Polychlorinated biphenyl congeners that increase the glucuronidation and biliary excretion of thyroxine are distinct from the congeners that enhance the serum disappearance of thyroxine

Drug Metabolism and Disposition

Volumn 40, Issue 3, 2012, Pages 588-595

  Martin, L A ^a,b   Wilson, D T ^b   Reuhl, K R ^b   Gallo, M A ^b   Klaassen, Curtis D ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,2',3,5',6 PENTACHLOROBIPHENYL; 2,2',4,4',5 PENTACHLOROBIPHENYL; 2,3',4,4',5 PENTACHLOROBIPHENYL; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 3,3',4,4',5 PENTACHLOROBIPHENYL; AROCLOR 1242; AROCLOR 1254; AROMATIC HYDROCARBON RECEPTOR; CORN OIL; GLUCURONIDE; GLUCURONOSYLTRANSFERASE; LIOTHYRONINE; POLYCHLORINATED BIPHENYL DERIVATIVE; THYROXINE; THYROXINE I 125; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILIARY EXCRETION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; GLUCURONIDATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORMONE DETERMINATION; LIOTHYRONINE BLOOD LEVEL; LIVER MICROSOME; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; THYROXINE BLOOD LEVEL;

ANIMALS; BILE; BODY WEIGHT; CHLORODIPHENYL (54% CHLORINE); GLUCURONIDES; GLUCURONOSYLTRANSFERASE; LIVER; MALE; MICROSOMES, LIVER; POLYCHLORINATED BIPHENYLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; THYROXINE;

EID: 84857377134     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.111.042796     Document Type: Article

References (40)

1. Abe T, Kakyo M, Sakagami H, Tokui T, Nishio T, Tanemoto M, Nomura H, Hebert SC, Matsuno S, Kondo H, et al. (1998) Molecular characterization and tissue distribution of a new organic anion transporter subtype (oatp3) that transports thyroid hormones and taurocholate and comparison with oatp2. J Biol Chem 273:22395-22401. (Pubitemid 28399802)
2. Barter RA and Klaassen CD (1992) UDP-glucuronosyltransferase inducers reduce thyroid hormone levels in rats by an extrathyroidal mechanism. Toxicol Appl Pharmacol 113:36-42.
3. Bastomsky CH (1974) Effects of a polychlorinated biphenyl mixture (aroclor 1254) and DDT on biliary thyroxine excretion in rats. Endocrinology 95:1150-1155.
4. Beetstra JB, van Engelen JG, Karels P, van der Hoek HJ, de Jong M, Docter R, Krenning EP, Hennemann G, Brouwer A, and Visser TJ (1991) Thyroxine and 3,3′,5-triiodothyronine are glucuronidated in rat liver by different uridine diphosphate-glucuronyltransferases. Endocrinology 128:741-746.
5. Capen CC (1994) Mechanisms of chemical injury of thyroid gland. Prog Clin Biol Res 387:173-191.
6. 125I-thyroxine and fine structural alterations in the thyroid glands of Gunn rats fed polychlorinated biphenyls (PCB). Lab Invest 43:158-164.
7. Craft ES, DeVito MJ, and Crofton KM (2002) Comparative responsiveness of hypothyroxinemia and hepatic enzyme induction in Long-Evans rats versus C57BL/6J mice exposed to TCDD-like and phenobarbital-like polychlorinated biphenyl congeners. Toxicol Sci 68:372-380. (Pubitemid 34919179)
8. De Voogt P and Brinkman AT (1989). Production properties and usage of polychlorinated biphenyls, in Halogenated Biphenyls, Terphenyls, Naphthalenes and Dibenzodioxins and Related Products (Kimbrough RD and Jensen AA eds), Elsevier, New York.
9. Docter R, Friesema EC, van Stralen PG, Krenning EP, Everts ME, Visser TJ, and Hennemann G (1997) Expression of rat liver cell membrane transporters for thyroid hormone in Xenopus laevis oocytes. Endocrinology 138:1841-1846. (Pubitemid 27180797)
10. Emi Y, Ikushiro S, and Iyanagi T (1996) Xenobiotic responsive element-mediated transcriptional activation in the UDP-glucuronosyltransferase family 1 gene complex. J Biol Chem 271:3952-3958. (Pubitemid 26065720)
11. Friesema EC, Docter R, Moerings EP, Stieger B, Hagenbuch B, Meier PJ, Krenning EP, Hennemann G, and Visser TJ (1999) Identification of thyroid hormone transporters. Biochem Biophys Res Commun 254:497-501. (Pubitemid 29290429)
12. Fujiwara K, Adachi H, Nishio T, Unno M, Tokui T, Okabe M, Onogawa T, Suzuki T, Asano N, Tanemoto M, et al. (2001) Identification of thyroid hormone transporters in humans: different molecules are involved in a tissue-specific manner. Endocrinology 142:2005-2012. (Pubitemid 32405959)
13. Guo GL, Choudhuri S, and Klaassen CD (2002) Induction profile of rat organic anion transporting polypeptide 2 (oatp2) by prototypical drug-metabolizing enzyme inducers that activate gene expression through ligand-activated transcription factor pathways. J Pharmacol Exp Ther 300:206-212. (Pubitemid 34028529)
14. Hagenbuch B (2007) Cellular entry of thyroid hormones by organic anion transporting polypeptides. Best Pract Res Clin Endocrinol Metab 21:209-221.
15. Hagenbuch N, Reichel C, Stieger B, Cattori V, Fattinger KE, Landmann L, Meier PJ, and Kullak-Ublick GA (2001) Effect of phenobarbital on the expression of bile salt and organic anion transporters of rat liver. J Hepatol 34:881-887. (Pubitemid 32595188)
16. Hennemann G, Docter R, Friesema EC, de Jong M, Krenning EP, and Visser TJ (2001) Plasma membrane transport of thyroid hormones and its role in thyroid hormone metabolism and bioavailability. Endocr Rev 22:451-476. (Pubitemid 32762323)
17. Hood A and Klaassen CD (2000) Differential effects of microsomal enzyme inducers on in vitro thyroxine (T(4)) and triiodothyronine (T(3)) glucuronidation. Toxicol Sci 55:78-84. (Pubitemid 30252438)
18. Klaassen CD (1974) Effect of microsomal enzyme inducers on the biliary excretion of cardiac glycosides. J Pharmacol Exp Ther 191:201-211.
19. Lecureux L, Dieter MZ, Nelson DM, Watson L, Wong H, Gemzik B, Klaassen CD, and Lehman-McKeeman LD (2009) Hepatobiliary disposition of thyroid hormone in Mrp2-deficient TR- rats: reduced biliary excretion of thyroxine glucuronide does not prevent xenobiotic-induced hypothyroidism. Toxicol Sci 108:482-491.
20. Li MH and Hansen LG (1997) Consideration of enzyme and endocrine interactions in the risk assessment of PCBs. Rev Toxicol 1:71-156.
21. Li M, Rhine C, and Hansen LG (1998) Hepatic enzyme induction and acute endocrine effects of 2,3,3′,4′,6-pentachlorobiphenyl in prepubertal female rats. Arch Environ Contam Toxicol 35:97-103. (Pubitemid 28275496)
22. Liu J, Liu Y, Barter RA, and Klaassen CD (1995) Alteration of thyroid homeostasis by UDP-glucuronosyltransferase inducers in rats: a dose-response study. J Pharmacol Exp Ther 273:977-985.
23. Martin L and Klaassen CD (2010) Differential effects of polychlorinated biphenyl congeners on serum thyroid hormone levels in rats. Toxicol Sci 117:36-44.
24. Masmoudi T, Hihi AK, Vázquez M, Artur Y, Desvergne B, Wahli W, and Goudonnet H (1997) Transcriptional regulation by triiodothyronine of the UDP-glucuronosyltransferase family 1 gene complex in rat liver. Comparison with induction by 3-methylcholanthrene. J Biol Chem 272:17171-17175. (Pubitemid 27289829)
25. Matthews HB and Dedrick RL (1984) Pharmacokinetics of PCBs. Annu Rev Pharmacol Toxicol 24:85-103. (Pubitemid 14129531)
26. McClain RM, Levin AA, Posch R, and Downing JC (1989) The effect of phenobarbital on the metabolism and excretion of thyroxine in rats. Toxicol Appl Pharmacol 99:216-228. (Pubitemid 19201310)
27. Murk AJ, Legler J, Denison MS, Giesy JP, van de Guchte C, and Brouwer A (1996) Chemical-activated luciferase gene expression (CALUX): a novel in vitro bioassay for Ah receptor active compounds in sediments and pore water. Fundam Appl Toxicol. 33:149-160.
28. Rausch-Derra LC, Hartley DP, Meier PJ, and Klaassen CD (2001) Differential effects of microsomal enzyme-inducing chemicals on the hepatic expression of rat organic anion transporters, OATP1 and OATP2. Hepatology 33:1469-1478. (Pubitemid 32496984)
29. Safe S, Bandiera S, Sawyer T, Robertson L, Safe L, Parkinson A, Thomas PE, Ryan DE, Reik LM, and Levin W (1985) PCBs: structure-function relationships and mechanism of action. Environ Health Perspect 60:47-56. (Pubitemid 15038884)
30. Schuur AG, Boekhorst FM, Brouwer A, and Visser TJ (1997) Extrathyroidal effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on thyroid hormone turnover in male Sprague-Dawley rats. Endocrinology 138:3727-3734. (Pubitemid 27351922)
31. Semler DE, Chengelis CP, and Radzialowski FM (1989) The effects of chronic ingestion of spironolactone on serum thyrotropin and thyroid hormones in the male rat. Toxicol Appl Pharmacol 98:263-268. (Pubitemid 19122373)
32. van Raaij JA, Kaptein E, Visser TJ, and van den Berg KJ (1993) Increased glucuronidation of thyroid hormone in hexachlorobenzene-treated rats. Biochem Pharmacol 45:627-631. (Pubitemid 23064568)
33. Vansell NR and Klaassen CD (2001) Increased biliary excretion of thyroxine by microsomal enzyme inducers. Toxicol Appl Pharmacol 176:187-194. (Pubitemid 34001309)
34. Vansell NR and Klaassen CD (2002) Effect of microsomal enzyme inducers on the biliary excretion of triiodothyronine (T(3)) and its metabolites. Toxicol Sci 65:184-191. (Pubitemid 34121110)
35. Visser TJ (1990) Importance of deiodination and conjugation in the hepatic metabolism of thyroid hormone, in The Thyroid Gland (Greer MA ed) pp 255-283, Raven Press Ltd, New York.
36. Visser TJ, Kaptein E, van Raaij JA, Joe CT, Ebner T, and Burchell B (1993a) Multiple UDP-glucuronyltransferases for the glucuronidation of thyroid hormone with preference for 3,3′,5′-triiodothyronine (reverse T3). FEBS Lett 315:65-68. (Pubitemid 23005732)
37. Visser TJ, Kaptein E, van Toor H, van Raaij JA, van den Berg KJ, Joe CT, van Engelen JG, and Brouwer A (1993b) Glucuronidation of thyroid hormone in rat liver: effects of in vivo treatment with microsomal enzyme inducers and in vitro assay conditions. Endocrinology 133:2177-2186. (Pubitemid 23324725)
38. Whitlock JP, Jr. (1993) Mechanistic aspects of dioxin action. Chem Res Toxicol 6:754-763.
39. Wong H, Lehman-McKeeman LD, Grubb MF, Grossman SJ, Bhaskaran VM, Solon EG, Shen HS, Gerson RJ, Car BD, Zhao B, et al. (2005) Increased hepatobiliary clearance of unconjugated thyroxine determines DMP 904-induced alterations in thyroid hormone homeostasis in rats. Toxicol Sci 84:232-242. (Pubitemid 40542282)
40. Wu SY, Green WL, Huang WS, Hays MT, and Chopra IJ (2005) Alternate pathways of thyroid hormone metabolism. Thyroid 15:943-958. (Pubitemid 41339272)