Identification of early target genes of aflatoxin B1 in human hepatocytes, inter-individual variability and comparison with other genotoxic compounds

Toxicology and Applied Pharmacology

Volumn 258, Issue 2, 2012, Pages 176-187

  Josse, Rozenn ^a,b   Dumont, Julie ^a,b   Fautrel, Alain ^a,b   Robin, Marie Anne ^a,b   Guillouzo, André ^a,b  

^a FACULTÉ DES SCIENCES PHARMACEUTIQUES ET BIOLOGIQUES   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

AFB1; Biomarker; FHIT; Genotoxic compounds; HepaRG cells; Human hepatocytes; Non genotoxic compounds; Transcriptomics

Indexed keywords

AFLATOXIN B1; BREAST CARCINOMA AMPLIFIED SEQUENCE 3 PROTEIN; DNA; FRAGILE HISTIDINE TRIAD PROTEIN; PROTEIN; PROTEIN P53; SET AND MYND DOMAIN CONTAINING 3 PROTEIN; SMALL INTERFERING RNA; TOXIC SUBSTANCE; UNCLASSIFIED DRUG;

ADULT; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; CELL POPULATION; CONTROLLED STUDY; DNA DAMAGE; DNA MICROARRAY; DNA REPAIR; EXPERIMENTAL MODEL; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; GENOTOXICITY; HUMAN; HUMAN CELL; LIVER CELL; PROTO ONCOGENE; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

AFLATOXIN B1; CELL CYCLE; CELLS, CULTURED; DNA DAMAGE; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; MUTAGENS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84855760394     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.10.019     Document Type: Article

References (51)

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. Bedard L.L., Massey T.E. Aflatoxin B1-induced DNA damage and its repair. Cancer Lett. 2006, 241:174-183.
3. Breuer M.L., Cuypers H.T., Berns A. Evidence for the involvement of pim-2, a new common proviral insertion site, in progression of lymphomas. EMBO J. 1989, 8:743-748.
4. Cai J., Sun W.M., Hwang J.J., Stain S.C., Lu S.C. Changes in S-adenosylmethionine synthetase in human liver cancer: molecular characterization and significance. Hepatology 1996, 24:1090-1097.
5. Chen L.B., Xu J.Y., Yang Z., Wang G.B. Silencing SMYD3 in hepatoma demethylates RIZI promoter induces apoptosis and inhibits cell proliferation and migration. World J. Gastroenterol. 2007, 13:5718-5724.
6. Croce C.M., Sozzi G., Huebner K. Role of FHIT in human cancer. J. Clin. Oncol. 1999, 17:1618-1624.
7. Dumont J., Josse R., Lambert C., Antherieu S., Laurent V., Loyer P., Robin M.A., Guillouzo A. Preferential induction of the AhR gene battery in HepaRG cells after a single or repeated exposure to heterocyclic aromatic amines. Toxicol. Appl. Pharmacol. 2010, 249:91-100.
8. Ellinger-Ziegelbauer H., Stuart B., Wahle B., Bomann W., Ahr H.J. Characteristic expression profiles induced by genotoxic carcinogens in rat liver. Toxicol. Sci. 2004, 77:19-34.
9. Ellinger-Ziegelbauer H., Stuart B., Wahle B., Bomann W., Ahr H.J. Comparison of the expression profiles induced by genotoxic and nongenotoxic carcinogens in rat liver. Mutat. Res. 2005, 575:61-84.
10. Ellinger-Ziegelbauer H., Gmuender H., Bandenburg A., Ahr H.J. Prediction of a carcinogenic potential of rat hepatocarcinogens using toxicogenomics analysis of short-term in vivo studies. Mutat. Res. 2008, 637:23-39.
11. Fielden M.R., Brennan R., Gollub J. A gene expression biomarker provides early prediction and mechanistic assessment of hepatic tumor induction by nongenotoxic chemicals. Toxicol. Sci. 2007, 99:90-100.
12. Fox C.J., Hammerman P.S., Cinalli R.M., Master S.R., Chodosh L.A., Thompson C.B. The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev. 2003, 17:1841-1854.
13. Gallagher E.P., Kunze K.L., Stapleton P.L., Eaton D.L. The kinetics of aflatoxin B1 oxidation by human cDNA-expressed and human liver microsomal cytochromes P450 1A2 and 3A4. Toxicol. Appl. Pharmacol. 1996, 141:595-606.
14. Genschel J., Bazemore L.R., Modrich P. Human exonuclease I is required for 5' and 3' mismatch repair. J. Biol. Chem. 2002, 277:13302-13311.
15. Gong J., Wang J., Ren K., Liu C., Li B., Shi Y. Serine/threonine kinase Pim-2 promotes liver tumorigenesis induction through mediating survival and preventing apoptosis of liver cell. J. Surg. Res. 2009, 153:17-22.
16. Goyak K.M., Johnson M.C., Strom S.C., Omiecinski C.J. Expression profiling of interindividual variability following xenobiotic exposures in primary human hepatocyte cultures. Toxicol. Appl. Pharmacol. 2008, 231:216-224.
17. 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.
18. Grombacher T., Eichhorn U., Kaina B. p53 is involved in regulation of the DNA repair gene O6-methylguanine-DNA methyltransferase (MGMT) by DNA damaging agents. Oncogene 1998, 17:845-851.
19. Guguen-Guillouzo C., Campion J.P., Brissot P., Glaise D., Launois B., Bourel M., Guillouzo A. High yield preparation of isolated human adult hepatocytes by enzymatic perfusion of the liver. Cell Biol. Int. Rep. 1982, 6:625-628.
20. Hamamoto R., Furukawa Y., Morita M., Iimura Y., Silva F.P., Li M., Yagyu R., Nakamura Y. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat. Cell Biol. 2004, 6:731-740.
21. Harris A.J., Dial S.L., Casciano D.A. Comparison of basal gene expression profiles and effects of hepatocarcinogens on gene expression in cultured primary human hepatocytes and HepG2 cells. Mutat. Res. 2004, 549:79-99.
22. Hu T., Gibson D.P., Carr G.J., Torontali S.M., Tiesman J.P., Chaney J.G., Aardema M.J. Identification of a gene expression profile that discriminates indirect-acting genotoxins from direct-acting genotoxins. Mutat. Res. 2004, 549:5-27.
23. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
24. Iida M., Anna C.H., Holliday W.M., Collins J.B., Cunningham M.L., Sills R.C., Devereux T.R. Unique patterns of gene expression changes in liver after treatment of mice for 2 weeks with different known carcinogens and non-carcinogens. Carcinogenesis 2005, 26:689-699.
25. Ishii H., Mimori K., Inoue H., Inageta T., Ishikawa K., Semba S., Druck T., Trapasso F., Tani K., Vecchione A., Croce C.M., Mori M., Huebner K. Fhit modulates the DNA damage checkpoint response. Cancer Res. 2006, 66:11287-11292.
26. Jennen D.G., Magkoufopoulou C., Ketelslegers H.B., van Herwijnen M.H., Kleinjans J.C., van Delft J.H. Comparison of HepG2 and HepaRG by whole-genome gene expression analysis for the purpose of chemical hazard identification. Toxicol. Sci. 2010, 115:66-79.
27. 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.
28. Kunizaki M., Hamamoto R., Silva F.P., Yamaguchi K., Nagayasu T., Shibuya M., Nakamura Y., Furukawa Y. The lysine 831 of vascular endothelial growth factor receptor 1 is a novel target of methylation by SMYD3. Cancer Res. 2007, 67:10759-10765.
29. Kvasha S., Gordiyuk V., Kondratov A., Ugryn D., Zgonnyk Y.M., Rynditch A.V., Vozianov A.F. Hypermethylation of the 5'CpG island of the FHIT gene in clear cell renal carcinomas. Cancer Lett. 2008, 265:250-257.
30. Lakin N.D., Jackson S.P. Regulation of p53 in response to DNA damage. Oncogene 1999, 18:7644-7655.
31. 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.
32. Le Hegarat L., Dumont J., Josse R., Huet S., Lanceleur R., Mourot A., Poul J.M., Guguen-Guillouzo C., Guillouzo A., Fessard V. Assessment of the genotoxic potential of indirect chemical mutagens in HepaRG cells by the comet and the cytokinesis-block micronucleus assays. Mutagenesis 2010, 25:555-560.
33. Li Y., Wan D.F., Su J.J., Cao J., Ou C., Qiu X.K., Ban K.C., Yang C., Qin L.L., Luo D., Yue H.F., Zhang L.S., Gu J.R. Differential expression of genes during aflatoxin B(1)-induced hepatocarcinogenesis in tree shrews. World J. Gastroenterol. 2004, 10:497-504.
34. Li J., Ramani K., Sun Z., Zee C., Grant E.G., Yang H., Xia M., Oh P., Ko K., Mato J.M., Lu S.C. Forced expression of methionine adenosyltransferase 1A in human hepatoma cells suppresses in vivo tumorigenicity in mice. Am. J. Pathol. 2010, 176:2456-2466.
35. Liu S.P., Li Y.S., Lee C.M., Yen C.H., Liao Y.J., Huang S.F., Chien C.H., Chen Y.M. Higher susceptibility to aflatoxin B(1)-related hepatocellular carcinoma in glycine N-methyltransferase knockout mice. Int. J. Cancer 2011, 128:511-523.
36. Maruyama R., Toyooka S., Toyooka K.O., Virmani A.K., Zochbauer-Muller S., Farinas A.J., Minna J.D., McConnell J., Frenkel E.P., Gazdar A.F. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin. Cancer Res. 2002, 8:514-519.
37. Mathijs K., Brauers K.J., Jennen D.G., Boorsma A., van Herwijnen M.H., Gottschalk R.W., Kleinjans J.C., van Delft J.H. Discrimination for genotoxic and nongenotoxic carcinogens by gene expression profiling in primary mouse hepatocytes improves with exposure time. Toxicol. Sci. 2009, 112:374-384.
38. Mathijs K., Brauers K.J., Jennen D.G., Lizarraga D., Kleinjans J.C., van Delft J.H. Gene expression profiling in primary mouse hepatocytes discriminates true from false-positive genotoxic compounds. Mutagenesis 2010, 25:561-568.
39. Nie A.Y., McMillian M., Parker J.B., Leone A., Bryant S., Yieh L., Bittner A., Nelson J., Carmen A., Wan J., Lord P.G. Predictive toxicogenomics approaches reveal underlying molecular mechanisms of nongenotoxic carcinogenicity. Mol. Carcinog. 2006, 45:914-933.
40. Pellegrino R., Calvisi D.F., Ladu S., Ehemann V., Staniscia T., Evert M., Dombrowski F., Schirmacher P., Longerich T. Oncogenic and tumor suppressive roles of polo-like kinases in human hepatocellular carcinoma. Hepatology 2010, 51:857-868.
41. Pichiorri F., Palumbo T., Suh S.S., Okamura H., Trapasso F., Ishii H., Huebner K., Croce C.M. Fhit tumor suppressor: guardian of the preneoplastic genome. Future Oncol. 2008, 4:815-824.
42. Rogue A., Lambert C., Josse R., Antherieu S., Spire C., Claude N., Guillouzo A. Comparative gene expression profiles induced by PPARgamma and PPARalpha/gamma agonists in human hepatocytes. PLoS One 2011, 6:e18816.
43. Siva K., Venu P., Mahadevan A., Shankar K.S., Inamdar M.S. Human BCAS3 expression in embryonic stem cells and vascular precursors suggests a role in human embryogenesis and tumor angiogenesis. PLoS One 2007, 2:e1202.
44. Tilton S.C., Gerwick L.G., Hendricks J.D., Rosato C.S., Corley-Smith G., Givan S.A., Bailey G.S., Bayne C.J., Williams D.E. Use of a rainbow trout oligonucleotide microarray to determine transcriptional patterns in aflatoxin B1-induced hepatocellular carcinoma compared to adjacent liver. Toxicol. Sci. 2005, 88:319-330.
45. van Delft J.H., van Agen E., van Breda S.G., Herwijnen M.H., Staal Y.C., Kleinjans J.C. Discrimination of genotoxic from non-genotoxic carcinogens by gene expression profiling. Carcinogenesis 2004, 25:1265-1276.
46. 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.
47. Yen C.H., Hung J.H., Ueng Y.F., Liu S.P., Chen S.Y., Liu H.H., Chou T.Y., Tsai T.F., Darbha R., Hsieh L.L., Chen Y.M. Glycine N-methyltransferase affects the metabolism of aflatoxin B1 and blocks its carcinogenic effect. Toxicol. Appl. Pharmacol. 2009, 235:296-304.
48. Yuan B.Z., Keck-Waggoner C., Zimonjic D.B., Thorgeirsson S.S., Popescu N.C. Alterations of the FHIT gene in human hepatocellular carcinoma. Cancer Res. 2000, 60:1049-1053.
49. Zhao P., Song X., Nin Y.Y., Lu Y.L., Li X.H. Loss of fragile histidine triad protein in human hepatocellular carcinoma. World J. Gastroenterol. 2003, 9:1216-1219.
50. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 2000, 408:433-439.
51. Zochbauer-Muller S., Fong K.M., Maitra A., Lam S., Geradts J., Ashfaq R., Virmani A.K., Milchgrub S., Gazdar A.F., Minna J.D. 5' CpG island methylation of the FHIT gene is correlated with loss of gene expression in lung and breast cancer. Cancer Res. 2001, 61:3581-3585.