Potent inhibition of estrogen sulfotransferase by hydroxylated metabolites of polyhalogenated aromatic hydrocarbons reveals alternative mechanism for estrogenic activity of endocrine disrupters

Journal of Clinical Endocrinology and Metabolism

Volumn 87, Issue 3, 2002, Pages 1142-1150

  Kester, Monique H A ^a   Bulduk, Sema ^a   Van Toor, Hans ^a   Tibboel, Dick ^a   Meinl, Walter ^b   Glatt, Hansruedi ^b   Falany, Charles N ^c   Coughtrie, Michael W H ^d   Gerlienke Schuur, A ^e   Brouwer, Abraham ^f   Visser, Theo J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f INSTITUTE FOR ENVIRONMENTAL STUDIES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON; DRUG METABOLITE; ESTROGEN SULFOTRANSFERASE; HALOGEN; HYDROCARBON; HYDROXYL GROUP; POLYHALOGENATED AROMATIC HYDROCARBON; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; COMPETITIVE INHIBITION; CORRELATION ANALYSIS; DRUG INHIBITION; ENDOCRINOLOGY; ESTROGEN ACTIVITY; HUMAN; HYDROXYLATION; LIVER CYTOSOL; PRIORITY JOURNAL; SULFATION;

AVES; MAMMALIA; REPTILIA; VERTEBRATA;

EID: 0036963632     PISSN: 0021972X     EISSN: None     Source Type: Journal    
DOI: 10.1210/jcem.87.3.8311     Document Type: Article

References (54)

1. Cheek AO, Vonier PM, Oberdorster E, Burrow BC, McLachlan JA 1998 Environmental signaling: a biological context for endocrine disruption. Environ Health Perspect 106(Suppl 1):5-10
2. Cooper RL, Kavlock RJ 1997 Endocrine disruptors and reproductive development: a weight-of-evidence overview. J Endocrinol 152:159-166
3. Neubert D 1997 Vulnerability of the endocrine system to xenobiotic influence. Regul Toxicol Pharmacol 26:9-29
4. Ahlborg UG, Brouwer A, Fingerhut MA, Jacobson JL, Jacobson SW, Kennedy SW, Kettrup AAF, Koeman JH, Poiger H, Rappe C, Safe SH, Seegal RF, Tuomisto J, van den Berg M 1992 Impact of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls on human and environmental health, with special emphasis on application of the toxic equivalency factor concept. Eur J Pharmacol 228:179-199
5. Safe S, Astroff M, Harris M, Zacharewski T, Dickerson R, Romkes M, Biegel L 1991 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and related compounds as antiestrogens: characterization and mechanism of action. Pharmacol Toxicol 69:400-409
6. Peterson RE, Theobald HM, Kimmel GL 1993 Developmental and reproductive toxicity of dioxins and related compounds: cross-species comparisons. Crit Rev Toxicol 23:283-335
7. Safe SH 1994 Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol 24:87-149
8. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman MA 1997 A maternal diet high in n-6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci USA 94:9372-9377
9. Auger J, Kunstmann JM, Czyglik F, Jouannet P 1995 Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med 332:281-285
10. Skakkebaek NE, Rajpert-de Meyts E, Jørgensen N, Carlsen E, Petersen PM, Giwercman A, Andersen AG, Jensen TK, Andersson AM, Muller J 1998 Germ cell cancer and disorders of spermatogenesis: an environmental connection? APMIS 106:3-11
11. Wolff MS, Tonioli PG, Lee EW, Rivera M, Dubin N 1993 Blood levels of organochlorine residues and risk of breast cancer. J Natl Cancer Inst 85:648-652
12. Hoyer AP, Jorgensen T, Brock JW, Grandjean P 2000 Organochlorine exposure and breast cancer survival. J Clin Epidemiol 53:323-330
13. Dorgan JF, Brock JW, Rothman N, Needham LL, Miller R, Stephenson HE Jr, Schussler N, Taylor PR 1999 Serum organochlorine pesticides and PCBs and breast cancer risk: results from a prospective analysis (USA). Cancer Causes Control 10:1-11
14. Adami HO, Lipworth L, Titus-Emstoff L, Hsieh CC, Hanberg A, Ahlborg U, Baron J, Trichopoulos D 1995 Organochlorine compounds and estrogen-related cancers in women. Cancer Causes Control 6:551-566
15. Safe S 2000 Endocrine disruptors and human health-is there a problem? An update. Environ Health Perspect 108:487-493
16. Bergman A, Klasson-Wehler E, Kuroki H 1994 Selective retention of hydroxylated PCB metabolites in blood. Environ Health Perspect 102:464-469
17. Morse DC, Klasson-Wehler E, Wesseling W, Koeman JH, Brouwer A 1996 Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (Aroclor 1254). Toxicol Appl Pharmacol 136:269-279
18. Wroblewski VJ, Olson JR 1985 Hepatic metabolism of 2,3,7,8-tetradibenzop-dioxin (TCDD) in the rat and guinea pig. Toxicol Appl Pharmacol 81:231-240
19. Pluess N, Poiger H, Schlatter C, Buser HR 1987 The metabolism of some pentachlorodibenzofurans in the rat. Xenobiotica 17:209-216
20. Hu K, Bunce NJ 1999 Metabolism of polychlorinated dibenzo-p-dioxins and related dioxin-like compounds. J Toxicol Environ Health 2:183-210
21. Crews D, Bergeron JM, McLachlan JA 1995 The role of estrogen in sex turtle determination and the effect of PCBs. Environ Health Perspect 103(Suppl 7):73-77
22. Bergeron RM, Thompson TB, Leonard LS, Pluta L, Gaido KW 1999 Estrogenicity of bisphenol A in a human endometrial carcinoma cell line. Mol Cell Endocrinol 150:179-187
23. Kuiper GGJM, Lemmen JG, Carlsson B, Corton JC, Safe SH, Van Der Saag PT, Van der Burg B, Gustafsson JA 1998 Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139:4252-4263
24. Strott CA 1996 Steroid sulfotransferases. Endocr Rev 17:670-697
25. Kester MHA, Van Dijk CH, Tibboel D, Hood AM, Rose NJM, Meinl W, Pabel U, Glatt H, Falany CN, Coughtrie MWH, Visser TJ 1999 Sulfation of thyroid hormone by estrogen sulfotransferase. J Clin Endocrinol Metab 84:2577-2580
26. Falany JL, Azziz R, Falany CN 1998 Identification and characterization of cytosolic sulfotransferases in normal human endometrium. Chem Biol Interact 109:329-339
27. Lewis AJ, Walle UK, King RS, Kadlubar FF, Falany CN, Walle T 1998 Bioactivation of the cooked food mutagen N-hydroxy-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by estrogen sulfotransferase in human mammary epithelial cells. Carcinogenesis 19:2049-2053
28. Qian VM, Song WC 1999 Regulation of estrogen sulfotransferase expression in Leydig cells by cyclic adenosine 3′,5′-monophosphate and androgen. Endocrinology 140:1048-1053
29. Song WC, Qian Y, Li AP 1998 Estrogen sulfotransferase expression in the human liver: marked interindividual variation and lack of gender specificity. J Pharmacol Exp Ther 284:1197-1202
30. Kester MHA, Bulduk S, Tibboel D, Meinl W, Glatt H, Falany CN, Coughtrie MWH, Bergman A, Safe SH, Kuiper GGJM, Schuur AG, Brouwer A, Visser TJ 2000 Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: a novel pathway explaining the estrogenic activity of PCBs. Endocrinology 141:1897-1900
31. Wilborn TW, Comer KA, Dooley TP, Reardon IM, Heinrikson IL, Falany CN 1993 Sequence analysis and expression of the cDNA for the phenol-sulfating form of human liver phenol sulfotransferase. Mol Pharmacol 43:70-77
32. Falany CN 1997 Enzymology of human cytosolic sulfotransferases. FASEB J 11:211-218
33. Schuur AG, Legger FF, Van Meeteren ME, Moonen MJ, Van Leeuwen-Bol I, Bergman A, Visser TJ, Brouwer A 1998 In vitro inhibition of thyroid hormone sulfation by hydroxylated metabolites of halogenated aromatic hydrocarbons. Chem Res Toxicol 111:1075-1081
34. Meerts IATM, Van Zanden JJ, Luijks EAC, Van Leeuwen-Bol I, Marsh G, Jakobsson E, Bergman A, Brouwer A 2000 Potent competitive interactions of some brominated flame retardants and related compounds with human transthyretin in vitro. Toxicol Sci 56:95-104
35. Falany CN, Krashnykh V, Falany J 1995 Bacterial expression and characterization of a cDNA for human liver estrogen sulfotransferase. J Steroid Biochem Mol Biol 52:529-539
36. Hagen M, Pabel U, Landsiedel R, Bartsch I, Falany CN, Glatt H 1998 Expression of human estrogen sulfotransferase in Salmonella typhimurium: differences between hHST and hEST in the enantioselective activation of 1-hydroxyethylpyrene to a mutagen. Chem Biol Interact 109:249-253
37. Glatt H, Engelke CEH, Pabel U, Teubner W, Jones AL, Coughtrie MWH, Andrae U, Falany CN, Meinl W 2000 Sulfotransferases: genetics and role in toxicology. Toxicol Lett 112-113:341-348
38. Rubin GL, Harrold AJ, Mills JA, Falany CN, Coughtrie MWH 1999 Regulation of sulphotransferase expression in the endometrium during the menstrual cycle, by oral contraceptives and during early pregnancy. Mol Hum Reprod 5:995-1002
39. Visser TJ, Kaptein E, Terpstra OT, Krenning EP 1988 Deiodination of thyroid hormone by human liver. J Clin Endocrinol Metab 67:17-24
40. Ainsworth S 1977 Michaelis-Menten kinetics. In: Ainsworth S, ed. Steady-state enzyme kinetics. London: MacMillan; 43-73
41. Foldes A, Meek JL 1973 Rat brain phenolsulfotransferase: partial purification and some properties. Biochim Biophys Acta 327:365-374
42. Song WC, Melner MH 2000 Editorial: steroid transformation enzymes as critical regulators of steroid action in vivo. Endocrinology 141:1587-1589
43. Kakuta Y, Pedersen LG, Carter CW, Negishi M, Pedersen LC 1997 Crystal structure of estrogen sulfotransferase. Nat Struct Biol 4:904-908
44. Kakuta Y, Pedersen LP, Chae K, Song WC, Leblanc D, London R, Carter CW, Negishi M 1998 Mouse steroid sulfotransferases: substrate specificity and preliminary x-ray crystallographic analysis. Biochem Pharmacol 55:313-317
45. Brotons JA, Olea-Serrano MF, Villalobos M, Pedraza V, Olea N 1995 Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect 103:608-612
46. WHO 1995 International Programme on Chemical Safety: tetrabromobisphenol A and derivatives. Geneva: WHO; Environ Health Criteria 172
47. Larsen J 1995 Levels of pollutants and their metabolites: exposures to organic substances. Toxicology 101:11-27
48. Zhang H, Varmalova O, Vargas FM, Falany CN, Leyh TS 1998 Sulfuryl transfer: the catalytic mechanism of human estrogen sulfotransferase. J Biol Chem 273:10888-10892
49. Harris RM, Waring RH, Kirk CJ, Hughes PJ 2000 Sulfation of "estrogenic" alkylphenols and 17β-estradiol by human platelet phenol sulfotransferases. J Biol Chem 275:159-166
50. Suiko M, Sakakibara Y, Liu MC 2000 Sulfation of environmental estrogen-like chemicals by human cytosolic sulfotransferases. Biochem Biophys Res Commun 267:80-84
51. Falany CN, Wheeler J, Oh TS, Falany JL 1994 Steroid sulfation by expressed human cytosolic sulfotransferases. J Steroid Biochem Mol Biol 48:369-375
52. Coughtrie MWH, Sharp S, Maxwell K, Innes NP 1998 Biology and function of the reversible sulfation pathway catalysed by human sulfotransferases and sulfatases. Chem Biol Interact 109:3-27
53. Brouwer A, Morse DC, Lans MC, Schuur AG, Murk AJ, Klasson-Wehler E, Bergman A, Visser TJ 1998 Interactions of persistant environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol Industr Health 14:59-84
54. Visser TJ 1994 Role of sulfation in thyroid hormone metabolism. Chem Biol Interact 92:293-303