The interplay of the aryl hydrocarbon receptor and β-catenin alters both AhR-dependent transcription and wnt/β-catenin signaling in liver progenitors

Toxicological Sciences

Volumn 122, Issue 2, 2011, Pages 349-360

  Procházková, Jiřina ^a,b   Kabátková, Markéta ^a   Bryja, Vítězslav ^a,c   Umannová, Lenka ^a,b   Bernatík, Ondřej ^c   Kozubík, Alois ^a   Machala, Miroslav ^b   Vondrácěk, Jan ^a,b  

^a INSTITUTE OF BIOPHYSICS   (Czech Republic)

^b VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^c MASARYK UNIVERSITY   (Czech Republic)

Author keywords

Contact inhibition; Differentiation; Dioxin; Intercellular junctions; Liver progenitor cells; Wnt signaling

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; BETA CATENIN; BIOLOGICAL MARKER; CYTOCHROME P450 1A1; CYTOKERATIN 14; CYTOKERATIN 19; CYTOKERATIN 8; DIGITALIS LIKE FACTOR; UVOMORULIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL DISRUPTION; CELL JUNCTION; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; LIVER CARCINOGENESIS; LIVER STEM CELL; NONHUMAN; PHENOTYPE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BETA CATENIN; CADHERINS; CELL ADHESION; CELL DIFFERENTIATION; CELL LINE; CYTOCHROME P-450 CYP1A1; DOWN-REGULATION; HEPATOCYTES; LIVER; RATS; RATS, INBRED F344; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 80051702065     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr129     Document Type: Article

References (41)

1. Ale-Agha, N., Galban, S., Sobieroy, C., Abdelmohsen, K., Gorospe, M., Sies, H., and Klotz, L. O. (2009). HuR regulates gap junctional intercellular communication by controlling beta-catenin levels and adherens junction integrity. Hepatology 50, 1567-76.
2. Andrysík, Z., Vondrácěk, J., Machala, M., Krčmář, P., Š vihálková-Šindlerová, L., Kranz, A., Weiss, C., Faust, D., Kozubík, A., and Dietrich, C. (2007). The aryl hydrocarbon receptor-dependent deregulation of cell cycle control induced by polycyclic aromatic hydrocarbons in rat liver epithelial cells. Mutat. Res. 615, 87-97.
3. Angers, S., and Moon, R. T. (2009). Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 10, 468-477.
4. Apte, U., Thompson, M. D., Cui, S., Liu, B., Cieply, B., and Monga, S. P. (2008). Wnt/beta-catenin signaling mediates oval cell response in rodents. Hepatology 47, 288-295.
5. Atienza, J. M., Zhu, J., Wang, X., Xu, X., and Abassi, Y. (2005). Dynamic monitoring of cell adhesion and spreading on microelectronic sensor arrays. J. Biomol. Screen. 10, 795-805.
6. Benhamouche, S., Decaens, T., Godard, C., Chambrey, R., Rickman, D. S., Moinard, C., Vasseur-Cognet, M., Kuo, C. J., Kahn, A., and Perret, C. (2006). Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev. Cell 10, 759-770.
7. Bisgaard, H. C., Nagy, P., Ton, P. T., Hu, Z., and Thorgeirsson, S. S. (1994). Modulation of keratin 14 and alpha-fetoprotein expression during hepatic oval cell proliferation and liver regeneration. J. Cell. Physiol. 159, 475-484.
8. Braeuning, A., Köhle, C., Buchmann, A., and Schwarz, M. (2011). Coordinate regulation of cytochrome P450 1A1 expression in mouse liver by the aryl hydrocarbon receptor and the beta-catenin pathway. Toxicol. Sci. Adv. Advance access published on April 16, 2011; doi: 10.1093/toxsci/kfr080.
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. Bryja, V., Schulte, G., Rawal, N., Grahn, A., and Arenas, E. (2007). Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J. Cell Sci. 120, 586-595.
11. Bui, L. C., Tomkiewicz, C., Chevallier, A., Pierre, S., Bats, A. S., Mota, S., Raingeaud, J., Pierre, J., Diry, M., Transy, C., et al. (2009). Nedd9/Hef1/Cas-L mediates the effects of environmental pollutants on cell migration and plasticity. Oncogene 28, 3642-3651.
12. 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/beta-catenin pathway target gene in prostate cancer cells. Cancer Res. 64, 2523-25-33.
13. Clevers, H. (2006). Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480.
14. Dietrich, C., and Kaina, B. (2010). The aryl hydrocarbon receptor (AhR) in the regulation of cell-cell contact and tumor growth. Carcinogenesis 31, 1319-1328.
15. Diry, M., Tomkiewicz, C., Koehle, C., Coumoul, X., Bock, K. W., Barouki, R., and Transy, C. (2006). Activation of the dioxin/aryl hydrocarbon receptor (AhR) modulates cell plasticity through a JNK-dependent mechanism. Oncogene 25, 5570-5574.
16. Fan, Y., Boivin, G. P., Knudsen, E. S., Nebert, D. W., Xia, Y., and Puga, A. (2010). The aryl hydrocarbon receptor functions as a tumor suppressor of liver carcinogenesis. Cancer Res. 70, 212-220.
17. Golding, M., Sarraf, C. E., Lalani, E. N., Anilkumar, T. V., Edwards, R. J., Nagy, P., Thorgeirsson, S. S., and Alison, M. R. (1995). Oval cell differentiation into hepatocytes in the acetylaminofluorene-treated regenerating rat liver. Hepatology 22, 1243-1253.
18. 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.
19. Heuberger, J., and Birchmeier, W. (2010). Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb. Perspect. Biol. 2, a002915.
20. Hu, M., Kurobe, M., Jeong, Y. J., Fuerer, C., Ghole, S., Nusse, R., and Sylvester, K. G. (2007). Wnt/beta-catenin signaling in murine hepatic transit amplifying progenitor cells. Gastroenterology 133, 1579-1591.
21. Kawajiri, K., Kobayashi, Y., Ohtake, F., Ikuta, T., Matsushima, Y., Mimura, J., Pettersson, S., Pollenz, R. S., Sakaki, T., Hirokawa, T., et al. (2009). Aryl hydrocarbon receptor suppresses intestinal carcinogenesis in ApcMin/+ mice with natural ligands. Proc. Natl. Acad. Sci. U.S.A. 106, 13481-13486.
22. Ke, Z., Zhou, F., Wang, L., Chen, S., Liu, F., Fan, X., Tang, F., Liu, D., and Zhao, G. (2008). Down-regulation of Wnt signaling could promote bone marrow-derived mesenchymal stem cells to differentiate into hepatocytes. Biochem. Biophys. Res. Commun. 367, 342-348.
23. Kleber, M., and Sommer, L. (2004). Wnt signaling and the regulation of stem cell function. Curr. Opin. Cell. Biol. 16, 681-687.
24. Kung, T., Murphy, K. A., and White, L. A. (2009). The aryl hydrocarbon receptor (AhR) pathway as a regulatory pathway for cell adhesion and matrix metabolism. Biochem. Pharmacol. 77, 536-546.
25. Loeppen, S., Koehle, C., Buchmann, A., and Schwarz, M. (2005). A betacatenin-dependent pathway regulates expression of cytochrome P450 isoforms in mouse liver tumors. Carcinogenesis 26, 239-248.
26. Mathew, L. K., Sengupta, S. S., Ladu, J., Andreasen, E. A., and Tanguay, R. L. (2008). Crosstalk between AHR and Wnt signaling through R-Spondin1 impairs tissue regeneration in zebrafish. Faseb. J. 22, 3087-3096.
27. Nebert, D. W., and Dalton, T. P. (2006). The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat. Rev. Cancer 6, 947-960.
28. Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., Hintz, L., Nusse, R., and Weissman, I. L. (2003). A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423, 409-414.
29. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P., and Brivanlou, A. H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55-63.
30. Shafritz, D. A., and Dabeva, M. D. (2002). Liver stem cells and model systems for liver repopulation. J. Hepatol. 36, 552-564.
31. Singh, K. P., Casado, F. L., Opanashuk, L. A., and Gasiewicz, T. A. (2009). The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem. Pharmacol. 77, 577-587.
32. Sissung, T. M., Price, D. K., Sparreboom, A., and Figg, W. D. (2006). Pharmacogenetics and regulation of human cytochrome P450 1B1: implications in hormone-mediated tumor metabolism and a novel target for therapeutic intervention. Mol. Cancer Res. 4, 135-150.
33. Thompson, M. D., and Monga, S. P. (2007). WNT/beta-catenin signaling in liver health and disease. Hepatology 45, 1298-1305.
34. Tsao, M. S., Smith, J. D., Nelson, K. G., and Grisham, J. W. (1984). A diploid epithelial cell line from normal adult rat liver with phenotypic properties of 'oval' cells. Exp. Cell Res. 154, 38-52.
35. Vondrácěk, J., Machala, M., Bryja, V., Chramostová, K., Krčmář, P., Dietrich, C., Hampl, A., and Kozubík, A. (2005). Aryl hydrocarbon receptor-activating polychlorinated biphenyls and their hydroxylated metabolites induce cell proliferation in contact-inhibited rat liver epithelial cells. Toxicol. Sci. 83, 53-63.
36. Wallingford, J. B., and Habas, R. (2005). The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132, 4421-4436.
37. Weiss, C., Faust, D., Schreck, I., Ruff, A., Farwerck, T., Melenberg, A., Schneider, S., Oesch-Bartlomowicz, B., and Zatloukalová, J. (2008). TCDD deregulates contact inhibition in rat liver oval cells via Ah receptor, JunD and cyclin A. Oncogene 27, 2198-2207.
38. Wheelock, M. J., and Johnson, K. R. (2003). Cadherins as modulators of cellular phenotype. Annu. Rev. Cell Dev. Biol. 19, 207-235.
39. Yang, W., Yan, H. X., Chen, L., Liu, Q., He, Y. Q., Yu, L. X., Zhang, S. H., Huang, D. D., Tang, L., Kong, X. N., et al. (2008). Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res. 68, 4287-4295.
40. Zatloukalová, J., Švihálková-Šindlerová, L., Kozubík, A., Krčmář, P., Machala, M., and Vondrácěk, J. (2007). beta-Naphthoflavone and 3'-methoxy-4'-nitroflavone exert ambiguous effects on Ah receptordependent cell proliferation and gene expression in rat liver 'stem-like' cells. Biochem. Pharmacol. 73, 1622-1634.
41. Zhang, Y., Li, X. M., Zhang, F. K., and Wang, B. E. (2008). Activation of canonical Wnt signaling pathway promotes proliferation and self-renewal of rat hepatic oval cell line WB-F344 in vitro. World J. Gastroenterol. 14, 6673-6680.