. Toxicol 2013, 10.1002/jat.2850.
7. Chen J., Ahn K.C., Gee N.A., Gee S.J., Hammock B.D., Lasley B.L. Antiandrogenic properties of parabens and other phenolic containing small molecules in personal care products. Toxicol. Appl. Pharmacol. 2007, 221:278-284.
8. Coward P., Lee D., Hull M.V., Lehmann J.M. 4-Hydroxytamoxifen binds to and deactivates the estrogen-related receptor gamma. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8880-8884.
9. Daniel J.W. Metabolic aspects of antioxidants and preservatives. Xenobiotica 1986, 16:1073-1078.
10. Darbre P.D., Harvey P.W. Paraben esters: review of recent studies of endocrine toxicity, absorption, esterase and human exposure, and discussion of potential human health risks. J. Appl. Toxicol. 2008, 28:561-578.
11. Darbre P.D., Aljarrah A., Miller W.R., Coldham N.G., Sauer M.J., Pope G.S. Concentrations of parabens in human breast tumours. J. Appl. Toxicol. 2004, 24:5-13.
12. Elder R.L. Final report on the safety assessment of methylparaben, ethylparaben, propylparaben and butylparaben. J. Am. Coll. Toxicol. 1984, 3:147-209.
13. Eudy J., Yao S., Weston M., Ma-Edmonds M., Talmadge C., Cheng J., Kimberling W., Sumegi J. Isolation of a gene encoding a novel member of the nuclear receptor superfamily from the critical region of Usher syndrome type IIa at 1q41. Genomics 1998, 50:382-384.
14. Frederiksen H., Jorgensen N., Andersson A.M. Parabens in urine, serum and seminal plasma from healthy Danish men determined by liquid chromatography-tandem mass spectrometry (LC-MS/MS). J. Expo. Sci. Environ. Epidemiol. 2011, 21:262-271.
15. Frye C.A., Bo E., Calamandrei G., Calza L., Dessi-Fulgheri F., Fernandez M., Fusani L., Kah O., Kajta M., Le Page Y., Patisaul H.B., Venerosi A., Wojtowicz A.K., Panzica G.C. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J. Neuroendocrinol. 2012, 24:144-159.
16. Giguere V. To ERR in the estrogen pathway. Trends Endocrinol. Metab. 2002, 13:220-225.
17. Golden R., Gandy J. Letter to the editor. J. Appl. Toxicol. 2004, 24:297-299. ([Reply Darbre, P.D., Pope, G.S., Aljarrah, A., Miller, W.R., Coldham, N.G., Sauer, M.J., 2004. J. Appl. Toxicol. 24, 299-301.]).
18. Golden R., Gandy J., Vollmer G. A review of the endocrine activity of parabens and implications for potential risks to human health. Crit. Rev. Toxicol. 2005, 35:435-458.
19. Heard D.J., Norby P.L., Holloway J., Vissing H. Human ERRγ, a third member of the estrogen receptor-related receptor (ERR) subfamily of orphan nuclear receptors: tissue-specific isoforms are expressed during development and in the adult. Mol. Endocrinol. 2000, 14:382-392.
20. Hong H., Yang L., Stallcup M.R. Hormone-independent transcriptional activation and coactivator binding by novel orphan nuclear receptor ERR3. J. Biol. Chem. 1999, 274:22618-22626.
21. Ijichi N., Shigekawa T., Ikeda K., Horie-Inoue K., Fujimura T., Tsuda H., Osaki A., Saeki T., Inoue S. Estrogen-related receptor γ modulates cell proliferation and estrogen signaling in breast cancer. J. Steroid Biochem. Mol. Biol. 2011, 123:1-7.
22. JECFA 17th report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organization Technical Report Series 1974, 539.
23. Kanayama T., Mamiya S., Nishihara T., Nishikawa J. Basis of a high through put method for nuclear receptor ligands. J. Biochem. 2003, 133:791-797.
24. Lorke D.E., Susens U., Borgmeyer U., Hermans-Borgmeyer I. Differential expression of the estrogen receptor-related receptor gamma in the mouse brain. Mol. Brain Res. 2000, 77:277-280.
25. Matsushima A., Teramoto T., Okada H., Liu X., Tokunaga T., Kakuta Y., Shimohigashi Y. ERRgamma tethers strongly bisphenol A and 4-alpha-cumylphenol in an induced-fit manner. Biochem. Biophys. Res. Commun. 2008, 373:408-413.
26. Meeker J.D., Yang T., Ye X., Calafat A.M., Hauser R. Urinary concentrations of parabens and serum hormone levels, semen quality parameters, and sperm DNA damage. Environ. Health Perspect. 2011, 119:252-257.
27. Miller W.R. Estrogen and Breast Cancer 1996, Chapman and Hall, London.
28. Oishi S. Effects of butylparaben on the male reproductive system in rats. Toxicol. Ind. Health 2001, 17:31-39.
29. Oishi S. Effects of propylparaben on the male reproductive system. Food Chem. Toxicol. 2002, 40:1807-1813.
30. Oishi S. Effects of butylparaben on the male reproductive system in mice. Arch. Toxicol. 2002, 76:423-429.
31. Okada H., Tokunaga T., Liu X.H., Takayanagi S., Matsushima A., Shimohigashi Y. Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma. Environ. Health Perspect. 2008, 116:32-38.
32. Pugazhendhi D., Sadler A.J., Darbre P.D. Comparison of the global gene expression profiles produced by methylparaben, butylparaben and 17β-oestradiol in MCF7 human breast cancer cells. J. Appl. Toxicol. 2007, 27:67-77.
33. Rastogi S.C., Schouten A., De Kruijf N., Weijland J.W. Contents of methyl-, ethyl-, propyl-, butyl- and benzylparaben in cosmetic products. Contact Dermatitis 1995, 32:28-30.
34. Routledge E.J., Parker J., Odum J., Ashby J., Sumpter J.P. Some alkyl hydroxyl benzoate preservatives (parabens) are estrogenic. Toxicol. Appl. Pharmacol. 1998, 153:12-19.
35. Sandanger T.M., Huber S., Moe M.K., Braathen T., Leknes H., Lund E. Plasma concentrations of parabens in postmenopausal women and self-reported use of personal care products: the NOWAC postgenome study. J. Exp. Sci. Environ. Epidemiol. 2011, 21:595-600.
36. Satoh K., Nonaka R., Ohyama K., Nagai K. Androgenic and antiandrogenic effects of alkylphenols and parabens assessed using the reporter gene assay with stably transfected CHO-K1 cells (AR-Eco-Screen System). J. Health Sci. 2005, 51:557-568.
37. Smith K.W., Braun J.M., Williams P.L., Ehrlich S., Correia K.F., Calafat A.M., Ye X., Ford J., Keller M., Meeker J.D., Hauser R. Predictors and variability of urinary paraben concentrations in men and women, including before and during pregnancy. Environ. Health Perspect. 2012, 120:1538-1543.
38. Soni M.G., Carabin I.G., Burdock G.A. Safety assessment of esters of p-hydroxybenzoic acid (parabens). Food Chem. Toxicol. 2005, 43:985-1015.
39. Suetsugi M., Su L., Karlsberg K., Yuan Y.C., Chen S. Flavone and isoflavone phytoestrogens are agonists of estrogen-related receptors. Mol. Cancer Res. 2003, 1:981-991.
40. Takayanagi S., Tokunaga T., Liu X.H., Okada H., Matsushima A., Shimohigashi Y. Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERR gamma) with high constitutive activity. Toxicol. Lett. 2006, 167:95-105.
41. Terasaka S., Inoue A., Tanji M., Kiyama R. Expression profiling of estrogen-responsive genes in breast cancer cells treated with alkylphenols, chlorinated phenols, parabens, or bis- and benzoylphenols for evaluation of estrogenic activity. Toxicol. Lett. 2006, 163:130-141.
42. Wang L.P., Zuercher W.J., Consler T.G., Lambert M.H., Miller A.B., Orband-Miller L.A., McKee D.D., Willson T.M., Nolte R.T. X-ray crystal structures of the estrogen-related receptor-gamma ligand binding domain in three functional states reveal the molecular basis of small molecule regulation. J. Biol. Chem. 2006, 281:37773-37781.
43. Xie W., Hong H., Yang N.N., Lin R.J., Simon C.M., Stallcup M.R., Evans R.M. Constitutive activation of transcription and binding of coactivator by estrogen related receptors 1 and 2. Mol. Endocrinol. 1999, 13:2151-2162.
44. Yamamoto T., Mori T., Sawada M., Kuroboshi H., Tatsumi H., Yoshioka T., Matsushima H., Iwasaku K., Kitawaki J. Estrogen-related receptor-gamma regulates estrogen receptor-alpha responsiveness in uterine endometrial cancer. Int. J. Gynecol. Cancer 2012, 22:1509-1516.
45. Ye X., Tao L.J., Needham L.L., Calafat A.M. Automated on-line column-switching HPLCMS/MS method for measuring environmental phenols and parabens in serum. Talanta 2008, 76:865-871.
46. Ye X., Wong L.Y., Jia L.T., Needham L.L., Calafat A.M. Stability of the conjugated species of environmental phenols and parabens in human serum. Environ. Int. 2009, 35:1160-1163.
47. Zhang Z.B., Jia C.X., Hu Y., Sun L.B., Jiao J., Zhao L., Zhu D.S., Li J., Tian Y.L., Bai H.C., Li R.B., Hu J.Y. The estrogenic potential of salicylate esters and their possible risks in foods and cosmetics. Toxicol. Lett. 2012, 209:146-153.