Preferential induction of the AhR gene battery in HepaRG cells after a single or repeated exposure to heterocyclic aromatic amines

Toxicology and Applied Pharmacology

Volumn 249, Issue 1, 2010, Pages 91-100

  Dumont, Julie ^a,b,c   Jossé, Rozenn ^a,b   Lambert, Carine ^a,b   Anthérieu, Sébastien ^a,b   Laurent, Véronique ^a,b   Loyer, Pascal ^a,b   Robin, Marie Anne ^a,b   Guillouzo, André ^a,b  

^a Univ Rennes   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIV LILLE   (France)

Author keywords

Arylhydrocarbon receptor; HepaRG cells; Heterocyclic aromatic amines; Repeated exposure; Toxicogenomics

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 2 AMINO 3,8 DIMETHYLIMIDAZO[4,5 F]QUINOXALINE; AROMATIC AMINE; AROMATIC HYDROCARBON; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; CYTOCHROME P450 3A1; 2-AMINO-1-METHYL-6-PHENYLIMIDAZO(4,5-B)PYRIDINE; 2-AMINO-3,8-DIMETHYLIMIDAZO(4,5-F)QUINOXALINE; AMINE; AROMATIC HYDROCARBON RECEPTOR; IMIDAZOLE DERIVATIVE; QUINOXALINE DERIVATIVE;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CYTOTOXICITY; DOWN REGULATION; EXPOSURE; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; NEOPLASM; NUCLEOTIDE SEQUENCE; OLIGONUCLEOTIDE PROBE; PROMOTER REGION; RNA INTERFERENCE; BIOSYNTHESIS; COMPARATIVE STUDY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; PROCEDURES; TOXICITY; TUMOR CELL LINE;

RODENTIA;

AMINES; CELL LINE, TUMOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMIDAZOLES; QUINOXALINES; RECEPTORS, ARYL HYDROCARBON;

EID: 77957874665     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.08.027     Document Type: Article

References (46)

1. Alaejos M.S., Gonzalez V., Afonso A.M. Exposure to heterocyclic aromatic amines from the consumption of cooked red meat and its effect on human cancer risk: a review. Food Addit. Contam. A Chem. Anal. Control Expo. Risk Assess. 2008, 25:2-24.
2. Aninat C., Piton A., Glaise D., Le Charpentier T., Langouet S., Morel F., Guguen-Guillouzo C., Guillouzo A. Expression of cytochromes P450, conjugating enzymes and nuclear receptors in human hepatoma HepaRG cells. Drug Metab. Dispos. 2006, 34:75-83.
3. Barouki R., Coumoul X., Fernandez-Salguero P.M. The aryl hydrocarbon receptor, more than a xenobiotic-interacting protein. FEBS Lett. 2007, 581:3608-3615.
4. Cai J., Mao Z., Hwang J.J., Lu S.C. Differential expression of methionine adenosyltransferase genes influences the rate of growth of human hepatocellular carcinoma cells. Cancer Res. 1998, 58:1444-1450.
5. Cerec V., Glaise D., Garnier D., Morosan S., Turlin B., Drenou B., Gripon P., Kremsdorf D., Guguen-Guillouzo C., Corlu A. Transdifferentiation of hepatocyte-like cells from the human hepatoma HepaRG cell line through bipotent progenitor. Hepatology 2007, 45:957-967.
6. Chen C.H., Lu P.J., Chen Y.C., Fu S.L., Wu K.J., Tsou A.P., Lee Y.C., Lin T.C., Hsu S.L., Lin W.J., Huang C.Y., Chou C.K. FLJ10540-elicited cell transformation is through the activation of PI3-kinase/AKT pathway. Oncogene 2007, 26:4272-4283.
7. Dietrich C., Kaina B. The aryl hydrocarbon receptor (AhR) in the regulation of cell-cell contact and tumor growth. Carcinogenesis 2010, 8:1319-1328.
8. Dumont J., Josse R., Lambert C., Antherieu S., Le Hegarat L., Aninat C., Robin M.A., Guguen-Guillouzo C., Guillouzo A. Differential toxicity of heterocyclic aromatic amines and their mixture in metabolically competent HepaRG cells. Toxicol. Appl. Pharmacol. 2010, 245:256-263.
9. Ellinger-Ziegelbauer H., Aubrecht J., Kleinjans J.C., Ahr H.J. Application of toxicogenomics to study mechanisms of genotoxicity and carcinogenicity. Toxicol. Lett. 2009, 186:36-44.
10. Felton J.S., Knize M.G., Shen N.H., Andresen B.D., Bjeldanes L.F., Hatch F.T. Identification of the mutagens in cooked beef. Environ. Health Perspect. 1986, 67:17-24.
11. Felton J.S., Malfatti M.A., Knize M.G., Salmon C.P., Hopmans E.C., Wu R.W. Health risks of heterocyclic amines. Mutat. Res. 1997, 376:37-41.
12. Fielden M.R., Nie A., McMillian M., Elangbam C.S., Trela B.A., Yang Y., Dunn R.T., Dragan Y., Fransson-Stehen R., Bogdanffy M., Adams S.P., Foster W.R., Chen S.J., Rossi P., Kasper P., Jacobson-Kram D., Tatsuoka K.S., Wier P.J., Gollub J., Halbert D.N., Roter A., Young J.K., Sina J.F., Marlowe J., Martus H.J., Aubrecht J., Olaharski A.J., Roome N., Nioi P., Pardo I., Snyder R., Perry R., Lord P., Mattes W., Car B.D. Interlaboratory evaluation of genomic signatures for predicting carcinogenicity in the rat. Toxicol. Sci. 2008, 103:28-34.
13. Fontana R.J., Lown K.S., Paine M.F., Fortlage L., Santella R.M., Felton J.S., Knize M.G., Greenberg A., Watkins P.B. Effects of a chargrilled meat diet on expression of CYP3A, CYP1A, and P-glycoprotein levels in healthy volunteers. Gastroenterology 1999, 117:89-98.
14. Fujiwara K., Ochiai M., Ubagai T., Ohki M., Ohta T., Nagao M., Sugimura T., Nakagama H. Differential gene expression profiles in colon epithelium of two rat strains with distinct susceptibility to colon carcinogenesis after exposure to PhIP in combination with dietary high fat. Cancer Sci. 2003, 94:672-678.
15. Fulda S. Caspase-8 in cancer biology and therapy. Cancer Lett. 2009, 281:128-133.
16. Gripon P., Rumin S., Urban S., Le Seyec J., Glaise D., Cannie I., Guyomard C., Lucas J., Trepo C., Guguen-Guillouzo C. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl Acad. Sci. USA 2002, 99:15655-15660.
17. Hao M.W., Liang Y.R., Liu Y.F., Liu L., Wu M.Y., Yang H.X. Transcription factor EGR-1 inhibits growth of hepatocellular carcinoma and esophageal carcinoma cell lines. World J. Gastroenterol. 2002, 8:203-207.
18. He N., Park K., Zhang Y., Huang J., Lu S., Wang L. Epigenetic inhibition of nuclear receptor small heterodimer partner is associated with and regulates hepatocellular carcinoma growth. Gastroenterology 2008, 134:793-802.
19. Hu Y., Lehrach H., Janitz M. Apoptosis screening of human chromosome 21 proteins reveals novel cell death regulators. Mol. Biol. Rep. 2010, 37:3381-3387.
20. Ito Y., Takeda T., Sakon M., Monden M., Tsujimoto M., Matsuura N. Expression and prognostic role of cyclin-dependent kinase 1 (cdc2) in hepatocellular carcinoma. Oncology 2000, 59:68-74.
21. Josse R., Aninat C., Glaise D., Dumont J., Fessard V., Morel F., Poul J.M., Guguen-Guillouzo C., Guillouzo A. Long-term functional stability of human HepaRG hepatocytes and use for chronic toxicity and genotoxicity studies. Drug Metab. Dispos. 2008, 36:1111-1118.
22. Kang J.S., Wanibuchi H., Murai T., Morimura K., Kinoshita A., Fukushima S. Analysis of gene expression in different stages of MeIQx-induced rat hepatocarcinogenesis. Oncol. Rep. 2007, 17:747-752.
23. Keating G.A., Bogen K.T. Methods for estimating heterocyclic amine concentrations in cooked meats in the US diet. Food Chem. Toxicol. 2001, 39:29-43.
24. Kleman M., Overvik E., Mason G., Gustafsson J.A. Effects of the food mutagens MeIQx and PhIP on the expression of cytochrome P450IA proteins in various tissues of male and female rats. Carcinogenesis 1990, 11:2185-2189.
25. Kleman M.I., Overvik E., Mason G.G., Gustafsson J.A. In vitro activation of the dioxin receptor to a DNA-binding form by food-borne heterocyclic amines. Carcinogenesis 1992, 13:1619-1624.
26. Knasmuller S., Schwab C.E., Land S.J., Wang C.Y., Sanyal R., Kundi M., Parzefall W., Darroudi F. Genotoxic effects of heterocyclic aromatic amines in human derived hepatoma (HepG2) cells. Mutagenesis 1999, 14:533-540.
27. Komarov A.P., Rokhlin O.W., Yu C.A., Gudkov A.V. Functional genetic screening reveals the role of mitochondrial cytochrome b as a mediator of FAS-induced apoptosis. Proc. Natl Acad. Sci. USA 2008, 105:14453-14458.
28. Koskinas J., Petraki K., Kavantzas N., Rapti I., Kountouras D., Hadziyannis S. Hepatic expression of the proliferative marker Ki-67 and p53 protein in HBV or HCV cirrhosis in relation to dysplastic liver cell changes and hepatocellular carcinoma. J. Viral Hepat. 2005, 12:635-641.
29. Lambert C.B., Spire C., Claude N., Guillouzo A. Dose- and time-dependent effects of phenobarbital on gene expression profiling in human hepatoma HepaRG cells. Toxicol. Appl. Pharmacol. 2009, 234:345-360.
30. Langouet S., Paehler A., Welti D.H., Kerriguy N., Guillouzo A., Turesky R.J. Differential metabolism of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine in rat and human hepatocytes. Carcinogenesis 2002, 23:115-122.
31. Laurent V., Fraix A., Montier T., Cammas-Marion S., Ribault C., Benvegnu T., Jaffres P.A., Loyer P. Highly efficient gene transfer into hepatocyte-like HepaRG cells: new means for drug metabolism and toxicity studies. Biotechnol. J. 2010, 5:314-320.
32. Le Ferrec E., Lagadic-Gossmann D., Rauch C., Bardiau C., Maheo K., Massiere F., Le Vee M., Guillouzo A., Morel F. Transcriptional induction of CYP1A1 by oltipraz in human Caco-2 cells is aryl hydrocarbon receptor- and calcium-dependent. J. Biol. Chem. 2002, 277:24780-24787.
33. Liu Q., Wu K., Zhu Y., He Y., Wu J., Liu Z. Silencing MAT2A gene by RNA interference inhibited cell growth and induced apoptosis in human hepatoma cells. Hepatol. Res. 2007, 37:376-388.
34. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang Y., Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 2000, 59:65-85.
35. Nebert D.W., Dalton T.P., Okey A.B., Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279:23847-23850.
36. Shan L., Yu M., Schut H.A., Snyderwine E.G. Susceptibility of rats to mammary gland carcinogenesis by the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP) varies with age and is associated with the induction of differential gene expression. Am. J. Pathol. 2004, 165:191-202.
37. Silkworth J.B., Carlson E.A., McCulloch C., Illouz K., Goodwin S., Sutter T.R. Toxicogenomic analysis of gender, chemical, and dose effects in livers of TCDD- or aroclor 1254-exposed rats using a multifactor linear model. Toxicol. Sci. 2008, 102:291-309.
38. Sinha R., Rothman N., Brown E.D., Mark S.D., Hoover R.N., Caporaso N.E., Levander O.A., Knize M.G., Lang N.P., Kadlubar F.F. Pan-fried meat containing high levels of heterocyclic aromatic amines but low levels of polycyclic aromatic hydrocarbons induces cytochrome P4501A2 activity in humans. Cancer Res. 1994, 54:6154-6159.
39. Sugimura T., Wakabayashi K., Nakagama H., Nagao M. Heterocyclic amines: Mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci. 2004, 95:290-299.
40. Tsujimura K., Asamoto M., Suzuki S., Hokaiwado N., Ogawa K., Shirai T. Prediction of carcinogenic potential by a toxicogenomic approach using rat hepatoma cells. Cancer Sci. 2006, 97:1002-1010.
41. Turesky R.J., Guengerich F.P., Guillouzo A., Langouet S. Metabolism of heterocyclic aromatic amines by human hepatocytes and cytochrome P4501A2. Mutat. Res. 2002, 506-507:187-195.
42. van Delft J.H., van Agen E., van Breda S.G., Herwijnen M.H., Staal Y.C., Kleinjans J.C. Comparison of supervised clustering methods to discriminate genotoxic from non-genotoxic carcinogens by gene expression profiling. Mutat. Res. 2005, 575:17-33.
43. Wang S.P., Zhou H.J., Chen X.P., Ren G.Y., Ruan X.X., Zhang Y., Zhang R.L., Chen J. Loss of expression of Kruppel-like factor 6 in primary hepatocellular carcinoma and hepatoma cell lines. J. Exp. Clin. Cancer Res. 2007, 26:117-124.
44. Winter H.K., Ehrlich V.A., Grusch M., Lackner A., Schulte-Hermann R., Grasl-Kraupp B., Mikulits W., Knasmuller S. Use of four new human-derived liver-cell lines for the detection of genotoxic compounds in the single-cell gel electrophoresis (SCGE) assay. Mutat. Res. 2008, 657:133-139.
45. Wong N., Yeo W., Wong W.L., Wong N.L., Chan K.Y., Mo F.K., Koh J., Chan S.L., Chan A.T., Lai P.B., Ching A.K., Tong J.H., Ng H.K., Johnson P.J., To K.F. TOP2A overexpression in hepatocellular carcinoma correlates with early age onset, shorter patients survival and chemoresistance. Int. J. Cancer 2009, 124:644-652.
46. Yeager R.L., Reisman S.A., Aleksunes L.M., Klaassen C.D. Introducing the "TCDD-inducible AhR-Nrf2 gene battery". Toxicol. Sci. 2009, 111:238-246.