Cell-based systems to assess nuclear receptor activation and their use in drug development

References

• Allen SW, Mueller L, Williams SN, Quattrochi LC, Raucy JL (2001) The use of a high volume screening procedure to assess the effects of dietary flavonoids on human CYP1A1 expression. Drug Metabolism and Disposition 29:1074–1079.
   PubMed Web of Science ®Google Scholar
• Auerbach SS, Ramsden R, Stoner MA, Verlinde C, Hassett C, Omiecinski CJ (2003) Alternatively spliced isoforms of the human constitutive androstane receptor. Nucl Acids Res 31:3194–3207.
   PubMed Web of Science ®Google Scholar
• Auerbach SS, Stoner MA, Shengzhong S, Omiecinski CJ (2005) Retinoid X Receptor -a-dependent transactivation by a naturraly occurring structural variant of human constitutive androstane receptor (NR1I3). Mol Pharmacol 68:1239–1253.
   PubMed Web of Science ®Google Scholar
• Barbier O, Duran-Sandocal D, Pineda-Torra I, Kosykh V, Fruchart JC, Staels B (2003) Peroxisome Proliferator-activated Receptor alpha Induces Hepatic Expression of the Human Bile Acid Glucuronidating UDP-glucuronosyltransferase 2B4 Enzyme. The Journal of Biological Chemistry 278:32852–32860.
   PubMed Web of Science ®Google Scholar
• Barbier O, Fontaine C, Fruchart J, Staels B (2004) Genomic and non-genomic interactions of PPARalpha with xenobiotic-metabolizing enzymes. Trends Endocrinol Metab 15:324–330.
   PubMed Web of Science ®Google Scholar
• Bradfield CA Bjeldanes LF (1987) Structure-activity relationships of dietary indoles: a proposed mechanism of action as modifiers of xenobiotic metabolism. JToxicolEnvironHealth 21:311–323.
   Web of Science ®Google Scholar
• Chambon P (2005) The nuclear receptor superfamily: a personal retrospect on the first two decades. Mol Endocrinol 19:1418–1428.
   PubMed Web of Science ®Google Scholar
• Chen T, Xie W, Agler M, Banks M (2003) Coactivators in assay design for nuclear hormone receptor drug discovery. Assay and Drug Development Tech 1:835–842.
   PubMed Web of Science ®Google Scholar
• Chu V, Einolf HJ, Evers R, Kumar G, Moore D, Ripp SL, Silva J, Sinha V, Sinz M, Skerjanec A (2009) In Vitro and in Vivo induction of cytochrome P450: A survey of the current practices and recommendations: A Pharmaceutical Research and Manufacturers of America Perspective. Drug Met Disp 37:1339–1354.
   PubMed Web of Science ®Google Scholar
• Ciolino HP, Daschner PJ, Wang TT, Yeh GC (1998) Effect of curcumin on the aryl hydrocarbon receptor and cytochrome P450 1A1 in MCF-7 human breast carcinoma cells. Biochem Pharmacol 56:197–206.
   PubMed Web of Science ®Google Scholar
• Daujat M, Peryt B, Lesca P, Fourtanier G, Domergue J, Maurel P (1992) Omeprazole, an inducer of human CYP1A1 and 1A2, is not a ligand for the Ah receptor. Biochemical and Biophysical Research Communications 188:820–825.
   PubMed Web of Science ®Google Scholar
• Denison MS Whitlock JP, Jr. (1995) Xenobiotic-inducible transcription of cytochrome P450 genes. Journal of Biological Chemistry 270:18175–18178.
   PubMed Web of Science ®Google Scholar
• di Masi A, De Marinis E, Ascenzi P, Marino M (2009) Nuclear Receptors CAR and PXR: Molecular, functional, and biomedical aspects. Mol Aspects Med 30:297–343.
   PubMed Web of Science ®Google Scholar
• Ding X Staudinger J (2005) Induction of drug metabolism by Forskolin: The role of the pregnane X receptor and the protein kinase A signal transduction pathway. J Pharmacol Exp Therap 312:849–856.
   PubMed Web of Science ®Google Scholar
• Dussault I Forman B (2002) The nuclear receptor PXR: A master regulator of “homeland” defense. Crit RevEukaryotic Gene Expression 12:53–64.
   PubMed Web of Science ®Google Scholar
• Ekins S, Kortagere S, Iyer M, Reschly EJ, Lill MA, Redinbo MR, Krasowski MD (2009) Challenges predicting ligand-receptor interactions of promiscuous proteins: The nuclear receptor PXR. PLos Computational Biol 5:1–12.
   Web of Science ®Google Scholar
• Fahmi O, Kish M, Boldt S, Obach R (2010) Cytochrome P450 3A4 mRNA is a more reliable marker than CYP3A4 activity for detecting pregnane X receptor-activated induction of drug metabolizing enzymes. Drug Metab Disp 38:1605–1611.
   PubMed Web of Science ®Google Scholar
• Fahmi O, Raucy J, Ponce E, Hassanali S, Lasker J (2012) The utility of DPX2 cells for predicting CYP3A induction-mediated drug-drug interactions and associated structure-activity relationships. Drug Met Disp.
   PubMed Web of Science ®Google Scholar
• Fahmi O Ripp S (2010) Evaluation of models for predicting drug-drug interactions due to induction. Exp Opinion Drug Metab Toxicol 6:1399–1416.
   PubMed Web of Science ®Google Scholar
• Ferguson S, LeCluyse E, Negishi M, Goldstein J (2002) Regulation of huyman CYP2C9 by the constitutive androstane receptor: Discovery of a new distal binding site. Mol Pharmacol 62:737–746.
   PubMed Web of Science ®Google Scholar
• Fitzgerald CT, Fernandez-Salguero P, Gonzalez FJ, Nebert DW, Puga A (1996) Differential regulation of mouse Ah receptor gene expression in cell lines of different tissue origins. Arch Biochem Biophys 333:170–178.
   PubMed Web of Science ®Google Scholar
• Fuhr U, Woodcock BG, Siewert M (1992) Verapamil and drug metabolism by the cytochrome P450 isoform CYP1A2. European Journal of Clinical Pharmacology 42:463–464.
   PubMed Web of Science ®Google Scholar
• Gerbal-Chaloin S, Pascussi JM, Pichard-Garcia L, Daujat M, Waechter F, Fabre JM, Carrere N, Maurel P (2001) Induction of CYP2C genes in human hepatocytes in primary culture, in: Drug Metabolism and Disposition, pp 242–251.
   PubMed Web of Science ®Google Scholar
• Goodwin B, Moore LB, Stoltz CM, McKee DD, Kliewer SA (2001) Regulation of the human CYP2B6 gene by the nuclear pregnane X receptor. MolPharmacol 60:427–431.
   PubMed Web of Science ®Google Scholar
• Gu L, Gonzalez FJ, Kalow W, Tang BK (1992) Biotransformation of caffeine, paraxanthine, theobromine and theophylline by cDNA-expressed human CYP1A2 and CYP2E1. Pharmacogenetics 2:73–77.
   PubMedGoogle Scholar
• Hankinson O (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307–340.
   PubMed Web of Science ®Google Scholar
• Heath-Pagliuso S, Rogers WJ, Tullis K, Seidel SD, Cenijn PH, Brouwer A, Denison MS (1998) Activation of the Ah receptor by tryptophan and tryptophan metabolites. Biochemistry 37:11508–11515.
   PubMed Web of Science ®Google Scholar
• Hewitt N, Gomez-Lechen J, Houston J, Hallifax D, Brown H, Maurel P, Kenna J, Gustavsson L, Lohmann C, Skonberg C, Guillouzo A, Tuschi G, Li A, LeCluyse E, Groothuis G, Hengstler J (2007) Primary hepatocytes: current understanding of the regulation of metabolic enzymes and transporter proteins, and pharmaceutical practice for the use of hepatocyte in metabolism, enzyme induction, transporter, clearance and heaptotoxicity studies. Drug Metab Rev 39:159–234.
   PubMed Web of Science ®Google Scholar
• Honkakoski P, JÑÑskelÑinen I, Kortelahti M, Urtti A (2001) A novel drug-regulated gene expression system based on the nuclear receptor constitutive androstane receptor (CAR). Pharmaceutical Research 18:146–150.
   PubMed Web of Science ®Google Scholar
• Honkakoski P Negishi M (2000) Regulation of cytochrome P450 (CYP) genes by nuclear receptors. Biochemical Journal 347:321–337.
   PubMed Web of Science ®Google Scholar
• IJpenberg A, Jeannin E, Wahli W, Desvergne B. (1997) Polarity and specific sequence requirements of peroxisome proliferator-activated receptor (PPAR)/retinoid X receptor heterodimer binding to DNA. A functional analysis of the malic enzyme gene PPAR response element. J Biol Chem 272:20108–20117.
   PubMed Web of Science ®Google Scholar
• Juge-Aubry C, Pernin A, Favez T, Burger AG, Wahli W, Meier CA Desvergne B (1997) DNA binding properties of peroxisome proliferator-activated receptor subtypes on various natural peroxisome proliferator response elements. Importance of the 5′-flanking region. J Biol Chem 272:25252–25259.
   PubMed Web of Science ®Google Scholar
• Kast HR, Goodwin B, Tarr PT, Jones SA, Anisfeld AM, Stoltz CM, Tontonoz P, Kliewer SA, Willson TM, Edwards PA (2002) Regulation of multidrug resistance-associated protein 2 (MRP2;ABCC2) by the nuclear receptors pregnane X receptor, farnesoid X-activated receptor, and constitutive androstane receptor. Journal of Biological Chemistry 277:2908–2915.
   PubMed Web of Science ®Google Scholar
• Kawajiri K Fuji-Kuriyama Y (2007) Cytochrome P450 regulation and physiological functions mediated by the aryl hydrocarbon receptor. Arch Biochem Biophys 464:207.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Lee SK, Na SY, Choi HS, Lee JW (1998) Molecular cloning of xSRC-3, a novel transcription coactivator from Xenopus, that is related to AIB1, p/CIP, and TIF2. Mol Endocrinol 512:1038–1047.
   Google Scholar
• Kliewer SA, Moore JT, Wade L, Staudinger JL, Watson MA, Jones SA, McKee DD, Oliver BB, Willson TM, Zetterstrom RH, Perlmann T, Lehmann JM (1998) An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell 92:73–82.
   PubMed Web of Science ®Google Scholar
• Kuljukka T, Vaaranrinta R, Veidebaum T, Sorsa M, Peltonen K (1996) Exposure to PAH compounds among cokery workers in the oil shale industry. EnvironHealth Perspect 104:539–541.
   PubMed Web of Science ®Google Scholar
• Kumar RaT EB (1999) The structure of the nuclear hormone receptors. Steroids 64:310–319.
   PubMed Web of Science ®Google Scholar
• Lehmann JM, McKee DD, Watson MA, Willson TM, Moore JT, Kliewer SA (1998) The human orphan nuclear receptor PXR is activated by compounds that regulate CYP3A4 gene expression and cause drug interactions. J Clin Invest 102:1016–1023.
   PubMed Web of Science ®Google Scholar
• Lemaire G, De Sousa G, Rahmani R (2004) A PXR reporter gene assay in a stable cell culture system: CYP3A4 and CYP2B6 induction by pesticides. Biochem Pharmacol 68:2347–2358.
   PubMed Web of Science ®Google Scholar
• Lemoine A, Gautier JC, Azoulay D, Kiffel L, Belloc C, Guengerich FP, Maurel P, Beaune P, Leroux JP (1993) Major pathway of imipramine metabolism is catalyzed by cytochromes P450 1A2 and P4503A4 in human liver. MolPharmacol 43:827–832.
   PubMed Web of Science ®Google Scholar
• Luo G, Cunningham M, Kim S, Burn T, Lin J, Sinz M, Hamilton G, Rizzo C, Jolley S, Gilbert D, Downey A, Mudra D, Graham R, Carroll K, Xie J, Madan A, Parkinson A, Christ D, Selling B, LeCluyse E, Gan LS (2002) CYP3A4 induction by drugs: correlation between a pregnane X receptor reporter gene assay and CYP3A4 expression in human hepatocytes. Drug Metabolism and Disposition 30:795–804.
   PubMed Web of Science ®Google Scholar
• Madsen H, Rasmussen BB, Brosen K (1997) Imipramine demethylation in vivo: Impact of CYP1A2, CYP2C19, and CYP3A4. Clinical Pharmacology and Therapeutics 61:319–324.
   PubMed Web of Science ®Google Scholar
• Maglich JM, Parks DJ, Moore LB, Collins JL, Goodwin B, Billin AN, Stoltz CA, Kliewer SA, Lambert MH, Willson TM, Moore JT (2003) Identification of a novel human CAR agonist and its use in the identification of CAR target genes. Journal of Biological Chemistry 278:17277–17283.
   PubMed Web of Science ®Google Scholar
• Maglich JM, Stoltz CM, Goodwin B, Hawkins-Brown D, Moore JT, Kliewer SA (2002) Nuclear Pregnane X receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. MolPharmacol 62:638–646.
   PubMed Web of Science ®Google Scholar
• Mangelsdorf D, Evans RM (1995) The RXR heterodimers and orphan receptors. Cell 83:841–850.
   PubMed Web of Science ®Google Scholar
• Moore J, Kliewer SA (2000) Use of the nuclear receptor PXR to predict drug interactions. Toxicology 153:1–10.
   PubMed Web of Science ®Google Scholar
• Moore LB, Maglich JM, McKee DD, Wisely B, Willson TM, Kliewer SA, Lambert MH, Moore JT (2002) Pregnane X receptor (PXR), constitutive androstane receptor (CAR), and benzoate X receptor (BXR) define three pharmacologically distinct classes of nuclear receptors. Molecular Endocrinology 16:977–986.
   PubMed Web of Science ®Google Scholar
• Moore LB, Parks DJ, Jones SA, Bledsoe RK, Consler TG, Stimmel JB, Goodwin B, Liddle C, Blanchard SG, Willson TM, Collins JL, Kliewer SA (2000) Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. Journal of Biological Chemistry 275:15122–15127.
   PubMed Web of Science ®Google Scholar
• Muangmoonchai R, Smirlis D, Wong SC, Edwards M, Phillips IR, Shephard EA (2001) Xenobiotic induction of cytochrome P4502B1 (CYP2B1) is mediated by the orphan nuclear receptor constitutive androstane receptor (CAR) and requires steroid co-activator 1 (SRC-1) and the transcription factor Sp1. Biochemical Journal 355:71–78.
   PubMed Web of Science ®Google Scholar
• Muerhoff AS, Griffin KJ, Johnson EF (1992) The Peroxisome Proliferator-activated receptor mediates the induction of CYP4A6, a cytochrome P450 fatty acid w-hydroxylase, by clofibric acid. J Biol Chem 267:19051–19053.
   PubMed Web of Science ®Google Scholar
• Mutoh S, Osabe M, Inoue K, Moore R, Pedersen L, Perera L, Rebolloso Y, Sueyoshi T, Negishi M (2009) Dephosphorylation of threonine 38 is required for nuclear translocation and activation of human xenobiotic receptor CAR (NR1I3). J Biol Chem 284:34785–34792.
   PubMed Web of Science ®Google Scholar
• Omiecinski C, Vanden Heuvel J, Perdew G, Peters J (2011) Xenobiotic Metabolism, Disposition, and regulation by receptors: From Biochemical phenomenon to predictors of major toxicities. Toxicol Sci 120:S49–S75.
   PubMed Web of Science ®Google Scholar
• Pastrakuljic A, Tang BK, Roberts EA, Kalow W (1997) Distinction of CYP1A1 and CYP1A2 activity by selective inhibition using fluvoxamine and isosafrole. BiochemPharmacol 53:531–538.
   PubMed Web of Science ®Google Scholar
• Peraza M, Burdick A, Marin H, Gonzalez F, Peters J (2006) The toxicology of ligands for peroxisome proliferator-activated receptors (PPAR). Toxicol Sci 90:269–295.
   PubMed Web of Science ®Google Scholar
• Phelan D, Winter GM, Rogers WJ, Lam JC, Denison MS (1998a) Activation of the Ah receptor signal transduction pathway by bilirubin and biliverdin. ArchBiochemBiophys 357:155–163.
   PubMed Web of Science ®Google Scholar
• Phelan DM, Brackney WR, Denison MS (1998b) The Ah receptor can bind ligand in the absence of receptor-associated heat-shock protein 90. ArchBiochemBiophys 353:47–54.
   PubMed Web of Science ®Google Scholar
• Quattrochi LC Tukey RH (1989) The human cytochrome CYP1A2 gene contains regulatory elements responsive to 3-methylcholanthrene. Molecular Pharmacology 36:66–71.
   PubMed Web of Science ®Google Scholar
• Raucy J Lasker J (2010) Current In Vitro high throughput screening approaches to assess nuclear receptor activation. Current Drug Metab 11:806–814.
   PubMed Web of Science ®Google Scholar
• Raucy J, Mueller L, Kuan K, Allen S, Strom S, Lasker J (2002a) Exoression and induction of CYP2C P450 enzymes in primary cultures of human hepatocytes. J Pharmacol Exp Ther 302:475–482.
   PubMed Web of Science ®Google Scholar
• Raucy JL, Warfe L, Yueh MF, Allen SW (2002b) A cell-based reporter gene assay for determining induction of CYP3A4 in a high volume system. J Pharmacol Exp Ther 303:412–423.
   PubMed Web of Science ®Google Scholar
• Shukla SJ, Nguyen D-T, MacArhur R, Simeonov A, Frazee WJ, Hallis TM, Marks BD, Singh U, Eliason HC, Printen J, Austin CP, Inglese J, Auld DS (2009) Identification of Pregnane X Receptor Ligands using time-resolved fluorescence resonance energy transfer and quantitative high-throughput screening. Assay and Drug Development Tech 7:143–169.
   PubMed Web of Science ®Google Scholar
• Shukla SJ, Sakamuru S, Huang R, Moeller TA, Shinn P, Van Leer D, Auld DS, Austin CP, Xia M (2011) Identification of clinically utilized drugs that activate pregnane X receptors. Drug Met Disp 39:151–159.
   PubMed Web of Science ®Google Scholar
• Sinz M, Kim S, Zhu Z, Chen T, Anthony M, Dickinson K, Rodrigues AD (2006) Evaluation of 170 xenobiotics as transactivators of human pregnane X receptor (hPXR) and correlation to known to CYP3A4 drug interactions. Curr Drug Metab 7:375–388.
   PubMed Web of Science ®Google Scholar
• Sinz M, Pray D, Raucy J (2007) The utility of stable cell lines to assess species differences in PXR transactivation. Drug Metab Lett 1:147–152.
   PubMedGoogle Scholar
• Stanley LA, Horsburgh BC, Ross J, Scheer N, Wolf CR (2006) PXR and CAR: Nuclear receptors which play a pivotal role in drug disposition and chemical toxicity. Drug MetRev 38:515–597.
   PubMed Web of Science ®Google Scholar
• Sueyoshi T, Kawamoto T, Zelko I, Honkakoski P, Negishi M (1999a) The repressed nuclear receptor CAR responds to phenobarbital in activating the human CYP2B6 gene. Journal of Biological Chemistry 274:6043–6046.
   PubMed Web of Science ®Google Scholar
• Sueyoshi T, Kawamoto T, Zelko I, Honkakoski P, Negishi M (1999b) The repressed nuclear receptor CAR responds to phenobarbital inactivating the human CYP2B6 gene. J Biol Chem 274:6043–6046.
   PubMed Web of Science ®Google Scholar
• Sueyoshi T Negishi M (2001) Phenobarbital response elements of cytochrome P450 genes and nuclear receptors. Annual Review of Pharmacology and Toxicology 41:123–143.
   PubMed Web of Science ®Google Scholar
• Synold T, Dussault I, Forman B (2001) The orphan nuclear receptor SXR coordinately regulates drug metabolism and efflux. Nature Medicine 7:584–590.
   PubMed Web of Science ®Google Scholar
• Trubetskoy OV, Marks BD, Zielinski T, Yueh MF, Raucy J (2005) A simultaneous assessment of CYP3A4 metabolism and induction in the DPX2 cell line. AAPS J 7:E6-E13.
   PubMed Web of Science ®Google Scholar
• Tzameli I, Pissios P, Schuetz EG, Moore DD (2000) The Xenobiotic Compound 1,4-Bis[2-(3,5-Dicholorpyridyloxy)] Benzene Is an Agonist Ligand for the Nuclear Receptor CAR. Molecular and Cellular Biology 20:2951–2958.
   PubMed Web of Science ®Google Scholar
• Ueda A, Hamadeh HK, Webb HK, Yamamoto Y, Sueyoshi T, Afshari CA, Lehmann JM, Negishi M (2002) Diverse roles of the nuclear orphan receptor CAR in regulating hepatic genes in response to phenobarbital. MolPharmacol 61:1–6.
   PubMed Web of Science ®Google Scholar
• Urquhart BL, Tirona RG, Kim RB (2007) Nuclear receptors and the regulation of drug-metabolizing enzymes and drugtransporters: Implications for interindividual variability in response to drugs. Journal of Clinical Pharmacology 47:566–578.
   PubMed Web of Science ®Google Scholar
• Vanden Heuvel J (2004) Diet, fatty acids, and regulation of genes important for heart disease. Curr AtherosclerResp 6:432–440.
   PubMedGoogle Scholar
• Vignati LA, Bogni A, Grossi P, Monshouwer M (2004) A human and mouse pregnane X receptor reporter gene assay in combination with cytotoxicity measurements as a tool to evaluate species-specific CYP3A induction. Toxicology 199:23–33.
   PubMed Web of Science ®Google Scholar
• Watkins RE, Wisely GB, Moore LB, Collins JL, Lambert MH, Williams SP, Willson TM, Kliewer SA, Redinbo MR (2001) The human nuclear xenobiotic receptor PXR: Structural determinants of directed promiscuity. Science 292:2329–2333.
   PubMed Web of Science ®Google Scholar
• Wei P, Zhang J, Egan-Hafley M, Liang SG, Moore DD (2000) The nuclear receptor CAR mediates specific xenobiotic induction of drug metabolism. Nature 407:920–923.
   PubMed Web of Science ®Google Scholar
• Xia J Kemper B (2004) Structural determinants of CAR required for its GRIP1-mediated nuclear accumulation. J Biol Chem.
   Google Scholar
• Xie W, Barwick J, Simon C, Pierce AM, Safe S, Blumberg B, Guzelian PS, Evans RM (2000) Reciprocal activation of xenobiotic response genes by nuclear receptors SXR/PXR and CAR. Genes Dev 14:3014–3023.
   PubMed Web of Science ®Google Scholar
• Xie W, Yueh M, Radominska-Pandya A, Saini S, Negishi Y, Bottroff B, Cabrera G, Tukey R, Evans R (2003) Control of steroid, heme, and crcinogen metabolism by nuclear pregnane X receptor and constitutive androstane receptor. ProcNatl Acad Sci 100:4150–4155.
   PubMed Web of Science ®Google Scholar
• Xiong H, Yoshinari K, Brouwer K, Negishi M (2002) Role of constitutive androstane receptor in the in vivo induction of mrp3 and CYP2V1/2 by pehnobarbital. Drug Metab Disp 30:918–923.
   PubMed Web of Science ®Google Scholar
• Yueh MF, Kawahara M, Raucy J (2004) Cell-based high-throughput bioassays to assess induction and inhibition of CYP1A enzymes. Molecular and Cellular Toxicology.
   Google Scholar
• Yueh MF, Kawahara M, Raucy JL (2005a) Cell-based high-througput bioassays to assess induction and inhibition of CYP1A enzymes. ToxicolIn Vitro 19:275–287.
   PubMed Web of Science ®Google Scholar
• Yueh MF, Kawahara M, Raucy JL (2005b) High volume bioassays to assess CYP3A4-mediated drug interactions: induction and inhibition in a single cell line. Drug Metabolism and Disposition 33:38–48.
   PubMed Web of Science ®Google Scholar
• Zhang J-H, Chung TDY, Oldenburg KR (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screening 4:67–73.
   PubMed Web of Science ®Google Scholar
• Zhou C, Verma S, Blumberg B (2009) The steroid and xenobiotic receptor (SXR), beyond xenobiotic metabolism. Nuclear Receptor Signaling 7:1–21.
   PubMedGoogle Scholar