Role of UDP-Glucuronosyltransferase (UGT) 2B2 in metabolism of triiodothyronine: Effect of microsomal enzyme inducers in sprague dawley and UGT2B2-deficient fischer 344 rats

Toxicological Sciences

Volumn 116, Issue 2, 2010, Pages 413-421

  Richardson, Terrilyn A ^a,b   Klaassen, Curtis D ^a  

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

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Microsomal enzyme inducers; Thyroid stimulating hormone; Triiodothyronine metabolism; UDP glucuronosyltransferase; UGT2B2 deficient Fischer 344 rats

Indexed keywords

16ALPHA CYANOPREGNENOLONE; 3 METHYLCHOLANTHRENE; AROCLOR 1254; GLUCOSE TRANSPORTER 3; GLYCOSYLTRANSFERASE; LIOTHYRONINE; MICROSOME ENZYME; THYROTROPIN; UDP GLUCURONOSYLTRANSFERASE 2B2; UNCLASSIFIED DRUG; ANDROSTERONE; GLUCURONIDE; GLUCURONOSYLTRANSFERASE;

AMINO ACID METABOLISM; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; FISCHER 344 RAT; GLUCURONIDATION; HORMONE METABOLISM; MALE; NONHUMAN; OVARY FOLLICLE CELL; RAT; RAT STRAIN; SPRAGUE DAWLEY RAT; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; ANIMAL; BLOOD; DEFICIENCY; DRUG EFFECTS; ENZYME INDUCTION; ENZYMOLOGY; METABOLISM; MICROSOME; PATHOLOGY; PHYSIOLOGY; THYROID GLAND;

ANDROSTERONE; ANIMALS; ENZYME INDUCTION; GLUCURONIDES; GLUCURONOSYLTRANSFERASE; MALE; MICROSOMES; PREGNENOLONE CARBONITRILE; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; THYROID GLAND; THYROTROPIN; TRIIODOTHYRONINE;

RATTUS; RODENTIA;

EID: 77955058999     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq125     Document Type: Article

References (40)

1. Abe, T., Kakyo, M., Tokui, T., Nakagomi, R., Nishio, T., Nakai, D., Nomura, H., Unno, M., Suzuki, M., Naitoh, T., et al. (1999). Identification of a novel gene family encoding human liver-specific organic anion transporter LST-1. J. Biol. Chem. 274, 17159-17163.
2. Bastomsky, C. H., and Papapetrou, P. D. (1973). The effect of methylcholanthrene on biliary thyroxine excretion in normal and Gunn rats. J. Endocrinol. 56, 267-273.
3. Beetstra, J. B., van Engelen, J. G. M., Karels, P., van der Hoek, H. J., de Jong, M., Docter, R., Krenning, E. P., Hennemann, G., Brower, A., and Visser, T. J. (1991). Thyroxine and 3, 3′, 5-triiodothyronine are glucuronidated in rat liver by different uridine diphosphate-glucuronosyltransferases. Endocrinology 128, 741-746.
4. Capen, C. C. (2008) Toxic responses of the endocrine system. In Casarett and Doull's Toxicology: The Basic Science of Poisons, (C .D. Klaassen, Ed.), 7th edn. pp. 807-879. New York: McGraw-Hill Professional.
5. Cattori, V., Hagenbuch, B., Hagenbuch, N., Stieger, B., Ha, R., Winterhalter, K. E., and Meier, P. J. (2000). Identification of organic anion transporting polypeptide 4 (oatp4) as a major full-length isoform of the liver-specific transporter-1 (rlst-1) in rat liver. FEBS Lett. 22, 451-476.
6. Corser, R. B., Coughtrie, M. W. H., Jackson, M. R., and Burchell, B. (1987). The molecular basis of the inherited deficiency of androsterone UDP-glurcuronosyltransferase in Wistar rats. FEBS Lett. 213, 448-452.
7. Friesema, E. C. H., Docter, R., Moerings, E. P. C. M., Stieger, B., Hagenbuch, B., Meier, P. J., Krenning, E. P., Hennemann, G., and Visser, T. J. (1999). Identification of thyroid hormone transporter. Biochem. Biophys. Res. Comm. 254, 497-501.
8. Friesema, E. C. H., Ganguly, S., Abdalla, A., Manning Fox, J. E., Halestrap, A. P., and Visser, T. J. (2003). Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J. Biol. Chem. 278, 40128-40135.
9. 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.
10. Guo, G. L., Staudinger, J., Ogura, K., and Klaassen, C. D. (2002). Induction of rat organic anion transporting polypeptide 2 by pregnenolone-16α-carbonitrile is via interaction with pregnane X receptor. Mol. Pharmacol. 61, 832-839.
11. Haque, S. J., Petersen, D. D., Nebert, D. W., and Mackenzie, P. I. (1991). Isolation, sequence, and developmental expression of rat UGT2B2: The gene encoding a constitutive UDP glucuronosyltranferase that metabolizes etiocholanolone and androsterone. DNA Cell Biol. 10, 515-524.
12. Hennemann, G., Docter, R., Friesema, E. C. H., de Jong, M., Krenning, E. P., and Visser, T. J. (2001). Plasma membrane transport of thyroid hormones and its role in thyroid hormone metabolism and bioavailability. Endocr. Rev. 22, 451-476.
13. Higuchi, K., Kobayashi, Y., Kuroda, M., Tanaka, Y., Itani, T., Araki, J., Mifuji, R., Kaito, M., and Adachi, Y. (2004). Modulation of organic anion transporting polypeptide 1 and multidrug resistance protein 3 expression in the liver and kidney of Gunn rats. Hepatol. Res. 29, 60-66.
14. Homma, H., Kawai, H., Kubota, M., and Matsui, M. (1992). Large deletion of androsterone UDP-glucuronosyltransferase gene in the inherited deficient strain of Wistar rats. Biochim. Biophys. Acta 1138, 34-40.
15. Hood, A., Hashmi, R., and Klaassen, C. D. (1999a). Effects of microsomal enzyme inducers on thyroid-follicular cell proliferation, hyperplasia, and hypertrophy. Toxicol. Appl. Pharmacol. 160, 163-170.
16. Hood, A., and Klaassen, C. D. (1999). Effects of microsomal enzyme inducers on outer-ring deiodinase activity toward thyroid hormones in various rat tissues. Toxicol. Appl. Pharmacol. 163, 240-248.
17. 3) glucuronidation. Toxicol. Sci. 55, 78-84.
18. Hood, A., Liu, J., Liu, Y., Gattone, V., and Klaassen, C. D. (1999b). Sensitivity of thyroid gland growth to thyroid stimulating hormone (TSH) in rats treated with antithyroid drugs. Toxicol. Sci. 49, 263-271.
19. Kurki, P., Vanderlaan, M., Dolbeare, F., Gray, J., and Tan, E. M. (1986). Expression of proliferation cell nuclear antigen (PCNA)/cyclin during the cell cycle. Exp. Cell Res. 166, 209-219.
20. Lecureux, L., Dieter, M. Z., Nelson, D. M., Watson, L., Wong, H., Gemzik, B., Klaassen, C. D., and Lehman-McKeeman, L. D. (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.
21. Liu, J., Liu, Y., Barter, R. A., and Klaassen, C. D. (1995). Alteration of thyroid homeostasis by UDP-glucuronosyltransferase inducers in rats: a dose-response study. J. Pharmacol. Exp. Ther. 273, 977-985.
22. Masmoudi, T., Planells, R., Mounie, J., Artur, Y., Magdalou, J., and Goudonnet, H. (1996). Opposite regulation of bilirubin and 4-nitrophenol UDP-glucuronosyltransferase mRNA levels by 3,3′,5 triiodo-L-thyronine in rat liver. FEBS Lett. 379, 181-5.
23. Matsui, M., and Hakozaki, M. (1979). Discontinuous variation in hepatic uridine diphosphate glucuronosyltransferase toward androsterone in Wistar rats. Biochem. Pharmacol. 28, 411-415.
24. McClain, R. M., Levin, A. A., Posch, R., and Downing, J. C. (1989). The effect of phenobarbital on the metabolism and excretion of thyroxine in rats. Toxicol. Appl. Pharmacol. 99, 216-228.
25. McClain, R. M., Posch, R. C., Bosakowski, T., and Armstrong, J. M. (1988). Studies on the mode of action for thyroid gland tumor promotion in rats by phenobarbital. Toxicol. Appl. Pharmacol. 94, 254-265.
26. Pizzagalli, F., Hagenbuch, B., Stieger, B., Klenk, U., Folkers, G., and Meier, P. J. (2002). Identification of a novel human organic anion transporting polypeptide as a high affinity thyroxine transporter. Mol. Endocrinol. 16, 2283-2296.
27. Radominska, A., Little, J. M., Lester, R., and Mackenzie, P. I. (1994). Bile acid glucuronidation by rat liver microsomes and cDNA-expressed UDP-glucuronosyltransferases. Biochim. Biophys. Acta 1205, 75-82.
28. Rao, G. S., Haueter, G., Rao, M. L., and Breuer, H. (1976). An improved assay for steroid glucuronosyltransferase in rat liver microsomes. Anal. Biochem. 74, 35-40.
29. Ritter, J. K. (2000). Roles of glucuronidation and UDP-glucuronosyltransferases in xenobiotic bioactivation reactions. Chem. Biol. Interact 129, 171-193.
30. Saghir, S. A., Charles, G. D., Bartels, M. J., Kan, L. H., Dryzga, M. D., Brzak, K. A., and Clark, A. J. (2008). Mechanism of trifluralin-induced thyroid tumors in rats. Toxicol. Lett. 180, 38-45.
31. Sugiyama, D., Kusuhara, H., Taniguchi, H., Ishikawa, S., Nozaki, Y., Aburatani, H., and Sugiyama, Y. (2003). Functional characterization of rat brain-specific organic anion transporter (Oatp14) at the blood-brain barrier. J. Biol. Chem. 278, 43489-43495.
32. Tohyama, K., Kusuhara, H., and Sugiyama, Y. (2004). Involvement of multispecific organic anion transporter, Oatp14 (Slc21a14), in the transport of thyroxine across the blood-brain barrier. Endocrinology 145, 4384-4391.
33. van Raaij, J. A. G. M., Kaptein, E., Visser, T. J., and Van Den Berg, K. J. (1993). Increased glucuronidation of thyroid hormone in hexachlorobenzenetreated rats. Biochem. Pharmacol. 45, 627-631.
34. Vansell, N. R., and Klaassen, C. D. (2001). Increased biliary excretion of thyroxine by microsomal enzyme inducers. Toxicol. Appl. Pharmacol. 176, 187-194.
35. 3) and its metabolites. Toxicol. Sci. 65, 184-191.
36. Vansell, N. R., and Klaassen, C. D. (2002b). Increase in rat liver UDP-glucuronosyltransferase mRNA by microsomal enzyme inducers that enhance thyroid hormone glucuronidation. Drug Metab. Disp. 30, 240-246.
37. Vansell, N. R., Muppidi, J. R., Habeebu, S. M., and Klaassen, C. D. (2004). Promotion of thyroid tumors in rats by pregnenolone-16α-carbonitrile (PCN) and polychlorinated biphenyl (PCB). Toxicol. Sci. 81, 50-59.
38. Velicky, J., Titlbach, M., Lojda, Z., Jelinek, F., Vobecky, M., and Raska, I. (1997). Expression of the proliferating nuclear cell antigen (PCNA) in the rat thyroid gland after exposure to bromide. Acta Histochem. 99, 391-399.
39. Visser, T. J., Kaptein, E., and Harpur, E. S. (1991). Differential expression and ciprofibrate induction of hepatic UDP-glucuronyltransferases for thyroxine and triiodothyronine in Fischer rats. Biochem. Pharmacol. 42, 444-446.
40. Visser, T. J., Kaptein, E., van Toor, H., van Raaij, J. A. G. M., van den Berg, K. J., Joe, C. T. T., van Engelen, J. G. M., and Brouwer, A. (1993). 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.