Cytochrome P450 expression in human hepatocytes and hepatoma cell lines: molecular mechanisms that determine lower expression in cultured cells

References

• ADEN, D. P., FOGEL, A., PurrxiN, S., DAMJANOV, I. and KNOWLES, B. B., 1979, Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature, 282, 615–616.
   PubMed Web of Science ®Google Scholar
• BACKLUND, M., JOHANSSON, I., MKRTCHIAN, S. and INGELMAN-SUNDBERG, M., 1997, Signal trans duction-mediated activation of the aryl hydrocarbon receptor in rat hepatoma H4IIE cells. Journal of Biological Chemistry, 272, 31 755–31 763.
   Google Scholar
• BORT, R., PONSODA, X., CARRASCO, E., GeniEz-LEcii6N, M. J. and CASTELL, J. V., 1996, Metabolism of aceclofenac in humans. Drug Metabolism and Disposition, 24, 834–841.
   Google Scholar
• CASTELL, J. V., JoyEa, R., BORT, R. and GemiEz-LEcii6N, M. J., 1998, The challenge of using hepatic cell using cell lines for drug metabolism studies. In Proceedings of COST B1 European Symposium on the Prediction of Drug Metabolism in Man: Progress and Problems (Luxembourg: European Commission) pp. 77–92.
   Google Scholar
• CEREGHINI, S., 1996, Liver-enriched transcription factors and hepatocyte differentiation. FASEB Journal, 10, 267–282.
   PubMed Web of Science ®Google Scholar
• DELESQUE-TOUCHARD, N., PARK, S. H. and WAXMAN, D. J., 2000, Synergistic action of hepatocyte nuclear factors 3 and 6 on CYP2C1 2 gene expression and suppression by growth hormone-activated STAT5b. Proposed model for female specific expression of CYP2C12 in adult rat liver. Journal of Biological Chemistry, 275, 34173–34182.
   Google Scholar
• DESCOMBES, P. and SCHIBLER, U., 1991, A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell, 67, 569–579.
   PubMed Web of Science ®Google Scholar
• DICKER, E., McHumt, T. and CEDERBAUM, A. I., 1990, Increased oxidation of p-nitrophenol and aniline by intact hepatocytes isolated from pyrazole-treated rats. Biochimica et Biophysica Ada, 1035, 249–256.
   PubMed Web of Science ®Google Scholar
• DIPPOLD, W. G., DIENES, H. P., KNUTH, A., SACHSSE, W., PRELLWITZ, W., BITTERSUERMANN, D. and MEYER ZUM BUSCHENFELDE, K. H., 1985, Hepatocellular carcinoma after thorotrast exposure: establishment of a new cell line (Mz-Hep-1). Hepatology, 5, 1112–1119.
   Google Scholar
• DONATO, M. T., CASTELL, J. V. and GOmEz-LEctiON, M. J., 1995, Effect of model inducers on cytochrome P450 activities of human hepatocytes in primary cultures. Drug Metabolism and Disposition, 25, 553–558.
   Google Scholar
• DONATO, M. T., GentEz-LEctiON, M. J. and CASTELL, J. V., 1993, A microassay for measuring cytochrome P4501A1 and P45011B1 activities in intact human and rat hepatocytes cultured on 96-well plates. Analytical Biochemistry, 213, 29–33.
   Google Scholar
• DUNCAN, S. A., NAVAS, M. A., DUFORT, D., ROSSANT, J. and SmEE, M., 1998, Regulation of a transcription factor network required for differentiation and metabolism. Science, 281, 692–695.
   PubMed Web of Science ®Google Scholar
• EDWARDS, A. M., GLISTAK, M. L., LUCAS, C. M. and WILSON, P. A., 1984, Ethoxycoumarin deethylase activity as a convenient measure of liver drug metabolizing enzymes: regulation in cultured rat hepatocytes. Biochemical Pharmacology, 33, 1537–1546.
   PubMed Web of Science ®Google Scholar
• EDWARDS, R. J., ADAMS, D. A., WATTS, P. S., DAVIES, D. S. and Booms, A. R., 1998, Development of a comprehensive panel of antibodies against the major xenobiotic metabolising forms of cytochrome P450 in human. Biochemical Pharmacology, 56, 377–387.
   PubMed Web of Science ®Google Scholar
• ELFERINK, C. J. and REINERS, J. J. J, 1996, Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques, 20, 470–477.
   PubMed Web of Science ®Google Scholar
• GEORGE, J., GOODWIN, B., LIDDLE, C., TAPNER, M. and FARRELL, G. C., 1997, Time-dependent expression of cytochrome P450 genes in primary cultures of well-differentiated human hepatocytes. Journal of Laboratory and Clinical Medicine, 129, 638–648.
   PubMed Web of Science ®Google Scholar
• GOmEz-LEctiON, M., JovER, R., DONATO, M. T., PONSODA, X., RODRIGUEZ, C., STENZEL, K. G., KLOCKE, R., PAUL, D., GuiLLEN, I., BORT, R. and CASTELL, J. V., 1998, Long-term expression of differentiated functions in hepatocytes cultured in three-dimensional collagen matrix. Journal of Cellular Physiology, 177, 553–562.
   Google Scholar
• GemEz-LEctiON, M. J., DONATO, M. T., PONSODA, X., FABRA, R., TRULLENQUE, R. and CASTELL, J. V., 1997, Isolation, culture and use of human hepatocytes in drug research. In In Vitro Methods in Pharmaceutical Research (San Diego: Academic Press), pp. 129–154.
   Google Scholar
• GentEz-LEctiON, M. J., DONATO, T., JovER, R., RODRIGUEZ, C., PONSODA, X., GLAISE, D., CASTELL, J. V. and GUGUEN-GUILLOUZO, C., 2001, Expression and induction of a large set of drug metabolism enzymes by the highly differentiated human hepatoma cell line BC2. European Journal of Biochemistry, 268, 1448–1459.
   Google Scholar
• GentEz-LEctiON, M. J., LOPEZ, P., DONATO, T., MONTOYA, A., LARRAURI, A., GIMENEZ, P., TRULLENQUE, R., FABRA, R. and CASTELL, J. V., 1990, Culture of human hepatocytes from small surgical liver biopsies. Biochemical characterization and comparison with in vivo. In Vitro Cellular and Developmental Biology, 26, 67–74.
   Google Scholar
• GONZALEZ, F. and LEE, Y., 1996, Constitutive expression of hepatic cytochrome P450 genes. FASEB Journal, 10, 1112–1117.
   PubMed Web of Science ®Google Scholar
• GUENGUERICH, F. P., 1995, Human cytochrome P450 enzymes. In Cytochromes P-450: Structure, Mechanism and Biochemistry (New York: Plenum), pp. 473–535.
   Google Scholar
• GumEouzo, A. and GUGUEN-GUILLOUZO, C., 1992, In vitro approaches to hepatotoxicity studies. In In Vitro Methods in Toxicology (London: Academic Press), pp 133–160.
   Google Scholar
• GumEouzo, A., 1998, Liver cell models in in vitro toxicology. Environmental Health Perspectives, 106, 511–531.
   PubMed Web of Science ®Google Scholar
• HAEHNER, B. D., GORSKI, J. C., VANDENBRANDEN, M., WRIGHTON, S. A., JANARDAN, S. K., WATKINS, P. B. and HALL, S. D., 1996, Bimodal distribution of renal cytochrome P450 3A activity in humans. Molecular Pharmacology, 50, 52–59.
   PubMed Web of Science ®Google Scholar
• JovER, R., BORT, R., GOMEZ, L., M. J. and CASTELL, J., 1998, Re-expression of C/EBP alpha induces CYP2B6, CYP2C9 and CYP2D6 genes in HepG2 cells. FEBS Letters, 431, 227–230.
   Google Scholar
• JovER, R., BORT, R., GOMEZ-LECHON, M. J. and CASTELL, J. V., 2001, Cytochrome P450 regulation by hepatocyte nuclear factor 4 in human hepatocytes: a study using adenovirus-mediated antisense targeting. Hepatology, 33, 668–675.
   Google Scholar
• KOMORI, M., HAHIZUME, T., Om, H., MIURA, T., KITADA, M., NAGASHIMA, K. and KkMATAKI, T., 1988, Cytochrome P-450 in human liver microsomes: high-performance liquid chromatographic isolation of three forms and their characterization. Journal of Biochemistry, 104, 912–916.
   PubMed Web of Science ®Google Scholar
• KRONBACH, T., MATHYS, D., GUT, J., CATIN, T. and MEYER, U. A., 1987, High-performance liquid chromatographic assays for bufuralol l'-hydroxylase, debrisoquine 4-hydroxylase, and dextromethorphan O.demethylase in microsomes and purified cytochrome P-450 isozymes of human liver. Analytical Biochemistry, 162, 24–32.
   PubMed Web of Science ®Google Scholar
• Kuo, C. J., CONLEY, P. B., CHEN, L., SLADEK, F. M., DARNELL, J. E. and CRABTREE, G. R., 1992, A transcriptional hierarchy involved in mammalian cell-type specification. Nature, 355, 457–461.
   PubMed Web of Science ®Google Scholar
• LEE, Y. H., WILLIAMS, S. C., BAER, M., STERNECK, E., GONZALEZ, F. J. and JOHNSON, P. F., 1997, The ability of C/EBP 13 but not C/EBP a to synergize with an Spl protein is specified by the leucine zipper and activation domain. Molecular and Cellular Biology, 17, 2038–2047.
   PubMed Web of Science ®Google Scholar
• LEGRAVEREND, C., EGUCHI, H., STROM, A., LAHUNA, O., MODE, A., TOLLET, P., WESTIN, S. and OUSTAFSSON, J., 1994, Transactivation of the rat CYP2C13 gene promoter involves HNF-1, HNF-3, and members of the orphan receptor subfamily. Biochemistry, 33, 9889–9897.
   PubMed Web of Science ®Google Scholar
• Li, A. P., 1997, Primary hepatocyte cultures as an in vitro experimental model for the evaluation of pharmacokinetic drug—drug interactions. In Advances in Pharmacology: Drug—Drug Interactions, Scientific and Regulatory Perspectives (London: Academic Press), pp. 103–129.
   Google Scholar
• Li, A. P., MAUREL, P., GOniEz-LEcliON, M. J., CHENG, L. C. and JURIMA ROMERT, M., 1996, Preclinical evaluation of drug—drug interaction potential: present status of the application of primary human hepatocytes in the evaluation of cytochrome P450 induction. Chemico-Biological Interactions, 107, 5–16.
   Google Scholar
• LOWRY, O. H., ROSENBROUGH, N. J., FARR, A. L. and RANDAL, R. J., 1951, Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193, 265–275.
   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. Advanced Drug Delivery Reviews, 22, 105–132.
   Web of Science ®Google Scholar
• MEYER, U. A., 1996, Overview of enzymes of drug metabolism. Journal of Pharmacokinetics and Biopharmacy, 24, 449–459.
   PubMedGoogle Scholar
• MOREL, F., BEAUNE, P. H., RATANASAVANH, D., FLINOIS, J. P., YANG, C. S., GUENGERICH, F. P. and Gumwuzo, A., 1990, Expression of cytochrome P-450 enzymes in cultured human hepatocytes. European Journal of Biochemistry, 191, 437–444.
   PubMedGoogle Scholar
• MURRAY, G. I. and BURKE, D. M., 1995, Immunochemistry of drug metabolizing enzymes. Biochemical Pharmacology, 50, 895–903.
   PubMed Web of Science ®Google Scholar
• NAKAMA, A., KURODA, K. and YAMAD A., 1995, Induction of cytochrome P450-dependent monooxygenase in serum-free cultured HepG2. Biochemical Pharmacology, 50, 1407–1412.
   PubMed Web of Science ®Google Scholar
• OSSIPOW, V., DESCOMBES, P. and SCHIBLER, U., 1993, CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proceedings of the National Academy of Sciences, USA, 90, 8219–8223.
   PubMed Web of Science ®Google Scholar
• PADGHAM, C. R., BOYLE, C. C., WANG, X. J., RALEIGH, S. M., WRIGHT, M. C. and PAINE, A. J., 1993, Alteration of transcription factor mRNAs during the isolation and culture of rat hepatocytes suggests the activation of a proliferative mode underlies their de-differentiation. Biochemical Biophysical Research Communications, 197, 599–605.
   PubMed Web of Science ®Google Scholar
• PADGHAM, C. R., PAINE, A. J., PHILLIPS, I. R. and SHEPHARD, E. A., 1992, Maintenance of total cytochrome P-450 content in rat hepatocyte culture and the abundance of CYP1 A2 and CYP2B1/2 mRNAs. Biochemical Journal, 285, 929–932.
   PubMed Web of Science ®Google Scholar
• PAINE, A. J., 1995, Heterogeneity of cytochrome P450 and its toxicological significance. Human Experimental Toxicology, 14, 1–7.
   PubMed Web of Science ®Google Scholar
• RENWICK, A. B., WATTS, P. S., EDWARDS, R. J., BARTON, P. T., GUYONNET, I., PRICE, R. J., TREDGER, J. M., PELKONEN, O., BOOBIS, A. R. and LAKE, B. G., 2000, Differential maintenance of cytochrome P450 enzymes in cultured precision-cut human liver slices. Drug Metabolism and Disposition, 28, 1202–1209.
   PubMed Web of Science ®Google Scholar
• RODRIGUEZ-ANTONA, C., JOVER, R., GemEz-LEcHôN, M. J. and CASTELL, J. V, 2000, Quantitative RT-PCR measurement of human cytochrome P-450s: application to drug induction studies. Archives of Biochemistry and Biophysics, 376, 109–116.
   Google Scholar
• ROE, A. L., SNAWDER, J. E., BENSON, R. W., ROBERTS, D. W. and CASCIANO, D. A., 1993, HepG2 cells: an in vitro model for P450-dependent metabolism of acetaminophen. Biochemical Biophysical Research Communications, 190, 15–19.
   PubMed Web of Science ®Google Scholar
• RUNGE, D. M., RUNGE, D., FOTH, H., STROM, S. C. and MICHALOPOULOS, G. K., 1999, STAT lalpha/ lbeta, STAT 3 and STAT 5: expression and association with c-MET and EGF-receptor in long-term cultures of human hepatocytes. Biochemical Biophysical Research Communications, 265, 376–381.
   PubMed Web of Science ®Google Scholar
• SAVAS, U., GRIN, K. J. and JOHNSON, E. F., 1999, Molecular mechanisms of cytochrome P-450 induction by xenobiotics: an expanded role for nuclear receptors. Molecular Pharmacology, 56, 851–857.
   PubMed Web of Science ®Google Scholar
• SHAW, P. M., WEISS, M. C. and ADESNIK, M., 1994, Hepatocyte nuclear factor 3 is a major determinant of CYP2C6 promoter activity in hepatoma. Molecular Pharmacology, 46, 79–87.
   PubMed Web of Science ®Google Scholar
• SPATH, G. F. and WEISS, M. C., 1997, Hepatocyte nuclear factor 4 expression overcomes repression of the hepatic phenotye in dedifferentiated hepatoma cells. Molecular and Cellular Biology, 17, 1931–1942.
   Web of Science ®Google Scholar
• SUMIDA, A., FUKUEN, S., YAMAMOTO, I., MATSUDA, H., NAOHARA, M. and AZUMA, J., 2000, Quantitative analysis of constitutive and inducible CYPs mRNA expression in the HepG2 cell line using reverse transcription-competitive PCR. Biochemical Biophysical Research Communications, 267, 756–760.
   PubMed Web of Science ®Google Scholar
• VALLET, V., ANTOINE, B., CHAFEY, P., VANDEWALLE, A. and KAHN, A., 1995, Overproduction of a truncated hepatocyte nuclear factor 3 protein inhibits expression of liver-specific genes in hepatoma cells. Molecular and Cellular Biology, 15, 5453–5460.
   PubMed Web of Science ®Google Scholar
• WANG, X. J., HODGKINSON, C. P., WRIGHT, M. C. and PAINE, A. J., 1997, Temperature-sensitive mRNA degradation is an early event in hepatocyte de-differentiation. Biochemical Journal, 328, 937–944.
   PubMed Web of Science ®Google Scholar
• WAXMAN, D. J., 1999, P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Archives of Biochemistry and Biophysics, 369, 11–23.
   PubMed Web of Science ®Google Scholar
• WAXMAN, D. J., LAPENSON, D. P., ÄOYAMA, T., GELBOIN, H. V., GONZALEZ, F. J. and KORZEKWA, K., 1991, Steroid hormone hydroxylase specificities of eleven cDNA-expressed human cytochrome P450s. Archives of Biochemistry and Biophysics, 290, 160–166.
   Google Scholar
• WOODCROFT, K. J. and NOVAK, R. F., 1998, Xenobiotic-enhanced expression of cytochromes P450 2E1 and 2B in primary cultured rat hepatocytes. Drug Metabolism and Disposition, 26, 372–378.
   PubMed Web of Science ®Google Scholar
• WRIGHTON, S. A., VANDENBRANDEN, M. and RING, B. J., 1996, The human drug metabolizing cytochromes P450. Journal of Pharmacokinetics and Biopharmacy, 24, 461–473.
   PubMedGoogle Scholar
• Wu, D. F., CLUNK, L., POTTER, B. and CEDERBAUM, A. I., 1990, Rapid decrease of cytochrome P-45011E1 in primary hepatocyte culture and its maintenance by added 4-methylpyrazole. Hepatology, 12, 1379–1389.
   PubMed Web of Science ®Google Scholar