A physiological role for glucuronidated thyroid hormones: Preferential uptake by H9c2(2-1) myotubes

Molecular and Cellular Endocrinology

Volumn 264, Issue 1-2, 2007, Pages 109-117

  van der Heide, Sabine M ^a   Joosten, Brian J L J ^a   Dragt, Bieuwke S ^a   Everts, Maria E ^a   Klaren, Peter H M ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Cellular uptake; Differentiation; Glucuronidation; H9c2(2 1) cells; Myoblast; Thyroxine; Tri iodothyronine

Indexed keywords

BETA GLUCURONIDASE; LIOTHYRONINE; THYROID HORMONE; THYROXINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL STIMULATION; CELL STRAIN; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; GLUCURONIDATION; HEART MUSCLE CELL; HORMONE ACTION; HORMONE RELEASE; HORMONE TRANSPORT; INTERNALIZATION; MYOFIBROBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; RAT; THYROID HORMONE METABOLISM;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; FIBROBLASTS; GLUCURONATES; MUSCLE FIBERS; MYOBLASTS; MYOCARDIUM; RATS; RATS, WISTAR; TRIIODOTHYRONINE;

EID: 33846200424     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2006.10.012     Document Type: Article

References (58)

1. Abe T., Kakyo M., Sakagami H., Tokui T., Nishio T., Tanemoto M., Nomura H., Hebert S.C., Matsuno S., Kondo H., and Yawo H. 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 (1998) 22395-22401
2. Agocha A.E., and Eghbali-Webb M. A simple method for preparation of cultured cardiac fibroblasts from adult human ventricular tissue. Mol. Cell. Biochem. 172 (1997) 195-198
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., Brouwer A., and Visser T.J. Thyroxine and 3,3′,5-triiodothyronine are glucuronidated in rat liver by different uridine diphosphate-glucuronyltransferases. Endocrinology 128 (1991) 741-746
4. Blondeau J., Beslin A., Chantoux F., and Francon J. Triiodothyronine is a high-affinity inhibitor of amino acid transport system L1 in cultured astrocytes. J. Neurochem. 60 (1993) 1407-1413
5. Brown P.C., Thorgeirsson S.S., and Silverman J.A. Cloning and regulation of the rat mdr2 gene. Nucleic Acids Res. 21 (1993) 3885-3891
6. Burchell B., and Coughtrie M.W. UDP-glucuronosyltransferases. Pharmacol. Ther. 43 (1989) 261-289
7. Chang H.Y., Chi J.-T., Dudoit S., Bondre C., van de Rijn M., Botstein D., and Brown P.O. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 12877-12882
8. Cox D.S., Scott K.R., Gao H., and Eddington N.D. Effect of P-glycoprotein on the pharmacokinetics and tissue distribution of enaminone anticonvulsants: analysis by population and physiological approaches. J. Pharmacol. Exp. Ther. 302 (2002) 1096-1104
9. Csala M., Staines A.G., Bánhegyi G., Mandl J., Coughtrie M.W.H., and Burchell B. Evidence for multiple glucuronide transporters in rat liver microsomes. Biochem. Pharmacol. 68 (2004) 1353-1362
10. Cui Y., König J., Leier I., Buchholz U., and Keppler D. Hepatic uptake of bilirubin and its conjugates by the human organic anion transporter SLC21A6. J. Biol. Chem. 276 (2001) 9626-9630
11. Docter R., Krenning E.P., Bernard H.F., and Hennemann G. Active transport of iodothyronines into human cultured fibroblasts. J. Clin. Endocrinol. Metab. 65 (1987) 624-628
12. Eelkman Rooda S.J., Otten M.H., van Loon M.A.C., Kaptein E., and Visser T.J. Metabolism of triiodothyronine in rat hepatocytes. Endocrinology 125 (1989) 2187-2197
13. Everts M.E., Verhoeven F.A., Bezstarosti K., Moerings E.P.C.M., Hennemann G., Visser T.J., and Lamers J.-M.J. Uptake of thyroid hormones in neonatal rat cardiac myocytes. Endocrinology 137 (1996) 4235-4242
14. Fishman W.H. β-Glucuronidase. In: Bergmeyer H.U. (Ed). Methods of Enzymatic Analysis (1974), Academic Press, New York 929-943
15. Flens M.J., Zaman G.J., van der Valk P., Izquierdo M.A., Schroeijers A.B., Scheffer G.L., van der Groep P., de Haas M., Meijer C.J., and Scheper R.J. Tissue distribution of the multidrug resistance protein. Am. J. Pathol. 148 (1996) 1237-1247
16. 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. Identification of thyroid hormone transporters. Biochem. Biophys. Res. Commun. 254 (1999) 497-501
17. Friesema E.C.H., Docter R., Moerings E.P.C.M., Verrey F., Krenning E.P., Hennemann G., and Visser T.J. Thyroid hormone transport by the heterodimeric human system l-amino acid transporter. Endocrinology 142 (2001) 4339-4348
18. Friesema E.C.H., Ganguly S., Abdalla A., Manning Fox J.E., Halestrap A.P., and Visser T.J. Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J. Biol. Chem. 278 (2003) 40128-40135
19. Friesema E.C.H., Jansen J., and Visser T.J. Thyroid hormone transporters. Biochem. Soc. Trans. 33 (2005) 228-232
20. Fujiwara K., Adachi H., Nishio T., Unno M., Tokui T., Okabe M., Onogawa T., Suzuki T., Asano N., Tanemoto M., Seki M., Shiiba K., Suzuki M., Kondo Y., Nunoki K., Shimosegawa T., Iinuma K., Ito S., Matsuno S., and Abe T. Identification of thyroid hormone transporters in humans: different molecules are involved in a tissue-specific manner. Endocrinology 142 (2001) 2005-2012
21. Grams B., Harms A., Braun S., Strassburg C.P., Manns M.P., and Obermayer-Straub P. Distribution and inducibility by 3-methylcholanthrene of family 1 UDP-glucuronosyltransferases in the rat gastrointestinal tract. Arch. Biochem. Biophys. 377 (2000) 255-265
22. Hagenbuch B., and Meier P. Organic anion transporting polypeptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Pflügers Arch. 447 (2004) 653-665
23. Hays M.T., and Hsu L. Preparation and separation of the glucuronide and sulfate conjugates of thyroxine and triiodothyronine. Endocr. Res. 13 (1987) 215-228
24. Hays M.T., and Hsu L. Equilibrium dialysis studies of plasma binding of thyroxine, triiodothyronine and their glucuronide and sulfate conjugates in human and cat plasma. Endocr. Res. 14 (1988) 51-58
25. Hays M.T., and Cavalieri R.R. Deiodination and deconjugation of the glucuronide conjugates of the thyroid hormones by rat liver and brain microsomes. Metabolism 41 (1992) 494-497
26. Keppler D., Cui Y., König J., Leier I., and Nies A. Export pumps for anionic conjugates encoded by MRP genes. Adv. Enzyme Regul. 39 (1999) 237-246
27. Keppler D., Kamisako T., Leier I., Cui Y.H., Nies A.T., Tsujii H., and König J. Localization, substrate specificity, and drug resistance conferred by conjugate export pumps of the MRP family. Adv. Enzyme Regul. 40 (2000) 339-349
28. Kimes B.W., and Brandt B.L. Properties of a clonal muscle cell line from rat heart. Exp. Cell Res. 98 (1976) 367-381
29. König J., Nies A.T., Cui Y.H., Leier I., and Keppler D. Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim. Biophys. Acta Biomembr. 1461 (1999) 377-394
30. Lakshmanan M., Gonçalves E., Lessly G., Foti D., and Robbins J. The transport of thyroxine into mouse neuroblastoma cells, NB41A3: the effect of l-system amino acids. Endocrinology 126 (1990) 3245-3250
31. Leatherbarrow R.J. Enzfitter. A Non-Linear Regression Data Analysis Program for the IBM PC (1987), Elsevier Science Publishers BV, Amsterdam
32. Mackenzie P.I., Owens I.S., Burchell B., Bock K.W., Bairoch A., Belanger A., Fournel-Gigleux S., Green M., Hum D.W., Iyanagi T., Lancet D., Louisot P., Magdalou J., Chowdhury J.R., Ritter J.K., Schachter H., Tephly T.R., Tipton K.F., and Nebert D.W. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7 (1997) 255-269
33. Marquardt D.W. An algorithm for least squares estimation of parameters. J. Soc. Ind. Appl. Math. 11 (1963) 431-441
34. Meissner K., Jedlitschky G., Meyer zu Schwabedissen H., Dazert P., Eckel L., Vogelgesang S., Warzok R.W., Bohm M., Lehmann C., Wendt M., Cascorbi I., and Kroemer H.K. Modulation of multidrug resistance P-glycoprotein 1 (ABCB1) expression in human heart by hereditary polymorphisms. Pharmacogenetics 14 (2004) 381-385
35. Mol J.A., and Visser T.J. Synthesis and some properties of sulfate esters and sulfamates of iodothyronines. Endocrinology 117 (1985) 1-7
36. Nair K.G., Cutilletta A.F., Zak R., Koide T., and Rabinowitz M. Biochemical correlates of cardiac hypertrophy. Circ. Res. 23 (1968) 451-462
37. Pelsers M.M.A.L., Lutgerink J.T., van Nieuwenhoven F.A., Tandon N.N., van der Vusse G.J., Arends J.-W., Hoogenboom H.R., and Glatz J.F.C. A sensitive immunoassay for rat fatty acid translocase (CD36) using phage antibodies selected on cell transfectants: abundant presence of fatty acid translocase/CD36 in cardiac and red skeletal muscle and up-regulation in diabetes. Biochem. J. 337 (1999) 407-414
38. Samuels H.H., Stanley F., and Casanova J. Depletion of l-3,5,3′-triiodothyronine and l-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. Endocrinology 105 (1979) 80-85
39. Shelby M.K., Cherrington N.J., Vansell N.R., and Klaassen C.D. Tissue mRNA expression of the rat UDP-glucuronosyltransferase gene family. Drug Metab. Dispos. 31 (2003) 326-333
40. Shitara Y., Li A.P., Kato Y., Lu C., Ito K., Itoh T., and Sugiyama Y. Function of uptake transporters for taurocholate and estradiol 17β-d-glucuronide in cryopreserved human hepatocytes. Drug Metab. Pharmacokin. 18 (2003) 33-41
41. Sterling K., and Brenner M.A. Free thyroxine in human serum: simplified measurement with the aid of magnesium precipitation. J. Clin. Invest. 45 (1966) 153-163
42. Tsuruoka S., Ishibashi K., Yamamoto H., Wakaumi M., Suzuki M., Schwartz G.J., Imai M., and Fujimura A. Functional analysis of ABCA8, a new drug transporter. Biochem. Biophys. Res. Commun. 298 (2002) 41-45
43. Turgeon D., Carrier J.-S., Lévesque E., Hum D.W., and Bélanger A. Relative enzymatic activity, protein stability, and tissue distribution of human steroid-metabolizing UGT2B subfamily members. Endocrinology 142 (2001) 778-787
44. van der Heide S.M., Visser T.J., Everts M.E., and Klaren P.H.M. Metabolism of thyroid hormones in cultured cardiac fibroblasts of neonatal rats. J. Endocrinol. 172 (2002) 111-119
45. van der Heide S.M., Joosten B.J.L.J., Everts M.E., and Klaren P.H.M. Activities of UDP-glucuronyltransferase, β-glucuronidase and deiodinase types I and II in hyper- and hypothyroid rats. J. Endocrinol. 181 (2004) 393-400
46. van der Putten H.H.A.G.M., Joosten B.J.L.J., Klaren P.H.M., and Everts M.E. Characterization of uptake and compartmentalization of 3,5,3′-tri-iodothyronine in cultured neonatal rat cardiomyocytes. J. Endocrinol. 171 (2001) 183-192
47. van der Putten H.H.A.G.M., Joosten B.J.L.J., Klaren P.H.M., and Everts M.E. Uptake of tri-iodothyronine and thyroxine in myoblasts and myotubes of the embryonic heart cell line H9c2(2-1). J. Endocrinol. 175 (2002) 587-596
48. van der Putten H.H.A.G.M., Friesema E.C.H., Abumrad N.A., Everts M.E., and Visser T.J. Thyroid hormone transport by the rat fatty acid translocase. Endocrinology 144 (2003) 1315-1323
49. Verhoeven F.A., van der Putten H.H.A.G.M., Hennemann G., Lamers J.M.J., Visser T.J., and Everts M.E. Uptake of triiodothyronine and triiodothyroacetic acid in neonatal rat cardiomyocytes: effects of metabolites and analogs. J. Endocrinol. 173 (2002) 247-255
50. Visser T.J. Importance of deiodination and conjugation in the hepatic metabolism of thyroid hormone. In: Green M.A. (Ed). The Thyroid Gland (1990), Raven Press, New York 255-283
51. Visser T.J., Kaptein E., Gijzel A.L., de Herder W.W., Ebner T., and Burchell B. Glucuronidation of thyroid hormone by human bilirubin and phenol UDP-glucuronyltransferase isoenzymes. FEBS Lett. 324 (1993) 358-360
52. 3). FEBS Lett. 315 (1993) 65-68
53. Visser T.J. Pathways of thyroid hormone metabolism. Acta Med. Aust. 23 (1996) 10-16
54. Wassen F.W.J.S., Klootwijk W., Kaptein E., Duncker D.J., Visser T.J., and Kuiper G.G.J.M. Characteristics and thyroid state-dependent regulation of iodothyronine deiodinases in pigs. Endocrinology 145 (2004) 4251-4263
55. Wu S.-y., Green W.L., Huang W.-s., Hays M.T., and Chopra I.J. Alternate pathways of thyroid hormone metabolism. Thyroid 15 (2005) 943-958
56. Yonemoto T., Nishikawa M., Matsubara H., Mori Y., Toyoda N., Gondou A., Imai Y., Iwasaka T., and Inada M. Type 1 iodothyronine deiodinase in heart. Effects of triiodothyronine and angiotensin II on its activity and mRNA in cultured rat myocytes. Endocr. J. 46 (1999) 621-628
57. Zhou Y., Samson M., Osty J., Francon J., and Blondeau J.-P. Evidence for a close link between the thyroid hormone transport system and the aromatic amino acid transport system T in erythrocytes. J. Biol. Chem. 265 (1990) 17000-17004
58. Zhou Y., Samson M., Francon J., and Blondeau J.-P. Thyroid hormone concentrative uptake in rat erythrocytes. Involvement of the tryptophan transport system T in countertransport of tri-iodothyronine and aromatic amino acids. Biochem. J. 281 (1992) 81-86