Differential toxicity of heterocyclic aromatic amines and their mixture in metabolically competent HepaRG cells

Toxicology and Applied Pharmacology

Volumn 245, Issue 2, 2010, Pages 256-263

  Dumont, Julie ^a,b,d   Jossé, Rozenn ^a,b   Lambert, Carine ^a,b   Anthérieu, Sébastien ^a,b   Le Hegarat, Ludovic ^c   Aninat, Caroline ^a,b   Robin, Marie Anne ^a,b   Guguen Guillouzo, Christiane ^a,b   Guillouzo, André ^a,b  

^a FACULTÉ DES SCIENCES PHARMACEUTIQUES ET BIOLOGIQUES   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c Healthy Pigs Production and Experimentation Section   (France)

^d UNIV LILLE   (France)

Author keywords

Chemical mixture; Cytochrome P450 1A; Cytotoxicity; Genotoxicity; HepaRG cells; Heterocyclic aromatic amines

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 2 AMINO 3,8 DIMETHYLIMIDAZO[4,5 F]QUINOXALINE; AROMATIC AMINE; CASPASE 3; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; HETEROCYCLIC AMINE; MESSENGER RNA;

APOPTOSIS; ARTICLE; COMET ASSAY; CONTROLLED STUDY; CYTOTOXICITY; DETOXIFICATION; DNA DAMAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; EXPOSURE; GENOTOXICITY; HEPATOMA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; OXIDATIVE STRESS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION;

EID: 77952891821     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.03.008     Document Type: Article

References (40)

1. 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.
2. Breinholt V., Lauridsen S.T., Daneshvar B., Jakobsen J. Dose-response effects of lycopene on selected drug-metabolizing and antioxidant enzymes in the rat. Cancer Lett. 2000, 154:201-210.
3. Buonarati M.H., Turteltaub K.W., Shen N.H., Felton J.S. Role of sulfation and acetylation in the activation of 2-hydroxyamino-1-methyl-6-phenylimidazo[4, 5-b]pyridine to intermediates which bind DNA. Mutat. Res. 1990, 245:185-190.
4. 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.
5. Court M.H., Duan S.X., von Moltke L.L., Greenblatt D.J., Patten C.J., Miners J.O., Mackenzie P.I. Interindividual variability in acetaminophen glucuronidation by human liver microsomes: identification of relevant acetaminophen UDP-glucuronosyltransferase isoforms. J. Pharmacol. Exp.Ther. 2001, 299:998-1006.
6. Creton S., Zhu H., Gooderham N.J. A mechanistic basis for the role of cycle arrest in the genetic toxicology of the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP). Toxicol. Sci. 2005, 84:335-343.
7. Crofts F.G., Sutter T.R., Strickland P.T. Metabolism of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine by human cytochrome P4501A1, P4501A2 and P4501B1. Carcinogenesis 1998, 19:1969-1973.
8. Drahushuk A.T., McGarrigle B.P., Slezak B.P., Stegeman J.J., Olson J.R. Time- and concentration-dependent induction of CYP1A1 and CYP1A2 in precision-cut rat liver slices incubated in dynamic organ culture in the presence of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 1999, 155:127-138.
9. 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. U. S. A. 2002, 99:15655-15660.
10. Guillouzo A. Liver cell models in in vitro toxicology. Environ. Health Perspect. 1998, 106(Suppl 2):511-532.
11. Guillouzo A., Chesne C. Xenobiotic metabolism in epithelial cell cultures. Epithelial Cell Culture, A Pratical Approach 1996, 67-85. Oxford University Press, London. A.J. Shaw (Ed.).
12. Hasegawa R., Sano M., Tamano S., Imaida K., Shirai T., Nagao M., Sugimura T., Ito N. Dose-dependence of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]-pyridine (PhIP) carcinogenicity in rats. Carcinogenesis 1993, 14:2553-2557.
13. Hirata A., Tsukamoto T., Sakai H., Takasu S., Ban H., Imai T., Totsuka Y., Nishigaki R., Wakabayashi K., Yanai T., Masegi T., Tatematsu M. Carcinogenic risk of heterocyclic amines in combination - assessment with a liver initiation model. Food Chem. Toxicol. 2008, 46:2003-2009.
14. Hirose M., Takahashi S., Ogawa K., Futakuchi M., Shirai T. Phenolics: blocking agents for heterocyclic amine-induced carcinogenesis. Food Chem. Toxicol. 1999, 37:985-992.
15. Hummerich J., Zohm C., Pfau W. Modulation of cytochrome P450 1A1 by food-derived heterocyclic aromatic amines. Toxicology 2004, 199:231-240.
16. 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.
17. Kato T., Ohgaki H., Hasegawa H., Sato S., Takayama S., Sugimura T. Carcinogenicity in rats of a mutagenic compound, 2-amino-3, 8-dimethylimidazo[4, 5-f]quinoxaline. Carcinogenesis 1988, 9:71-73.
18. 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.
19. 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.
20. 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.
21. 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.
22. Lin D.X., Lang N.P., Kadlubar F.F. Species differences in the biotransformation of the food-borne carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine by hepatic microsomes and cytosols from humans, rats, and mice. Drug Metab. Dispos. 1995, 23:518-524.
23. Majer B.J., Mersch-Sundermann V., Darroudi F., Laky B., de Wit K., Knasmuller S. Genotoxic effects of dietary and lifestyle related carcinogens in human derived hepatoma (HepG2, Hep3B) cells. Mutat. Res. 2004, 551:153-166.
24. Moinova H.R., Mulcahy R.T. Up-regulation of the human gamma-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element. Biochem. Biophys. Res. Commun. 1999, 261:661-668.
25. Morel Y., Mermod N., Barouki R. An autoregulatory loop controlling CYP1A1 gene expression: role of H(2)O(2) and NFI. Mol. Cell. Biol. 1999, 19:6825-6832.
26. Nelson C.P., Kidd L.C., Sauvageot J., Isaacs W.B., De Marzo A.M., Groopman J.D., Nelson W.G., Kensler T.W. Protection against 2-hydroxyamino-1-methyl-6-phenylimidazo[4, 5-b]pyridine cytotoxicity and DNA adduct formation in human prostate by glutathione S-transferase P1. Cancer Res. 2001, 61:103-109.
27. Pfau W., Martin F.L., Cole K.J., Venitt S., Phillips D.H., Grover P.L., Marquardt H. Heterocyclic aromatic amines induce DNA strand breaks and cell transformation. Carcinogenesis 1999, 20:545-551.
28. Shih H., Pickwell G.V., Guenette D.K., Bilir B., Quattrochi L.C. Species differences in hepatocyte induction of CYP1A1 and CYP1A2 by omeprazole. Hum. Exp. Toxicol. 1999, 18:95-105.
29. Shimada T., Guengerich F.P. Inhibition of human cytochrome P450 1A1-, 1A2-, and 1B1-mediated activation of procarcinogens to genotoxic metabolites by polycyclic aromatic hydrocarbons. Chem. Res. Toxicol. 2006, 19:288-294.
30. Sohl C.D., Isin E.M., Eoff R.L., Marsch G.A., Stec D.F., Guengerich F.P. Cooperativity in oxidation reactions catalyzed by cytochrome P450 1A2: highly cooperative pyrene hydroxylation and multiphasic kinetics of ligand binding. J. Biol. Chem. 2008, 283:7293-7308.
31. Sparfel L., Van Grevenynghe J., Le Vee M., Aninat C., Fardel O. Potent inhibition of carcinogen-bioactivating cytochrome P450 1B1 by the p53 inhibitor pifithrin alpha. Carcinogenesis 2006, 27:656-663.
32. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27:502-522.
33. Tsuda H., Sekine K., Uehara N., Takasuka N., Moore M.A., Konno Y., Nakashita K., Degawa M. Heterocyclic amine mixture carcinogenesis and its enhancement by caffeine in F344 rats. Cancer Lett. 1999, 143:229-234.
34. Turesky R.J., Constable A., Fay L.B., Guengerich F.P. Interspecies differences in metabolism of heterocyclic aromatic amines by rat and human P450 1A2. Cancer Lett. 1999, 143:109-112.
35. 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.
36. Turpeinen M., Tolonen A., Chesne C., Guillouzo A., Uusitalo J., Pelkonen O. Functional expression, inhibition and induction of CYP enzymes in HepaRG cells. Toxicol In Vitro 2009, 23:748-753.
37. Wild A.C., Moinova H.R., Mulcahy R.T. Regulation of gamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 1999, 274:33627-33636.
38. Wilkening S., Stahl F., Bader A. Comparison of primary human hepatocytes and hepatoma cell line Hepg2 with regard to their biotransformation properties. Drug Metab. Dispos. 2003, 31:1035-1042.
39. Willett W.C. Diet, nutrition, and avoidable cancer. Environ. Health Perspect. 1995, 103(Suppl 8):165-170.
40. 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.