Efficient assessment of the utility of immortalized Fa2N-4 cells for cytochrome P450 (CYP) induction studies using multiplex quantitative reverse transcriptase-polymerase chain reaction (qRT-PCR) and substrate cassette methodologies

References

• Atkinson A, Kenny JR, Grime K. Automated assessment of time-dependent inhibition of human cytochrome P450 enzymes using liquid chromatography-tandem mass spectrometry analysis. Drug Metabolism and Disposition 2005; 33: 1637–1647
   PubMed Web of Science ®Google Scholar
• Berghard A, Gradin K, Pongratz I, Whitelaw M, Poellinger L. Cross-coupling of signal transduction pathways: The dioxin receptor mediates induction of cytochrome P-450IA1 expression via a protein kinase C-dependent mechanism. Molecular Cell Biology 1993; 13: 677–689
   PubMed Web of Science ®Google Scholar
• Castell JV, Jover R, Martinez-Jimenez CP, Gomez-Lechon MJ. Hepatocyte cell lines: Their use, scope and limitations in drug metabolism studies. Expert Opinion on Drug Metabolism and Toxicology 2006; 2: 183–212
   PubMed Web of Science ®Google Scholar
• Dickins M. Induction of cytochromes P450. Current Topics in Medicinal Chemistry 2004; 4: 1745–1766
   PubMed Web of Science ®Google Scholar
• Dixit V, Hariparsad N, Li F, Desai P, Thummel KE, Unadkat JD. Cytochrome P450 enzymes and transporters induced by anti-human immunodeficiency virus protease inhibitors in human hepatocytes: implications for predicting clinical drug interactions. Drug Metabolism and Disposition 2007; 35: 1853–1859
   PubMed Web of Science ®Google Scholar
• Drocourt L, Pascussi J-M, Assenat E, Fabre J-M, Maurel P, Vilarem M-J. Calcium channel modulators of the dihydropyridine family are human pregnane X receptor activators and inducers of CYP3A, CYP2B, and CYP2C in human hepatocytes. Drug Metabolism and Disposition 2001; 29: 1325–1331
   PubMed Web of Science ®Google Scholar
• Ernest CS II, Hall SD, Jones DR. Mechanism-based inactivation of CYP3A by HIV protease inhibitors. Journal of Pharmacology and Experimental Therapeutics 2005; 312: 583–591
   PubMed Web of Science ®Google Scholar
• Faucette SR, Sueyoshi T, Smith CM, Negishi M, LeCluyse EL, Wang H. Differential regulation of hepatic CYP2B6 and CYP3A4 genes by constitutive androstane receptor but not pregnane X receptor. Journal of Pharmacology and Experimental Therapeutics 2006; 317: 1200–1209
   PubMed Web of Science ®Google Scholar
• Faucette SR, Wang H, Hamilton GA, Jolley SL, Gilbert D, Lindley C, Yan B, Negishi M, LeCluyse EL. Regulation of CYP2B6 in primary human hepatocytes by prototypical inducers. Drug Metabolism and Disposition 2004; 32: 348–358
   PubMed Web of Science ®Google Scholar
• Faucette SR, Zhang T, Moore R, Sueyoshi T, Omiecinski CJ, LeCluyse EL, Negishi M, Wang H. Relative activation of human pregnane X receptor versus constitutive androstane receptor defines distinct classes of CYP2B6 and CYP3A4 inducers. Journal of Pharmacology and Experimental Therapeutics 2007; 320: 72–80
   PubMed Web of Science ®Google Scholar
• Hariparsad N, Carr BA, Evers R, Chu X. Comparison of immortalized Fa2N-4 cells and human hepatocytes as in vitro models for cytochrome P450 induction. Drug Metabolism and Disposition 2008; 36: 1046–1055
   PubMed Web of Science ®Google Scholar
• Hariparsad N, Nallani SC, Sane RS, Buckley DJ, Buckley AR, Desai PB. Induction of CYP3A4 by efavirenz in primary human hepatocytes: Comparison with rifampin and phenobarbital. Journal of Clinical Pharmacology 2004; 44: 1273–1281
   PubMed Web of Science ®Google Scholar
• Harmsen S, Koster A, Beijnen JH, Schellens JH, Meijerman I. Comparison of two immortalized human cell lines to study nuclear receptor mediated CYP3A4 induction. Drug Metabolism and Disposition 2008; 36: 1166–1171
   PubMed Web of Science ®Google Scholar
• Hewitt NJ, Lecluyse EL, Ferguson SS. Induction of hepatic cytochrome P450 enzymes: Methods, mechanisms, recommendations, and in vitro–in vivo correlations. Xenobiotica 2007a; 7: 1196–1224
   Google Scholar
• Hewitt NJ, Lechon MJ, Houston JB, Hallifax D, Brown HS, Maurel P, Kenna JG, Gustavsson L, Lohmann C, Skonberg C, et al. Primary hepatocytes: Current understanding of the regulation of metabolic enzymes and transporter proteins, and pharmaceutical practice for the use of hepatocytes in metabolism, enzyme induction, transporter, clearance, and hepatotoxicity studies. Drug Metabolism Reviews 2007b; 39: 159–234
   PubMed Web of Science ®Google Scholar
• Kanebratt KP, Andersson TB. HepaRG cells as an in vitro model for evaluation of cytochrome P450 induction in humans. Drug Metabolism and Disposition 2008; 36: 1137–1145
   Google Scholar
• Komoroski BJ, Zhang S, Cai H, Hutzler JM, Frye R, Tracy TS, Strom SC, Lehmann T, Ang CY, Cui YY, et al. Induction and inhibition of cytochromes P450 by the St. John's wort constituent hyperforin in human hepatocyte cultures. Drug Metabolism and Disposition 2004; 32: 512–518
   PubMed Web of Science ®Google Scholar
• LeCluyse E, Madan A, Hamilton G, Carroll K, DeHaan R, Parkinson A. Expression and regulation of cytochrome P450 enzymes in primary cultures of human hepatocytes. Journal of Biochemical and Molecular Toxicology 2000; 14: 177–188
   PubMed Web of Science ®Google Scholar
• LeCluyse EL. Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 expression and regulation. European Journal of Pharmaceutical Sciences 2001; 13: 343–368
   PubMed Web of Science ®Google Scholar
• Li AP, Reith MK, Rasmussen A, Gorski JC, Hall SD, Xu L, Kaminski DL, Cheng LK. Primary human hepatocytes as a tool for the evaluation of structure–activity relationship in cytochrome P450 induction potential of xenobiotics: Evaluation of rifampin, rifapentine and rifabutin. Chemico-Biological Interactions 1997; 107: 17–30
   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, et al. CYP3A4 induction by drugs: Correlation between a pregnane X receptor reporter gene assay and CYP3A4 expression in human hepatocytes. Drug Metabolism and Disposition 2002; 30: 795–804
   PubMed Web of Science ®Google Scholar
• Madan A, Graham RA, Carroll KM, Mudra DR, Burton LA, Krueger LA, Downey AD, Czerwinski M, Forster J, Ribadeneira MD, et al. Effects of prototypical microsomal enzyme inducers on cytochrome P450 expression in cultured human hepatocytes. Drug Metabolism and Disposition 2003; 31: 421–431
   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, et al. Identification of a novel human constitutive androstane receptor (CAR) agonist and its use in the identification of CAR target genes. Journal of Biological Chemistry 2003; 278: 17277–17283
   PubMed Web of Science ®Google Scholar
• Masubuchi Y. Metabolic and non-metabolic factors determining troglitazone hepatotoxicity: A review. Drug Metabolism and Pharmacokinetics 2006; 21: 347–356
   PubMed Web of Science ®Google Scholar
• McGinnity DF, Berry AJ, Kenny JR, Grime K, Riley RJ. Evaluation of time-dependent cytochrome P450 inhibition using cultured human hepatocytes. Drug Metabolism and Disposition 2006; 34: 1291–1300
   PubMed Web of Science ®Google Scholar
• Meneses-Lorente G, Pattison C, Guyomard C, Chesné C, Heavens R, Watt AP, Sohal B. Utility of long-term cultured human hepatocytes as an in vitro model for cytochrome p450 induction. Drug Metabolism and Disposition 2007; 35: 215–220
   PubMed Web of Science ®Google Scholar
• Meunier V, Bourrié M, Julian B, Marti E, Guillou F, Berger Y, Fabre G. Expression and induction of CYP1A1/1A2, CYP2A6 and CYP3A4 in primary cultures of human hepatocytes: A 10-year follow-up. Xenobiotica 2000; 30: 589–607
   PubMed Web of Science ®Google Scholar
• Mills JB, Rose KA, Sadagopan N, Sahi J, De Morais SM. Induction of drug metabolism enzymes and MDR1 using a novel human hepatocyte cell line. Journal of Pharmacology and Experimental Therapeutics 2004; 309: 303–309
   PubMed Web of Science ®Google Scholar
• Mohutsky MA, Petullo DM, Wrighton SA. The use of a substrate cassette strategy to improve the capacity and throughput of cytochrome P450 induction studies in human hepatocytes. Drug Metabolism and Disposition 2005; 33: 920–923
   PubMed Web of Science ®Google Scholar
• Nallani SC, Goodwin B, Buckley AR, Buckley DJ, Desai PB. Differences in the induction of cytochrome P450 3A4 by taxane anticancer drugs, docetaxel and paclitaxel, assessed employing primary human hepatocytes. Cancer Chemotherapy and Pharmacology 2004; 54: 219–229
   PubMed Web of Science ®Google Scholar
• Nishimura M, Koeda A, Suganuma Y, Suzuki E, Shimizu T, Nakayama M, Satoh T, Narimatsu S, Naito S. Comparison of inducibility of CYP1A and CYP3A mRNAs by prototypical inducers in primary cultures of human, cynomolgus monkey, and rat hepatocytes. Drug Metabolism and Pharmacokinetics 2007; 22: 178–186
   PubMed Web of Science ®Google Scholar
• Persson KP, Ekehed S, Otter C, Lutz ES, McPheat J, Masimirembwa CM, Andersson TB. Evaluation of human liver slices and reporter gene assays as systems for predicting the cytochrome P450 induction potential of drugs in vivo in humans. Pharmaceutical Research 2006; 23: 56–69
   PubMed Web of Science ®Google Scholar
• Ramachandran V, Kostrubsky VE, Komoroski BJ, Zhang S, Dorko K, Esplen JE, Strom SC, Venkataramanan R. Troglitazone increases cytochrome P-450 3A protein and activity in primary cultures of human hepatocytes. Drug Metabolism and Disposition 1999; 27: 1194–1199
   PubMed Web of Science ®Google Scholar
• Raucy JL. Regulation of CYP3A4 expression in human hepatocytes by pharmaceuticals and natural products. Drug Metabolism and Disposition 2003; 31: 533–539
   PubMed Web of Science ®Google Scholar
• Reinach B, De Sousa G, Dostert P, Ings R, Gugenheim J, Rahmani R. Comparative effects of rifabutin and rifampicin on cytochromes P 450 and UDP-glucuronosyltransferases expression in fresh and cryopreserved human hepatocytes. Chemico-Biological Interactions 1999; 121: 37–48
   PubMed Web of Science ®Google Scholar
• Riley RJ. The potential pharmacological and toxicological impact of P450 screening. Current Opinion on Drug Discovery and Development 2001; 4: 45–54
   PubMedGoogle Scholar
• Ripp SL, Mills JB, Fahmi OA, Trevena KA, Liras JL, Maurer TS, De Morais SM. Use of immortalized human hepatocytes to predict the magnitude of clinical drug–drug interactions caused by CYP3A4 induction. Drug Metabolism and Disposition 2006; 34: 1742–1748
   PubMed Web of Science ®Google Scholar
• Roymans D, Van Looveren C, Leone A, Parker JB, McMillian M, Johnson MD, Koganti A, Gilissen R, Silber P, Mannens G, et al. Determination of cytochrome P450 1A2 and cytochrome P450 3A4 induction in cryopreserved human hepatocytes. Biochemical Pharmacology 2004; 67: 427–437
   PubMed Web of Science ®Google Scholar
• Sahi J, Hamilton G, Sinz M, Barros S, Huang SM, Lesko LJ, LeCluyse EL. Effect of troglitazone on cytochrome P450 enzymes in primary cultures of human and rat hepatocytes. Xenobiotica 2000; 30: 273–284
   PubMed Web of Science ®Google Scholar
• Sinz M, Kim S, Zhu Z, Chen T, Anthony M, Dickinson K, Rodrigues AD. Evaluation of 170 xenobiotics as transactivators of human pregnane X receptor (hPXR) and correlation to known CYP3A4 drug interactions. Current Drug Metabolism 2006; 7: 375–388
   PubMed Web of Science ®Google Scholar
• Steen D. Immortalized human hepatocytes: A new advance in convenience and performance. Current Separations 2004; 20: 137–140
   Google Scholar
• Vermeir M, Annaert P, Mamidi RN, Roymans D, Meuldermans W, Mannens G. Cell-based models to study hepatic drug metabolism and enzyme induction in humans. Expert Opinion on Drug Metabolism and Toxicology 2005; 1: 75–90
   PubMedGoogle Scholar
• Wang H, LeCluyse EL. Role of orphan nuclear receptors in the regulation of drug-metabolising enzymes. Clinical Pharmacokinetics 2003; 42: 1331–1357
   PubMed Web of Science ®Google Scholar
• Weaver R, Graham K, Beatie IG, Riley RJ. Cytochrome P450 inhibition using recombinant proteins and mass spectrometry/multiple reaction monitoring technology in a cassette incubation. Drug Metabolism and Disposition 2003; 31: 955–966
   PubMed Web of Science ®Google Scholar
• Whitlock JP Jr. Induction of cytochrome P4501A1. Annual Review of Pharmacology and Toxicology 1999; 39: 103–125
   PubMed Web of Science ®Google Scholar
• Youdim KA, Tyman CA, Jones BC, Hyland R. Induction of cytochrome P450: Assessment in an immortalized human hepatocyte cell line (Fa2N-4) using a novel higher throughput cocktail assay. Drug Metabolism and Disposition 2007; 35: 275–282
   PubMed Web of Science ®Google Scholar