Ochratoxin A induces CYP3A4, 2B6, 3A5, 2C9, 1A1, and CYP1A2 gene expression in primary cultured human hepatocytes: a possible activation of nuclear receptors

References

• Bendele, A. M., Carlton, W. W., Krogh, I., Lillehoj, E. B. (1985). Ochratoxin A carcinogenesis in the (C57BL/6JXC3H) Fl mouse. Natl Cancer Inst 75:733–739.
   Google Scholar
• Boorman, G. A., McDonald, M. R., Imoto, S., Persing, R. (1992). Renal lesions induced by ochratoxin A exposure in the F344 rat. Toxicol Pathol 20:236–245.
   PubMed Web of Science ®Google Scholar
• Castegnaro, M., Mohr, U., Pfohl-Leszkowicz, A., Estève, J., Steinmann, J., Tillmann, T., et al. (1998). Sex- and strain-specific induction of renal tumors by ochratoxin A in rats correlates with DNA adduction. Int J Cancer 77:70–75.
   PubMed Web of Science ®Google Scholar
• Chu, F. S. (1971). Interaction of ochratoxin A with bovine serum albumin. Arch Biochem Biophys 147:359–366.
   PubMed Web of Science ®Google Scholar
• Chu, F. S. (1974). A comparative study of the interaction of ochratoxins with bovine serum albumin. Biochem Pharmacol 23:1105–1107.
   PubMed Web of Science ®Google Scholar
• Clark, H. A., Snedeker, S. M. (2006). Ochratoxin A: its cancer risk and potential for exposure. J Toxicol Environ Health B Crit Rev 9:265–296.
   PubMed Web of Science ®Google Scholar
• Dahlman, A., Dantzker, W. H., Silbernagl, S., Gekle, M. (1998). Detailed mapping of ochratoxin A reabsorption along the rate nephron in vivo: the nephrotoxin can be reabsorbed in all nephron segments by different mechanisms. J Pharmacol Exp Ther 286:157–162.
   PubMed Web of Science ®Google Scholar
• Davarinos, N. A., Pollenz, R. S. (1999). Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytosplasmic proteasome following nuclear export. J Biol Chem 274:28708–28715.
   PubMed Web of Science ®Google Scholar
• Dickins, M. (2004). Induction of cytochromes P450. Curr Top Med Chem 4:1745–1766.
   PubMed Web of Science ®Google Scholar
• EFSA. (2006). Opinion of the CONTAM Panel related to ochratoxin A in food. EFSA-Q-2005 154.
   Google Scholar
• El Adlouni, C., Pinelli, E., Azémar, B., Zaoui, D. (2000). Role of CYP 2C and microsomal glutathione-S-transferase in modulating susceptibility to ochratoxin A genotoxicity. Environ Mol Mutagen 35:123–131.
   PubMed Web of Science ®Google Scholar
• Ester, T., Jayyosi, Z., Creppy, E. E., El Amri, H. S., Batt, A. M. (1991). Characterization of pig liver purified cytochrome P-450 isoenzymes for ochratoxin A metabolism studies. Toxicol Lett 57:203–214.
   PubMed Web of Science ®Google Scholar
• Fink-Gremmels, J. (2005). Conclusions from the workshops on ochratoxin A in food: recent developments and significance, organized by ILSI Europe in Baden (Austria), 29 June-1 July. Food Addit Contam 22(Suppl. 1):1–5.
   PubMedGoogle Scholar
• Frank, C., Makkonen, H., Dunlop, T. W., Matilainen, M., Väisänen, S., Carlberg, C. (2005). Identification of pregnane X receptor binding sites in the regulatory regions of genes involved in bile acid homeostasis. J Mol Biol 346:505–519.
   PubMed Web of Science ®Google Scholar
• Fuchs, R., Radic, B., Peraica, M., Hult, K., Plestina, R. (1988). Enterohepatic circulation of ochratoxin A in rats. Period Biol 90:39–42.
   Web of Science ®Google Scholar
• Galtier, P., Baradat, C., Alvinerie, M. (1977). Etude d’élimination d’ochratoxin A par le lait chez la lapine. Ann Nutr Alim 31:911–918.
   PubMedGoogle Scholar
• Gautier, J. C., Holzhaeuser, D., Markovic, J., Gremaud, E., Schilter, B., Turesky, R. J. (2001). Oxidative damage and stress response from ochratoxin A exposure in rats. Free Radic Biol Med 30:1089–1098.
   PubMed Web of Science ®Google Scholar
• Gerbal-Chaloin, S., Pascussi, J. M., Pichard-Garcia, L., Daujat, M., Waechter, F., Fabre, J. M., et al. (2001). Induction of CYP2C genes in human hepatocytes in primary culture. Drug Metab Dispos 29:242–251.
   PubMed Web of Science ®Google Scholar
• Gillman, I. G., Clark, T. N., Manderville, R. A. (1999). Oxidation of ochratoxin A by an Fe-porphyrin system: model for enzymatic activation and DNA cleavage. Chem Res Toxicol 12:1066–1076.
   PubMed Web of Science ®Google Scholar
• Gomez-Lechon, M. J., Donato, M. T., Castell, J. V., Jover, R. (2003). Human hepatocytes as a tool for studying toxicity and drug metabolism. Curr Drug Metab 4:292–312.
   PubMed Web of Science ®Google Scholar
• Goodwin, B., Hodgson, E., Liddle, C. (1999). The orphan human pregnane X receptor mediates the transcriptional activation of CYP3A4 by rifampicin through a distal enhancer module. Mol Pharmacol 56:1329–1339.
   PubMed Web of Science ®Google Scholar
• Goodwin, B., Moore, J. T. (2004). CAR: detailing new models. Trends Pharmacol Sci 25:437–441.
   PubMed Web of Science ®Google Scholar
• Graham, M. J., Lake, B. G. (2008). Induction of drug metabolism: species differences and toxicological relevance. Toxicology 254:184–191.
   PubMed Web of Science ®Google Scholar
• Grosse, Y., Baudrimont, I., Castegnaro, M., Creppy, E. E. (1995). Ochratoxin A metabolites and DNA-adducts formation in monkey kidney cell. Chem Biol Interact 95:175–187.
   PubMed Web of Science ®Google Scholar
• Gross-Steinmeyer, K., Weymann, J., Hege, H. G., Metzler, M. (2002). Metabolism and lack of DNA reactivity of the mycotoxin ochratoxin A in cultured and human primary hepatocytes. J Agric Food Chem 50:935–938.
   Web of Science ®Google Scholar
• Guengerich, F. P., Parikh, A., Turesky, R. J., Josephy, P. D. (1999). Inter-individual differences in the metabolism of environmental toxicants: cytochrome P450 1A2 as a prototype. Mut Res 428:115–124.
   PubMed Web of Science ®Google Scholar
• Hagelberg, S., Hult, K., Fuchs, R. (1989). Toxicokinetics of ochratoxin A in several species and its plasma-binding properties. J Appl Toxicol 9:91–96.
   PubMed Web of Science ®Google Scholar
• Hahn, M. E. (2002). Aryl hydrocarbon receptors: diversity and evolution. Chem Biol Interact 141: 131–160.
   PubMed Web of Science ®Google Scholar
• Hassen, W., Ayed-Boussema, I., Bouslimi, A., Bacha, H. (2007). Heat shock proteins (Hsp 70) response is not systematic to cell stress: case of the mycotoxin ochratoxin A. Toxicology 242:63–70.
   PubMed Web of Science ®Google Scholar
• Hewitt, N. J., LeCluyse, E. L., Ferguson, S. S. (2007a). Induction of hepatic cytochrome P450 enzymes: methods, mechanisms, recommendations, and in vitro–in vivo correlations. Xenobiotica 37:1196–1224.
   PubMed Web of Science ®Google Scholar
• Hewitt, N. J., Gómez Lechon, M. J., Houston, J. B., Hallifax, D., Brown, H. S., Maurel, P., et al. (2007b). 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 Metab Rev 39:159–234.
   PubMed Web of Science ®Google Scholar
• Hietanen, E., Malaveille, C., Camus, A. M., Bereziate, J. C., Brun, G., Castegnaro, M., et al. (1986). Interstrain comparison of hepatic and renal microsomal carcinogen metabolism and liver S9 mediated mutagenicity in DA and Lewis rats phenotyped as poor and extensive metabolizers of debrisoquine. Drug Metab Dispos 14:118–126.
   PubMed Web of Science ®Google Scholar
• IARC.(1993). IARC monographs on the evaluation of carcinogenic risks to humans: some naturally occurring substances, food items and constituents, heterocyclic aromatic amines and mycotoxins, ochratoxin A, vol. 56, pp. 26–32). Geneva: International Agency for Research on Cancer.
   Google Scholar
• Isom, H. C., Secott, T., Georgoff, I., Woodworth, C., Mummaw, J. (1985). Maintenance of differentiated rat hepatocytes in primary culture. Proc Natl Acad Sci U S A 82:3252–3256.
   PubMed Web of Science ®Google Scholar
• Kane, A., Creppy, E. E., Roth, A., Schenthaler, R., Dirheimer, G. (1986). Distribution of the [3H]-label from low doses of radioactive ochratoxin A ingested by rats, and evidence for DNA single-strand breaks caused in liver and kidneys. Arch Toxicol 58:219–224.
   PubMed Web of Science ®Google Scholar
• Kanebratt, K. P., Andersson, T. B. (2008). Evaluation of HepaRG cells as an in vitro model for human drug metabolism studies. Drug Metab Dispos 36:1444–1452.
   PubMed Web of Science ®Google Scholar
• Kawamoto, T., Sueyoshi, T., Zelko, I., Moore, R., Washburn, K., Negishi, M. (1999). Phenobarbital-responsive nuclear translocation of the receptor CAR in induction of the CYP2B gene. Mol Cell Biol 19:6318–6322.
   PubMed Web of Science ®Google Scholar
• Kim, J., Min, G., Kemper, B. (2001). Chromatin assembly enhances binding to the CYP2B1 phenobarbital-responsive unit (PBRU) of nuclear factor-1, which binds simultaneously with constitutive androstane receptor (CAR)/retinoid X receptor (RXR) and enhances CAR/RXR-mediated activation of the PBRU. J Biol Chem 276:7559–7567.
   PubMed Web of Science ®Google Scholar
• Kliewer, S. A., Goodwin, B., Willson, T. M. (2002). The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr Rev 23:687–702.
   PubMed Web of Science ®Google Scholar
• Kuiper-Goodman, T., Scott, P. M. (1989). Risk assessment of the mycotoxin ochratoxin A. Biomed Environ Sci 2:179–248.
   PubMedGoogle Scholar
• Kumagai, S., Aibara, K. (1982). Intestinal absorption and secretion of ochratoxin A in the rat. Toxicol Appl Pharmacol 64:94–102.
   PubMed Web of Science ®Google Scholar
• LeCluyse, E. L. (2001). Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 expression and regulation. Eur J Pharm Sci 13:343–368.
   PubMed Web of Science ®Google Scholar
• Leszkowicz, A. P., Manderville, R. A. (2007). Ochratoxin A: an overview on toxicity and carcinogenicity in animals and humans. Mol Nutr Food Res 51:61–99.
   PubMed Web of Science ®Google Scholar
• Li, S., Marquardt, R. R., Frohlich, A. A., Vitti, T. G., Crow, G. (1997). Pharmacokinetics of ochratoxin A and its metabolites in rats, Toxicol Appl Pharmacol 145:82–90.
   PubMed Web of Science ®Google Scholar
• Lin, J. H. (2006). CYP induction-mediated drug interactions: in vitro assessment and clinical implications. Pharm Res 23:1089–1116.
   PubMed Web of Science ®Google Scholar
• Ma, Q. (2008). Xenobiotic-activated receptors: from transcription to drug metabolism to disease. Chem Res Toxicol 21:1651–1671.
   PubMed Web of Science ®Google Scholar
• Maglich, J. M., Stoltz, C. M., Goodwin, B., Hawkins-Brown, D., Moore, J. T., Kliewer, S. A. (2002). Nuclear pregnane X receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. Mol Pharmacol 62:638–646.
   PubMed Web of Science ®Google Scholar
• Martin, H, Sarsat, JP, De Waziers, I, Housset, C, Balladur, P, Beaune, P, et al. (2003). Induction of cytochrome P450 2B6 and 3A4 expression by phenobarbital and cyclophosphamide in cultured human liver slices. Pharm Res 20:557–568.
   PubMed Web of Science ®Google Scholar
• Maurel, P. (1996). The use of adult human hepatocytes in primary culture and other in vitro systems to investigate drug metabolism in man. Adv Drug Deliv Rev 22:105–132.
   Web of Science ®Google Scholar
• Moore, J.T, Moore, L. B, Maglich, J. M, Kliewer, S. A (2003). Functional and structural comparison of PXR and CAR. Biochim Biophys Acta 1619:235–238.
   PubMed Web of Science ®Google Scholar
• Moore, L. B., Parks, D. J., Jones, S. A., Bledsoe, R. K., Consler, T. G., Stimmel, J. B., et al. (2000). Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. J Biol Chem 275:15122–15127.
   PubMed Web of Science ®Google Scholar
• Nelson, DR, Kamataki, T, Waxman, DJ, Guengerich, FP, Estabrook, RW, Feyereisen, R, et al. (1993). The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol 12: 1–51.
   PubMed Web of Science ®Google Scholar
• Nelson, DR, Koymans, L, Kamataki, T, Stegeman, JJ, Feyereisen, R, Waxman, DJ, et al. (1996). P450 superfamily: update on new sequences, gene mapping, accession numbers, and nomenclature. Pharmacogenetics 6:1–42.
   PubMedGoogle Scholar
• Omar, R., Gelboin, H. V., Rahimtula, A. D. (1996). Effect of cytochrome P450 induction on the metabolism and toxicity of ochratoxin A. Biochem Pharmacol 51:207–216.
   PubMed Web of Science ®Google Scholar
• Pascussi, J. M., Gerbal-Chaloin, S., Drocourt, L., Assénat, E., Larrey, D., Pichard-Garcia, L., et al. (2004). Cross-talk between xenobiotic detoxication and other signalling pathways: clinical and toxicological consequences. Xenobiotica 34:633–664.
   PubMed Web of Science ®Google Scholar
• Persson, K. P., Ekehed, S., Otter, C., Lutz, E. S., Mcpheat, J., Masimirembwa, C. M., et al. (2006). Evaluation of human liver slices and reporter gene assays as systems for predicting the cytochrome p450 induction potential of drugs in vivo in humans. Pharm Res 23:56–69.
   PubMed Web of Science ®Google Scholar
• Pfohl-Leszkowicz, A., Pinelli, E., Bartsch, H., Mohr, U., Castegnaro, M. (1998). Sex- and strain-specific expression of cytochrome P450s in ochratoxin A induced genotoxicity and carcinigenicity of ochratoxin A in rats. Mol Carcinog 23:76–85.
   PubMed Web of Science ®Google Scholar
• Pichard-Garcia, L., Gerbal-Chaloin, S., Ferrini, J. B., Fabre, J. M., Maurel, P. (2002). Use of long-term cultures of human hepatocytes to study cytochrome P450 gene expression. Meth Enzymol 357:311–321.
   PubMed Web of Science ®Google Scholar
• Ringot, D., Chango, A., Schneider, Y. J., Larondelle, Y. (2006). Toxicokinetics and toxicodynamics of ochratoxin A, an update. Chem Biol Interact 159:18–46.
   PubMed Web of Science ®Google Scholar
• Roth, A., Chakor, K., Creppy, E. E., Kane, A., Roschenthaler, R., Dirheimer, G. (1988). Evidence of an enterohepatic circulation of ochratoxin A in mice. Toxicology 48:293–308.
   PubMed Web of Science ®Google Scholar
• Ryu, D. Y., Levi, P. E., Fernandez-Salguero, F. J., Hodgson, E. (1996). Piperonyl butoxide and acenaphthylene induce cytochrome P450 1A2 and 1B1 mRNA in aromatic hydrocarbon-responsive receptor knock-out mouse liver. Mol Pharmacol 50:443–446.
   PubMed Web of Science ®Google Scholar
• Størmer, F. C., Hansen, C. E., Pedersen, J. I., Aasen, J. (1983). Formation of (4R)- and (4S)-4-hydroxyochratoxin A and 10-hydroxyochratoxin A from ochratoxin A by rabbit liver microsomes. Appl Environ Microbiol 45:1183–1187.
   PubMed Web of Science ®Google Scholar
• Størmer, F. C., Pederson, J. I. (1980). Formation of (4R)- and (4S)-hydroxyochratoxin A from ochratoxin A by rat liver microsomes. Appl Environ Microbiol 39:971–975.
   PubMed Web of Science ®Google Scholar
• Størmer, F. C., Storen, O., Hansen, C. E., Pedersen, J. I., Hvistendahl, G., Aarsen, A. J. (1981). Formation of (4R)- and (4S)-hydroxyochratoxin A from ochratoxin A by liver microsomes from various species. Appl Environ Microbiol 42:1051–1056.
   PubMed Web of Science ®Google Scholar
• Tan, Z., Huang, M., Puga, A., Xia, Y. (2004). A critical role for MAP kinases in the control of Ah receptor complex activity. Toxicol Sci 82:80–87.
   PubMed Web of Science ®Google Scholar
• Tang, C., Lin, J. H., Lu, A. Y. H. (2005). Metabolism-based drug–drug interactions: what determines individual variability in cytochrome P450 induction? Drug Metab Dispos 33:603–613.
   PubMed Web of Science ®Google Scholar
• Wang, H., Faucette, S. R., Gilbert, D., Jolley, S. L., Sueyoshi, T., Negishi, M., et al. (2003). Glucocorticoid receptor enhancement of pregnane X receptor-mediated CYP2B6 regulation in primary human hepatocytes. Drug Metab Dispos 31:620–630.
   PubMed Web of Science ®Google Scholar
• WHO. (2001). Safety evaluation of certain mycotoxins in food. Fifty-sixth meeting of the joint FAO/WHO Expert Committee on Food Additives. In: WHO Food Additives Series 47 i-706.
   Google Scholar
• Williams, J. A., Stone, E. M., Millar, B. C., Gusterson, B. A., Grover, P. L., Phillips, D. H. (1998). Determination of the enzymes responsible for activation of the heterocyclic amine 2-amino-3-methylimidazo[4,5-f]quinoline in the human breast. Pharmacogenetics 8:519–528.
   Google Scholar
• Yoshinari, K., Tien, E., Negishi, M., Honkakoski, P. (2008). Receptor-mediated regulation of cytochromes P450. In: Ioannides, C. (Ed.), Cytochromes P450: role in the metabolism and toxicity of drugs and other xenobiotics ( pp. 417–448). Cambridge, UK: RSC.
   Google Scholar
• Zepnik, H., Pahler, A., Schauer, U., Dekant, W. (2001). Ochratoxin A induced tumor formation: is there a role of reactive ochratoxin A metabolites? Toxicol Sci 59:59–67.
   PubMed Web of Science ®Google Scholar