Lower expression of HNF4α and PGC1α might impair rifampicin-mediated CYP3A4 induction under Conditions Where PXR is overexpressed in human fetal liver cells

Drug Metabolism and Pharmacokinetics

Volumn 27, Issue 4, 2012, Pages 430-438

  Takezawa, Takashi ^a   Matsunaga, Tamihide ^b   Aikawa, Kaori ^a   Nakamura, Katsunori ^a   Ohmori, Shigeru ^a  

^a SHINSHU UNIVERSITY HOSPITAL   (Japan)

^b NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

CYP3As; Drug mediated induction; Fetal liver; HNF4a; PGC1a; PXR

Indexed keywords

CLOTRIMAZOLE; CYTOCHROME P450 3A4; DEXAMETHASONE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; HISTONE ACETYLTRANSFERASE PCAF; MESSENGER RNA; MIFEPRISTONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PREGNANE X RECEPTOR; RETINOID X RECEPTOR; RIFAMPICIN; STEROID RECEPTOR COACTIVATOR 1;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYP3A4 GENE; DOWN REGULATION; FETUS; FETUS CELL; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HNF4ALPHA GENE; HUMAN; HUMAN CELL; LIGAND BINDING; LIVER CELL; NUCLEOTIDE SEQUENCE; PGC1ALPHA; PHARMACOGENETICS; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PXR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RXRALPHA GENE; UPREGULATION;

EID: 84865388549     PISSN: 13474367     EISSN: 18800920     Source Type: Journal    
DOI: 10.2133/dmpk.DMPK-11-RG-126     Document Type: Article

References (54)

1. Nelson, D. R., Koymans, L., Kamataki, T., Stegeman, J. J., Feyereisen, R., Waxman, D. J., Waterman, M. R., Gotoh, O., Coon, M. J., Estabrook, R. W., Gunsalus, I. C. and Nebert, D. W.: P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics, 6: 1-42 (1996).
2. Thummel, K. E. and Wilkinson, G. R.: In vitro and in vivo drug interactions involving human CYP3A. Annu. Rev. Pharmacol. Toxicol., 38: 389-430 (1998).
3. Domanski, T. L., Finta, C., Halpert, J. R. and Zaphiropoulos, P. G.: cDNA cloning and initial characterization of CYP3A43, a novel human cytochrome P450. Mol. Pharmacol., 59: 386-392 (2001).
4. Shimada, T., Yamazaki, H., Mimura, M., Inui, Y. and Guengerich, F. P.: Interindividual variations in human liver cytochrome P-450 enzymes involved in the oxidation of drugs, carcinogens and toxic chemicals: studies with liver microsomes of 30 Japanese and 30 Caucasians. J. Pharmacol. Exp. Ther., 270: 414-423 (1994).
5. Li, A. P., Kaminski, D. L. and Rasmussen, A.: Substrates of human hepatic cytochrome P450 3A4. Toxicology, 104: 1-8 (1995).
6. Kitada, M.: Cytochrome P-450 in human fetal liver. Properties of P-450 HFLa, a form of cytochrome P-450 in human fetal livers. Yakugaku Zasshi, 111: 158-169 (1991).
7. Lu, C. and Li, A. P.: Species comparison in P450 induction: effects of dexamethasone, omeprazole, and rifampin on P450 isoforms 1A and 3A in primary cultured hepatocytes from man, Sprague-Dawley rat, minipig, and beagle dog. Chem. Biol. Interact., 134: 271-281 (2001).
8. Vignati, L. A., Bogni, A., Grossi, P. and Monshouwer, M.: 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 (2004).
9. Komoroski, B. J., Zhang, S., Cai, H., Hutzler, J. M., Frye, R., Tracy, T. S., Strom, S. C., Lehmann, T., Ang, C. Y., Cui, Y. Y. and Venkataramanan, R.: Induction and inhibition of cytochromes P450 by the St. Johnös wort constituent hyperforin in human hepatocyte cultures. Drug Metab. Dispos., 32: 512-518 (2004).
10. Gibson, G. G., Plant, N. J., Swales, K. E., Ayrton, A. and El-Sankary, W.: Receptor-dependent transcriptional activation of cytochrome P4503A genes: induction mechanisms, species differences and interindividual variation in man. Xenobiotica, 32: 165-206 (2002).
11. Maruyama, M., Matsunaga, T., Harada, E. and Ohmori, S.: Comparison of Basal Gene Expression and Induction of CYP3As in HepG2 and Human Fetal Liver Cells. Biol. Pharm. Bull., 30: 2091-2097 (2007).
12. Wang, H. and LeCluyse, E. L.: Role of orphan nuclear receptors in the regulation of drug-metabolising enzymes. Clin. Pharmacokinet., 42: 1331-1357 (2003).
13. Li, T. and Chiang, J. Y.: Rifampicin induction of CYP3A4 requires pregnane X receptor crosstalk with hepatocyte nuclear factor 4alpha and coactivators, and suppression of small heterodimer partner gene expression. Drug Metab. Dispos., 34: 756-764 (2006).
14. Usui, T., Saitoh, Y. and Komada, F.: Induction of CYP3As in HepG2 cells by several drugs. Association between induction of CYP3A4 and expression of glucocorticoid receptor. Biol. Pharm. Bull., 26: 510-517 (2003).
15. Pascussi, J. M., Drocourt, L., Gerbal-Chaloin, S., Fabre, J. M., Maurel, P. and Vilarem, M. J.: Dual effect of dexamethasone on CYP3A4 gene expression in human hepatocytes. Sequential role of glucocorticoid receptor and pregnane X receptor. Eur. J. Biochem., 268: 6346-6358 (2001).
16. Bertilsson, G., Heidrich, J., Svensson, K., Asman, M., Jendeberg, L., Sydow-Backman, M., Ohlsson, R., Postlind, H., Blomquist, P. and Berkenstam, A.: Identification of a human nuclear receptor defines a new signaling pathway for CYP3A induction. Proc. Natl. Acad. Sci. USA, 95: 12208-12213 (1998).
17. Blumberg, B., Sabbagh, W., Jr., Bolado, J., Jr., van Meter, C. M., Ong, E. S. and Evans, R. M.: SXR, a novel steroid and xenobiotic sensing nuclear receptor. Genes Dev., 12: 3195-3205 (1998).
18. Lehmann, J. M., McKee, D. D., Watson, M. A., Wilson, T. M., Moore, J. T. and Kliewer, S. A.: 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 (1998).
19. Kliewer, S. A., Moore, J. T., Wade, L., Staudinger, J. L., Watson, M. A., Jones, S. A., McKee, D. D., Oliver, B. B., Willson, T. M., Zetterstrom, R. H., Perlmann, T. and Lehmann, J. M.: An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell, 92: 73-82 (1998).
20. Takada, T., Ogino, M., Miyata, M., Shimada, M., Nagata, K. and Yamazoe, Y.: Differences in transactivation between rat CYP3A1 and human CYP3A4 genes by human pregnane X receptor. Drug Metab. Pharmacokinet., 19: 103-113 (2004).
21. Matsunaga, T., Maruyama, M., Harada, E., Katsuyama, Y., Sugihara, N., Ise, H., Negishi, N., Ikeda, U. and Ohmori, S.: Expression and induction of CYP3As in human fetal hepatocytes. Biochem. Biophys. Res. Commun., 318: 428-434 (2004).
22. Sladek, F. M., Zhong, W. M., Lai, E. and Darnell, J. E., Jr.: Liver-enriched transcription factor HNF-4 is a novel member of the steroid hormone receptor superfamily. Genes Dev., 4: 2353-2365 (1990).
23. Li, J., Ning, G. and Duncan, S. A.: Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev., 14: 464-474 (2000).
24. Hayhurst, G. P., Lee, Y. H., Lambert, G., Ward, J. M. and Gonzalez, F. J.: Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1. is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol., 21: 1393-1403 (2001).
25. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M. and Spiegelman, B. M.: A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 92: 829-839 (1998).
26. Rhee, J., Inoue, Y., Yoon, J. C., Puigserver, P., Fan, M., Gonzalez, F. J. and Spiegelman, B. M.: Regulation of hepatic fasting response by PPARgamma coactivator-1alpha (PGC-1): requirement for hepatocyte nuclear factor 4alpha in gluconeogenesis. Proc. Natl. Acad. Sci. USA, 100: 4012-4017 (2003).
27. Yoon, J. C., Puigserver, P., Chen, G., Donovan, J., Wu, Z., Rhee, J., Adelmant, G., Stafford, J., Kahn, C. R., Granner, D. K., Newgard, C. B. and Spiegelman, B. M.: Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature, 413: 131-138 (2001).
28. Herzog, B., Hall, R. K., Wang, X., Waltner-Law, M. and Granner, D. K.: Peroxisome proliferator-activated receptor gamma coactivator-1alpha, as a transcription amplifier, is not essential for basal and hormone-induced phosphoenolpyruvate carboxykinase gene expression. Mol. Endocrinol., 18: 807-819 (2004).
29. Bhalla, S., Ozalp, C., Fang, S., Xiang, L. and Kemper, J. K.: Ligand-activated Pregnane X Receptor Interferes with HNF-4 Signaling by Targeting a Common Coactivator PGC-1Æ. J. Biol. Chem., 279: 45139-45147 (2004).
30. Ourlin, J. C., Lasserre, F., Pineau, T., Fabre, J. M., Sa-Cunha, A., Maurel, P., Vilarem, M. J. and Pascussi, J. M.: The small heterodimer partner interacts with the pregnane X receptor and represses its transcriptional activity. Mol. Endocrinol., 17: 1693-1703 (2003).
31. Aden, D. P., Fogel, A., Plotkin, S., Damjanov, I. and Knowles, B. B.: Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature, 282: 615-616 (1979).
32. Sumida, A., Fukuen, S., Yamamoto, I., Matsuda, H., Naohara, M. and Azuma, J.: Quantitative analysis of constitutive and inducible CYPs mRNA expression in the HepG2 cell line using reverse transcription-competitive PCR. Biochem. Biophys. Res. Commun., 267: 756-760 (2000).
33. Sumida, A., Yamamoto, I., Zhou, Q., Morisaki, T. and Azuma, J.: Evaluation of induction of CYP3A mRNA using the HepG2 cell line and reverse transcription-PCR. Biol. Pharm. Bull., 22: 61-65 (1999).
34. Schuetz, E. G., Schuetz, J. D., Strom, S. C., Thompson, M. T., Fisher, R. A., Molowa, D. T., Li, D. and Guzelian, P. S.: Regulation of human liver cytochromes P-450 in family 3A in primary and continuous culture of human hepatocytes. Hepatology, 18: 1254-1262 (1993).
35. Stevens, J. C., Hines, R. N., Gu, C., Koukouritaki, S. B., Manro, J. R., Tandler, P. J. and Zaya, M. J.: Developmental expression of the major human hepatic CYP3A enzymes. J. Pharmacol. Exp. Ther., 307: 573-582 (2003).
36. Lehmann, J. M., McKee, D. D., Watson, M. A., Willson, T. M., Moore, J. T. and Kliewer, S. A.: 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 (1998).
37. Pascussi, J. M., Drocourt, L., Fabre, J. M., Maurel, P. and Vilarem, M. J.: Dexamethasone induces pregnane X receptor and retinoid X receptor-alpha expression in human hepatocytes: synergistic increase of CYP3A4 induction by pregnane X receptor activators. Mol. Pharmacol., 58: 361-372 (2000).
38. Pascussi, J. M., Gerbal-Chaloin, S., Fabre, J. M., Maurel, P. and Vilarem, M. J.: Dexamethasone enhances constitutive androstane receptor expression in human hepatocytes: consequences on cytochrome P450 gene regulation. Mol. Pharmacol., 58: 1441-1450 (2000).
39. Zhang, W., Purchio, A., Chen, K., Burns, S. M., Contag, C. H. and Contag, P. R.: In vivo activation of the human CYP3A4 promoter in mouse liver and regulation by pregnane X receptors. Biochem. Pharmacol., 65: 1889-1896 (2003).
40. Furukawa, M., Okubo, T., Ogino, M., Yamazaki, T., Shimada, M., Nagata, K. and Yamazoe, Y.: Adenovirus vector-mediated reporter system for in vivo analyses of human CYP3A4 gene activation. J. Biochem., 131: 71-78 (2002).
41. Iordanidou, P., Aggelidou, E., Demetriades, C. and Hadzopoulou-Cladaras, M.: Distinct amino acid residues may be involved in coactivator and ligand interactions in hepatocyte nuclear factor-4alpha. J. Biol. Chem., 280: 21810-21819 (2005).
42. Sladek, F. M., Ruse, M. D., Jr., Nepomuceno, L., Huang, S. M. and Stallcup, M. R.: Modulation of transcriptional activation and coactivator interaction by a splicing variation in the F domain of nuclear receptor hepatocyte nuclear factor 4alpha1. Mol. Cell. Biol., 19: 6509-6522 (1999).
43. Wang, J. C., Stafford, J. M. and Granner, D. K.: SRC-1 and GRIP1 coactivate transcription with hepatocyte nuclear factor 4. J. Biol. Chem., 273: 30847-30850 (1998).
44. Dell, H. and Hadzopoulou-Cladaras, M.: CREB-binding protein is a transcriptional coactivator for hepatocyte nuclear factor-4 and enhances apolipoprotein gene expression. J. Biol. Chem., 274: 9013-9021 (1999).
45. Eeckhoute, J., Formstecher, P. and Laine, B.: Maturity-onset diabetes of the young Type 1 (MODY1)-associated mutations R154X and E276Q in hepatocyte nuclear factor 4alpha (HNF4alpha. gene impair recruitment of p300, a key transcriptional co-activator. Mol. Endocrinol., 15: 1200-1210 (2001).
46. Johnson, D. R., Li, C. W., Chen, L. Y., Ghosh, J. C. and Chen, J. D.: Regulation and binding of pregnane X receptor by nuclear receptor corepressor silencing mediator of retinoid and thyroid hormone receptors (SMRT). Mol. Pharmacol., 69: 99-108 (2006).
47. Chen, Y., Kissling, G., Negishi, M. and Goldstein, J. A.: The nuclear receptors constitutive androstane receptor and pregnane X receptor cross-talk with hepatic nuclear factor 4alpha to synergistically activate the human CYP2C9 promoter. J. Pharmacol. Exp. Ther., 314: 1125-1133 (2005).
48. Ferguson, S. S., Chen, Y., LeCluyse, E. L., Negishi, M. and Goldstein, J. A.: Human CYP2C8 is transcriptionally regulated by the nuclear receptors constitutive androstane receptor, pregnane X receptor, glucocorticoid receptor, and hepatic nuclear factor 4alpha. Mol. Pharmacol., 68: 747-757 (2005).
49. Kamiya, A., Inoue, Y. and Gonzalez, F. J.: Role of the hepatocyte nuclear factor 4alpha in control of the pregnane X receptor during fetal liver development. Hepatology, 37: 1375-1384 (2003).
50. Tirona, R. G., Lee, W., Leake, B. F., Lan, L. B., Cline, C. B., Lamba, V., Parviz, F., Duncan, S. A., Inoue, Y., Gonzalez, F. J., Schuetz, E. G. and Kim, R. B.: The orphan nuclear receptor HNF4alpha determines PXR-and constitutive androstane receptormediated xenobiotic induction of CYP3A4. Nat. Med., 9: 220-224 (2003).
51. Martinez-Jiménez, C. P., Gomez-Lechon, M. J., Castell, J. V. and Jover, R.: Underexpressed coactivators PGC1alpha AND SRC1 impair hepatocyte nuclear factor 4alpha function and promote dedifferentiation in human hepatoma cells. J. Biol. Chem., 281: 29840-29849 (2006).
52. Rhee, J., Ge, H., Yang, W., Fan, M., Handschin, C., Cooper, M., Lin, J., Li, C. and Spiegelman, B. M.: Partnership of PGC-1alpha and HNF4alpha in the regulation of lipoprotein metabolism. J. Biol. Chem., 281: 14683-14690 (2006).
53. Prieur, X., Schaap, F. G., Coste, H. and Rodríguez, J. C.: Hepatocyte nuclear factor-4alpha regulates the human apolipoprotein AV gene: identification of a novel response element and involvement in the control by peroxisome proliferator-activated receptor-gamma coactivator-1alpha, AMP-activated protein kinase, and mitogen-activated protein kinase pathway. Mol. Endocrinol., 19: 3107-3125 (2005).
54. Linja, M. J., Porkka, K. P., Kang, Z., Savinainen, K. J., Janne, O. A., Tammela, T. L., Vessella, R. L., Palvimo, J. J. and Visakorpi, T.: Expression of androgen receptor coregulators in prostate cancer. Clin. Cancer Res., 10: 1032-1040 (2004).