The nuclear receptors pregnane X receptor and constitutive androstane receptor contribute to the impact of fipronil on hepatic gene expression linked to thyroid hormone metabolism

Biochemical Pharmacology

Volumn 86, Issue 7, 2013, Pages 997-1039

  Roques, Béatrice B ^a,b   Leghait, Julien ^a,b   Lacroix, Marlène Z ^a,b   Lasserre, Frédéric ^a   Pineau, Thierry ^a   Viguié, Catherine ^a,b   Martin, Pascal G P ^a  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Constitutive androstane receptor; Fipronil; Hepatic metabolism; Pregnane X receptor; Rodents; Thyroid hormone metabolism

Indexed keywords

ACYL COENZYME A DESATURASE; ATP BINDING CASSETTE G5; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE 8; CARBOXYLESTERASE; CARBOXYLESTERASE 2; CARBOXYLESTERASE 6; CARRIER PROTEINS AND BINDING PROTEINS; CD36 ANTIGEN; CONSTITUTIVE ANDROSTANE RECEPTOR; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 3; CYTIDINE DEAMINASE; CYTOCHROME P450 2B1; CYTOCHROME P450 2B2; CYTOCHROME P450 3A1; CYTOCHROME P450 3A11; FIPRONIL; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1A1; GLUCURONOSYLTRANSFERASE 1A6; GLUCURONOSYLTRANSFERASE 1A9; GLUTATHIONE TRANSFERASE A2; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE 1; PHOSPHORIBOSYLTRANSFERASE; PREGNANE X RECEPTOR; THYROID HORMONE; UDP GLUCURONOSYLTRANSFERASE 1A2; UDP GLUCURONOSYLTRANSFERASE 2A3; UDP GLUCURONOSYLTRANSFERASE 2B1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG METABOLISM; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; LIVER; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; THYROID HORMONE METABOLISM; UNINDEXED SEQUENCE; UPREGULATION;

Γ-AMINOBUTYRIC ACID; (13)C(6)-LEVOTHYROXINE (PUBCHEM CID: 53442260); 5′-DIPHOSPHO (UDP)-GLUCURONOSYLTRANSFERASE; ABC; ATP-BINDING CASSETTE; CAR; CARBOXYLESTERASE; CES; CONSTITUTIVE ANDROSTANE RECEPTOR; CYP; CYTOCHROME P450; ELECTROSPRAY IONIZATION MODE; ESI(+); FIPRONIL; FIPRONIL (PUBCHEM CID: 3352); FREE THYROXINE; FREE TRIIODOTHYRONINE; FT3; FT4; GABA; GENE EXPRESSION OMNIBUS; GENE ONTOLOGY; GEO; GLUTATHIONE S-TRANSFERASE; GO; GST; HEPATIC METABOLISM; LIMIT OF QUANTIFICATION; LOQ; MRM; MRP; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN; MULTIPLE REACTION MONITORING; OATP; ORGANIC ANION-TRANSPORTING POLYPEPTIDE; PB; PCN; PHENOBARBITAL; POLR2A; PREGNANE X RECEPTOR; PREGNENOLONE-16ALPHA-CARBONITRILE; PXR; QC; QUALITY CONTROL; REAL-TIME QUANTITATIVE POLYMERASE CHAIN REACTION; RNA POLYMERASE II POLYPEPTIDE A; RODENTS; RT-QPCR; SLCO; SOLUTE CARRIER ORGANIC ANION TRANSPORTER; SULFOTRANSFERASE; SULT; T3; T4; TATA-BOX BINDING PROTEIN; TBP; THYROID HORMONE METABOLISM; THYROID-STIMULATING HORMONE; THYROXINE; THYROXINE (PUBCHEM CID: 5819); TOTAL THYROXINE; TOTAL TRIIODOTHYRONINE; TRIIODOTHYRONINE; TRIIODOTHYRONINE (PUBCHEM CID: 5920); TSH; TT3; TT4; UGT;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PYRAZOLES; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; SPECIES SPECIFICITY; THYROID HORMONES; TRANSCRIPTOME;

EID: 84884670048     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.08.012     Document Type: Article

References (35)

1. L.M. Cole, R.A. Nicholson, and J.E. Casida Action of phenylpyrazole insecticides at the GABA-gated chloride channel Pest Biochem Physiol 46 1993 47 54
2. D. Hainzl, L.M. Cole, and J.E. Casida Mechanisms for selective toxicity of fipronil insecticide and its sulfone metabolite and desulfinyl photoproduct Chem Res Toxicol 11 1998 1529 1535 (Pubitemid 29013629)
3. Agence Française de Sécurité Sanitaire des Aliments (AFSSA), Agence Française de Sécurité Sanitaire Environnementale (AFSSE) Evaluation des risques pour la santé humaine liés à une exposition au fipronil 2005 173
4. J. Leghait, V. Gayrard, N. Picard-Hagen, M. Camp, E. Perdu, and P.L. Toutain Fipronil-induced disruption of thyroid function in rats is mediated by increased total and free thyroxine clearances concomitantly to increased activity of hepatic enzymes Toxicology 255 2009 38 44
5. B.B. Roques, M.Z. Lacroix, S. Puel, V. Gayrard, N. Picard-Hagen, and I. Jouanin CYP450-dependent biotransformation of the insecticide fipronil into fipronil sulfone can mediate fipronil-induced thyroid disruption in rats Toxicol Sci 127 2012 29 41
6. P.M. Yen Physiological and molecular basis of thyroid hormone action Physiol Rev 81 2001 1097 1142 (Pubitemid 32606667)
7. J. Tang, K. Amin Usmani, E. Hodgson, and R.L. Rose In vitro metabolism of fipronil by human and rat cytochrome P450 and its interactions with testosterone and diazepam Chem Biol Interact 147 2004 319 329 (Pubitemid 38591501)
8. P. Wei, J. Zhang, D.H. Dowhan, Y. Han, and D.D. Moore Specific and overlapping functions of the nuclear hormone receptors CAR and PXR in xenobiotic response Pharmacogenomics J 2 2002 117 126 (Pubitemid 34982215)
9. W. Xie, M.F. Yeuh, A. Radominska-Pandya, S.P. Saini, Y. Negishi, and B.S. Bottroff Control of steroid, heme, and carcinogen metabolism by nuclear pregnane X receptor and constitutive androstane receptor Proc Natl Acad Sci U S A 100 2003 4150 4155 (Pubitemid 36418172)
10. J.M. Maglich, J. Watson, P.J. McMillen, B. Goodwin, T.M. Willson, and J.T. Moore The nuclear receptor CAR is a regulator of thyroid hormone metabolism during caloric restriction J Biol Chem 279 2004 19832 19838 (Pubitemid 38623423)
11. J.L. Staudinger, B. Goodwin, S.A. Jones, D. Hawkins-Brown, K.I. MacKenzie, and A. LaTour The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity Proc Natl Acad Sci U S A 98 2001 3369 3374 (Pubitemid 32220852)
12. N.J. Cherrington, A.L. Slitt, J.M. Maher, X.X. Zhang, J. Zhang, and W. Huang Induction of multidrug resistance protein 3 (mrp3) in vivo is independent of constitutive androstane receptor Drug Metab Dispos 31 2003 1315 1319 (Pubitemid 37310319)
13. G. Lemaire, W. Mnif, J.M. Pascussi, A. Pillon, F. Rabenoelina, and H. Fenet Identification of new human pregnane X receptor ligands among pesticides using a stable reporter cell system Toxicol Sci 91 2006 501 509 (Pubitemid 43832507)
14. P. Wei, J. Zhang, M. Egan-Hafley, S. Liang, and D.D. Moore The nuclear receptor CAR mediates specific xenobiotic induction of drug metabolism Nature 407 2000 920 923
15. M.Z. Lacroix, S. Puel, P.L. Toutain, and C. Viguie Quantification of fipronil and its metabolite fipronil sulfone in rat plasma over a wide range of concentrations by LC/UV/MS J Chromatogr B Analyt Technol Biomed Life Sci 878 2010 1934 1938
16. P.C. Das, Y. Cao, N. Cherrington, E. Hodgson, and R.L. Rose Fipronil induces CYP isoforms and cytotoxicity in human hepatocytes Chem Biol Interact 164 2006 200 214 (Pubitemid 44779573)
17. D.M. Klachko, and E.R. Johnson The liver and circulating thyroid hormones J Clin Gastroenterol 5 1983 465 471 (Pubitemid 13006348)
18. G.S. Kelly Peripheral metabolism of thyroid hormones: a review Altern Med Rev 5 2000 306 333
19. H. Ren, B. Vallanat, D.M. Nelson, L.W. Yeung, K.S. Guruge, and P.K. Lam Evidence for the involvement of xenobiotic-responsive nuclear receptors in transcriptional effects upon perfluoroalkyl acid exposure in diverse species Reprod Toxicol 27 2009 266 277
20. S.Y. Wu, W.L. Green, W.S. Huang, M.T. Hays, and I.J. Chopra Alternate pathways of thyroid hormone metabolism Thyroid 15 2005 943 958 (Pubitemid 41339272)
21. M.H. Kester, E. Kaptein, T.J. Roest, C.H. van Dijk, D. Tibboel, and W. Meinl Characterization of rat iodothyronine sulfotransferases Am J Physiol Endocrinol Metab 285 2003 E592 E598
22. P.M. Hurley, R.N. Hill, and R.J. Whiting Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents Environ Health Perspect 106 1998 437 445 (Pubitemid 28470158)
23. B. Hagenbuch Cellular entry of thyroid hormones by organic anion transporting polypeptides Best Pract Res Clin Endocrinol Metab 21 2007 209 221 (Pubitemid 46888194)
24. L. Lecureux, M.Z. Dieter, D.M. Nelson, L. Watson, H. Wong, and B. Gemzik 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 2009 482 491
25. A. di Masi, E. De Marinis, P. Ascenzi, and M. Marino Nuclear receptors CAR and PXR: molecular, functional, and biomedical aspects Mol Aspects Med 30 2009 297 343
26. M. Qatanani, J. Zhang, and D.D. Moore Role of the constitutive androstane receptor in xenobiotic-induced thyroid hormone metabolism Endocrinology 146 2005 995 1002 (Pubitemid 40289286)
27. C. Chen, J.L. Staudinger, and C.D. Klaassen Nuclear receptor, pregname X receptor, is required for induction of UDP-glucuronosyltranferases in mouse liver by pregnenolone-16 alpha-carbonitrile Drug Metab Dispos 31 2003 908 915 (Pubitemid 36759061)
28. P.G. Curran, and L.J. DeGroot The effect of hepatic enzyme-inducing drugs on thyroid hormones and the thyroid gland Endocr Rev 12 1991 135 150
29. T. Kawamoto, S. Kakizaki, K. Yoshinari, and M. Negishi Estrogen activation of the nuclear orphan receptor CAR (constitutive active receptor) in induction of the mouse Cyp2b10 gene Mol Endocrinol 14 2000 1897 1905
30. K.H. Koh, S. Jurkovic, K. Yang, S.Y. Choi, J.W. Jung, and K.P. Kim Estradiol induces cytochrome P450 2B6 expression at high concentrations: implication in estrogen-mediated gene regulation in pregnancy Biochem Pharmacol 84 2012 93 103
31. C. Viollon-Abadie, D. Lassere, E. Debruyne, L. Nicod, N. Carmichael, and L. Richert Phenobarbital, beta-naphthoflavone, clofibrate, and pregnenolone-16alpha-carbonitrile do not affect hepatic thyroid hormone UDP-glucuronosyl transferase activity, and thyroid gland function in mice Toxicol Appl Pharmacol 155 1999 1 12 (Pubitemid 29102756)
32. T.A. Richardson, and C.D. Klaassen Disruption of thyroid hormone homeostasis in Ugt1a-deficient Gunn rats by microsomal enzyme inducers is not due to enhanced thyroxine glucuronidation Toxicol Appl Pharmacol 248 2010 38 44
33. C. Kohle, and K.W. Bock Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2 Biochem Pharmacol 73 2007 1853 1862 (Pubitemid 46677898)
34. P.C. Boutros, C.Q. Yao, J.D. Watson, A.H. Wu, I.D. Moffat, and S.D. Prokopec Hepatic transcriptomic responses to TCDD in dioxin-sensitive and dioxin-resistant rats during the onset of toxicity Toxicol Appl Pharmacol 251 2011 119 129
35. Q.T. Tran, L. Xu, V. Phan, S.B. Goodwin, M. Rahman, and V.X. Jin Chemical genomics of cancer chemopreventive dithiolethiones Carcinogenesis 30 2009 480 486