γ-Catenin as a multilayer modulator of zonal cytochrome P450 expression in mouse liver

Biological Chemistry

Volumn 391, Issue 2-3, 2010, Pages 139-148

  Braeuning, Albert ^a   Schwarz, Michael ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

catenin; Cytochrome P450; Drug metabolism; Enzyme induction; Hepatic zonation; Transcriptional

Indexed keywords

APC PROTEIN; AROMATIC HYDROCARBON RECEPTOR; BETA CATENIN; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 2A5; CYTOCHROME P450 2C; EPIDERMAL GROWTH FACTOR RECEPTOR; FRIZZLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; GUANOSINE TRIPHOSPHATASE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; ISOENZYME; LIGAND; MESSENGER RNA; RAS PROTEIN; TRANSCRIPTION FACTOR; UVOMORULIN; WNT PROTEIN; XENOBIOTIC AGENT; CATNB PROTEIN, MOUSE;

CELL SUBPOPULATION; CENTRAL VEIN; GENE EXPRESSION; KNOCKOUT MOUSE; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; REVIEW; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; LIVER; METABOLISM; MOUSE; MOUSE MUTANT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION PROFILING; LIVER; MICE; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77749336635     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.012     Document Type: Review

References (58)

1. Aydinlik, H., Nguyen, T.D., Moennikes, O., Buchmann, A., and Schwarz, M. (2001). Selective pressure during tumor promotion by phenobarbital leads to clonal outgrowth of beta-catenin-mutated mouse liver tumors. Oncogene 20, 7812-7816.
2. Benhamouche, S., Decaens, T., Godard, C., Chambrey, R., Rickman, D.S., Moinard, C., Vasseur-Cognet, M., Kuo, C.J., Kahn, A., Perret, C., et al. (2006). Apc tumor suppressor gene is the 'zonation-keeper' of mouse liver. Dev. Cell 10, 759-770.
3. Bock, K.W. (1994). Aryl hydrocarbon or dioxin receptor: biologic and toxic responses. Rev. Physiol. Biochem. Pharmacol. 125, 1-42.
4. Braeuning, A. (2009). Regulation of cytochrome p450 expression by ras- and Beta catenin-dependent signaling. Curr. Drug Metab. 10, 138-158.
5. Braeuning, A. and Buchmann, A. (2009). The glycogen synthase kinase inhibitor SB216763 is a partial agonist of the aryl hydrocarbon receptor. Drug Metab. Dispos. 37, 1576-1580.
6. Braeuning, A., Ittrich, C., Kohle, C., Hailfinger, S., Bonin, M., Buchmann, A., and Schwarz, M. (2006). Differential gene expression in periportal and perivenous mouse hepatocytes. FEBS J. 273, 5051-5061.
7. Braeuning, A., Ittrich, C., Kohle, C., Buchmann, A., and Schwarz, M. (2007a). Zonal gene expression in mouse liver resembles expression patterns of Ha-ras and β-catenin mutated hepatomas. Drug Metab. Dispos. 35, 503-507.
8. Braeuning, A., Menzel, M., Kleinschnitz, E.M., Harada, N., Tamai, Y., Kohle, C., Buchmann, A., and Schwarz, M. (2007b). Serum components and activated Ha-ras antagonize expression of perivenous marker genes stimulated by β-catenin signaling in mouse hepatocytes. FEBS J. 274, 4766-4777.
9. Braeuning, A., Sanna, R., Huelsken, J., and Schwarz, M. (2009). Inducibility of drug-metabolizing enzymes by xenobiotics in mice with liver-specific knockout of Ctnnb1. Drug Metab. Dispos. 37, 1138-1145.
10. Cadoret, A., Ovejero, C., Terris, B., Souil, E., Levy, L., Lamers, W.H., Kitajewski, J., Kahn, A., and Perret, C. (2002). New targets of β-catenin signaling in the liver are involved in the glutamine metabolism. Oncogene 21, 8293-8301.
11. Cavard, C., Colnot, S., Audard, V., Benhamouche, S., Finzi, L., Torre, C., Grimber, G., Godard, C., Terris, B., and Perret, C. (2008). Wnt/β-catenin pathway in hepatocellular carcinoma pathogenesis and liver physiology. Future Oncol. 4, 647-660.
12. Chafey, P., Finzi, L., Boisgard, R., Caüzac, M., Clary, G., Broussard, C., Pegorier, J.P., Guillonneau, F., Mayeux, P., Camoin, et al. (2009). Proteomic analysis of β-catenin activation in mouse liver by DIGE analysis identifies glucose metabolism as a new target of the Wnt pathway. Proteomics 9, 3889-3900.
13. Chesire, D.R., Dunn, T.A., Ewing, C.M., Luo, J., and Isaacs, W.B. (2004). Identification of aryl hydrocarbon receptor as a putative Wnt/β-catenin pathway target gene in prostate cancer cells. Cancer Res. 64, 2523-2533.
14. Colletti, M., Cicchini, C., Conigliaro, A., Santangelo, L., Alonzi, T., Pasquini, E., Tripodi, M., and Amicone, L. (2009). Convergence of Wnt signaling on the HNF4α-driven transcription in controlling liver zonation. Gastroenterology 137, 660-672.
15. Fernandez-Salguero, P., Pineau, T., Hilbert, D.M., McPhail, T., Lee, S.S.T., Kimura, S., Nebert, D.W., Rudikoff, S., Ward, J.M., and Gonzalez, F.J. (1995). Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268, 722-726.
16. Gebhardt, R. (1992). Metabolic zonation of the liver: regulation and implications for liver function. Pharmacol. Ther. 53, 275-354.
17. Gebhardt, R. and Gaunitz, F. (1997). Cell-cell interactions in the regulation of the expression of hepatic enzymes. Cell Biol. Toxicol. 13, 263-273.
18. Gebhardt, R. and Hovhannisyan, A. (2010). Organ patterning in the adult stage: the role of Wnt/beta-catenin signaling in liver zonation and beyond. Dev. Dyn. 239, 45-55.
19. Gebhardt, R., Schuler, M., and Schorner, D. (1998). The spontaneous induction of glutamine synthetase in pig hepatocytes cocultured with RL-ET-14 cells is completely inhibited by trijodothyronine and okadaic acid. Biochem. Biophys. Res. Commun. 246, 895-898.
20. Giannone, J.V., Li, W., Probst, M., and Okey, A.B. (1998). Prolonged depletion of AH receptor without alteration of receptor mRNA levels after treatment of cells in culture with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem. Pharmacol. 55, 489-497.
21. Gibson, G.G., Plant, N.J., Swales, K.E., Ayrton, A., and El-Sankary, W. (2002). Receptor-dependent transcriptional activation of cyto-chrome P4503A genes: induction mechanisms, species differences and interindividual variation in man. Xenobiotica 32, 165-206.
22. Gonzalez, F.J. (2008). Regulation of hepatocyte nuclear factor 4α-mediated transcription. Drug Metab. Pharmacokinet. 23, 2-7.
23. Hailfinger, S., Jaworski, M., Braeuning, A., Buchmann, A., and Schwarz, M. (2006). Zonal gene expression in murine liver: lessons from tumors. Hepatology 43, 407-414.
24. Jover, R., Hoffmann, F., Scheffler-Koch, V., and Lindberg, R.L. (2000). Limited heme synthesis in porphobilinogen deaminase-deficient mice impairs transcriptional activation of specific cytochrome P450 genes by phenobarbital. Eur. J. Biochem. 267, 7128-7137.
25. Jungermann, K. (1995). Zonation of metabolism and gene expression in liver. Histochem. Cell Biol. 103, 81-91.
26. Jungermann, K. and Katz, N. (1989). Functional specialization of different hepatocyte populations. Physiol. Rev. 69, 708-764.
27. Jungermann, K. and Kietzmann, T. (1996). Zonation of parenchymal and nonparenchymal metabolism in liver. Annu. Rev. Nutr. 16, 179-203.
28. Kruithof-de Julio, M., Labruyere, W.T., Ruijter, J.M., Vermeulen, J.L., Stanulovic, V., Stallen, J.M., Baldysiak-Figiel, A., Gebhardt, R., Lamers, W.H., and Hakvoort, T.B. (2005). The RL-ET-14 cell line mediates expression of glutamine synthetase through the upstream enhancer/promoter region. J. Hepatol. 43, 126-131.
29. Kuo, F.C. and Darnell, J.E., Jr. (1991). Evidence that interaction of hepatocytes with the collecting (hepatic) veins triggers position-specific transcription of the glutamine synthetase and ornithine aminotransferase genes in the mouse liver. Mol. Cell. Biol. 11, 6050-6058.
30. Lindl, T. (2002). Zell- und Gewebekultur (Heidelberg/Berlin: Spektrum Akademischer Verlag).
31. Lindros, K.O., Oinonen, T., Johansson, I., and Ingelman-Sundberg, M. (1997). Selective centrilobular expression of the aryl hydrocarbon receptor in rat liver. J. Pharmacol. Exp. Ther. 280, 506-511.
32. Loeppen, S., Koehle, C., Buchmann, A., and Schwarz, M. (2005). A β-catenin-dependent pathway regulates expression of cytochrome P450 isoforms in mouse liver tumors. Carcinogenesis 26, 239-248.
33. Lustig, B. and Behrens, J. (2003). The Wnt signaling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 129, 199-221.
34. Ma, Q. and Baldwin, K.T. (2000). 2,3,7,8-tetrachlorodibenzo-p-dioxin- induced degradation of aryl hydrocarbon receptor (AhR) by the ubiquitin-proteasome pathway. Role of the transcription activaton and DNA binding of AhR. J. Biol. Chem. 275, 8432-8438.
35. Moennikes, O., Buchmann, A., Romualdi, A., Ott, T., Werringloer, J., Willecke, K., and Schwarz, M. (2000). Lack of phenobarbital-mediated promotion of hepatocarcinogenesis in connexin32-null mice. Cancer Res. 60, 5087-5091.
36. Morgan, E.T. (2001). Regulation of cytochrome p450 by inflammatory mediators: why and how? Drug Metab. Dispos. 29, 207-212.
37. Morgan, E.T., Li-Masters, T., and Cheng, P.Y. (2002). Mechanisms of cytochrome P450 regulation by inflammatory mediators. Toxicology 181-182, 207-210.
38. Moriyama, A., Kii, I., Sunabori, T., Kurihara, S., Takayama, I., Shimazaki, M., Tanabe, H., Oginuma, M., Fukayama, M., Matsuzaki, et al. (2007). GFP transgenic mice reveal active canonical wnt signal in neonatal brain and in adult liver and spleen. Genesis 45, 90-100.
39. Mulholland, D.J., Dedhar, S., Coetzee, G.A., and Nelson, C.C. (2005). Interaction of nuclear receptors with the Wnt/β-catenin/Tcf signaling axis: Wnt you like to know? Endocr. Rev. 26, 898-915.
40. Oinonen, T. and Lindros, K.O. (1995). Hormonal regulation of the zonated expression of cytochrome P-450 3A in rat liver. Biochem. J. 309, 55-61.
41. Oinonen, T. and Lindros, K.O. (1998). Zonation of hepatic cyto-chrome P-450 expression and regulation. Biochem. J. 329, 17-35.
42. Oinonen, T., Nikkola, E., and Lindros, K.O. (1993). Growth hormone mediates zone-specific gene expression in liver. FEBS Lett. 327, 237-240.
43. Oinonen, T., Ronis, M., Wigell, T., Tohmo, K., Badger, T., and Lindros, K.O. (2000). Growth hormone-regulated periportal expression of CYP2C7 in rat liver. Biochem. Pharmacol. 59, 583-589.
44. Quistorff, B., Dich, J., and Grunnet, N. (1986). Periportal and perivenous hepatocytes retain their zonal characteristics in primary culture. Biochem. Biophys. Res. Commun. 139, 1055-1061.
45. Rogiers, V. and Vercruysse, A. (1998). Hepatocyte cultures in drug metabolism and toxicological research and testing. In: Cyto-chrome P450 Protocols, I.R. Phillips and E.A. Shepard, eds. (Totowa, NJ, USA: Humana Press), pp. 279-294.
46. Saad, B., Thomas, H., Schawalder, H., Waechter, F., and Maier, P. (1994). Oxygen tension, insulin, and glucagon affect the preservation and induction of cytochrome P450 isoforms in cultured rat hepatocytes. Toxicol. Appl. Pharmacol. 126, 372-379.
47. Sasse, D. (1986). Liver structure and innervation. In: Regulation of Hepatic Metabolism, Intra- and Intercellular Compartmentation, R.G. Thurman, ed. (New York/London: Plenum press), pp. 3-53.
48. Sekine, S., Lan, B.Y.A., Bedolli, M., Feng, S., and Hebrok, M. (2006). Liver-specific loss of β-catenin blocks glutamine synthesis pathway activity and cytochrome P450 expression in mice. Hepatology 43, 817-825.
49. Sekine, S., Gutierrez, P.J., Lan, B.Y., Feng, S., and Hebrok, M. (2007). Liver-specific loss of β-catenin results in delayed hepatocyte proliferation after partial hepatectomy. Hepatology 45, 361-368.
50. Stahl, S., Ittrich, C., Marx-Stoelting, P., Kohle, C., Altug-Teber, O., Riess, O., Bonin, M., Jobst, J., Kaiser, S., Buchmann, A., et al. (2005). Genotype-phenotype relationships in hepatocellular tumors from mice and man. Hepatology 42, 353-361.
51. Swales, K. and Negishi, M. (2004). CAR, driving into the future. Mol. Endocrinol. 18, 1589-1598.
52. Tan, X., Apte, U., Micsenyi. A., Kotsagrelos, E., Luo, J.H., Ranganathan, S., Monga, D.K., Bell, A., Michalopoulos, G.K., and Monga, S.P. (2005). Epidermal growth factor receptor: a novel target of the Wnt/β-catenin pathway in liver. Gastroenterology 129, 285-302.
53. Tan, X., Behari, J., Cieply, B., Michalopoulos, G.K., and Monga, S.P. (2006). Conditional deletion of β-catenin reveals its role in liver growth and regeneration. Gastroenterology 131, 1561-1572.
54. Tritscher, A.M., Goldstein, J.A., Portier, C.J., McCoy, Z., Clark, G.C., and Lucier, G.W. (1992). Dose-response relationships for chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin in a rat tumor promotion model: quantification and immunolocalization of CYP1A1 and CYP1A2 in the liver. Cancer Res. 52, 3436-3442.
55. Venkateswar, V. and Padmanaban, G. (1991). Involvement of heme in the transcriptional activation of CYPIIB1/B2 gene by phenobarbitone in rat liver - studies with succinylacetone. Arch. Biochem. Biophys. 290, 167-172.
56. Waxman, D.J. and Holloway, M.G. (2009). Sex differences in the expression of hepatic drug metabolizing enzymes. Mol. Pharmacol. 76, 215-228.
57. Willert, K. and Nusse, R. (1998). Beta-catenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8, 95-102.
58. Wolf, C.R., Buchmann, A., Friedberg, T., Moll, E., Kuhlmann, W.D., Kunz, H.W., and Oesch, F. (1984). Dynamics of the localization of drug metabolizing enzymes in tissues and cells. Biochem. Soc. Trans. 12, 60-62.