Comparison of phenotypic and transcriptomic effects of false-positive genotoxins, true genotoxins and non-genotoxins using HepG2 cells

Mutagenesis

Volumn 26, Issue 5, 2011, Pages 593-604

  Magkoufopoulou, C ^a,b   Claessen, S M H ^a   Jennen, D G J ^a,b   Kleinjans, J C S ^a,b   Van Delft, J H M ^a,b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b Netherlands Toxicogenomics Centre   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 8 QUINOLINOL; AFLATOXIN B1; BENZO[A]PYRENE; CYCLOSPORIN A; ESTRADIOL; HISTONE H2AX; PIVAMPICILLIN; QUERCETIN;

ARTICLE; CELL CYCLE; CELL STRAIN HEPG2; DNA REPAIR; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; PHENOTYPE; PHOSPHORYLATION; PRIORITY JOURNAL; TRANSCRIPTOMICS; UPREGULATION;

CELL CYCLE; CLUSTER ANALYSIS; DNA DAMAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; MOLECULAR SEQUENCE ANNOTATION; MUTAGENICITY TESTS; MUTAGENS; PHENOTYPE;

EID: 80052319066     PISSN: 02678357     EISSN: 14643804     Source Type: Journal    
DOI: 10.1093/mutage/ger021     Document Type: Article

References (102)

1. Kirkland, D., Aardema, M., Henderson, L. and Müller, L. (2005) Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens I. Sensitivity, specificity and relative predictivity. Mutat. Res., 584, 1-256.
2. ICH (2008) Guidance on genotoxicity testing and data interpretation for pharmaceuticals intended for human use S2(R1).
3. Pfuhler, S. et al. (2010) A tiered approach to the use of alternatives to animal testing for the safety assessment of cosmetics: Genotoxicity. A COLIPA analysis. Regul. Toxicol. Pharmacol., 57, 315-324.
4. Evans, T. J., Yamamoto, K. N., Hirota, K. and Takeda, S. (2010) Mutant cells defective in DNA repair pathways provide a sensitive highthroughput assay for genotoxicity. DNA Repair (Amst.), 9, 1292-1298.
5. Parry, J. M., Parry, E., Phrakonkham, P. and Corvi, R. (2010) Analysis of published data for top concentration considerations in mammalian cell genotoxicity testing. Mutagenesis, 25, 531-538.
6. Birrell, L., Cahill, P., Hughes, C., Tate, M. and Walmsley, R. M. (2010) GADD45a-GFP GreenScreen HC assay results for the ECVAM recommended lists of genotoxic and non-genotoxic chemicals for assessment of new genotoxicity tests. Mutat. Res., 695, 87-95.
7. Winter, H. K. et al. (2008) 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., 657, 133-139.
8. Liu, X., Kramer, J. A., Swaffield, J. C., Hu, Y., Chai, G. and Wilson, A. G. (2008) Development of a highthroughput yeast-based assay for detection of metabolically activated genotoxins. Mutat. Res., 653, 63-69.
9. Fontaine, F. R., De Graaf, Y. C., Ghaoui, R., Sallustio, B. C., Edwards, J. and Burcham, P. C. (2004) Optimisation of the comet genotoxicity assay in freshly isolated murine hepatocytes: Detection of strong in vitro DNA damaging properties for styrene. Toxicol. In Vitro, 18, 343-350.
10. Brambilla, G. and Martelli, A. (2004) Failure of the standard battery of short-term tests in detecting some rodent and human genotoxic carcinogens. Toxicology, 196, 1-19.
11. Ohno, Y. (2002) ICH guidelines-implementation of the 3Rs (refinement, reduction, and replacement): Incorporating best scientific practices into the regulatory process. ILAR J, 43 (Suppl), S95-S98.
12. Nuwaysir, E. F., Bittner, M., Trent, J., Barrett, J. C. and Afshari, C. A. (1999) Microarrays and toxicology: The advent of toxicogenomics. Mol. Carcinog., 24, 153-159.
13. Hamadeh, H. K., Bushel, P. R. and Jayadev, S. (2002) Gene expression analysis reveals chemical-specific profiles. Toxicol. Sci., 67, 219-231.
14. Cui, Y. and Paules, R. S. (2010) Use of transcriptomics in understanding mechanisms of drug-induced toxicity. Pharmacogenomics, 11, 573-585.
15. Ellinger-Ziegelbauer, H., Aubrecht, J., Kleinjans, J. C. and Ahr, H. J. (2009) Application of toxicogenomics to study mechanisms of genotoxicity and carcinogenicity. Toxicol. Lett., 186, 36-44.
16. Guo, L., Dial, S. and Shi, L. (2011) Similarities and differences in the expression of drug metabolizing enzymes between human hepatic cell lines and primary human hepatocytes. Drug Metab. Dispos, 39, 528-538.
17. Knasmuller, S., Mersch-Sundermann, V., Kevekordes, S., Darroudi, F., Huber, W. W., Hoelzl, C., Bichler, J. and Majer, B. J. (2004) Use of human-derived liver cell lines for the detection of environmental and dietary genotoxicants; current state of knowledge. Toxicology, 198, 315-328.
18. Dvorak, Z., Vrzal, R., Starha, P., Klanicova, A. and Travnicek, Z. (2010) Effects of dinuclear copper(II) complexes with 6-(benzylamino)purine derivatives on AhR and PXR dependent expression of cytochromes P450 CYP1A2 and CYP3A4 genes in primary cultures of human hepatocytes. Toxicol. In Vitro, 24, 425-429.
19. Chen, Y., Huang, C., Zhou, T. and Chen, G. (2008) Genistein induction of human sulfotransferases in HepG2 and Caco-2 cells. Basic Clin. Pharmacol. Toxicol., 103, 553-559.
20. Liguori, M. J., Blomme, E. A. and Waring, J. F. (2008) Trovafloxacininduced gene expression changes in liver-derived in vitro systems: Comparison of primary human hepatocytes to HepG2 cells. Drug Metab. Dispos., 36, 223-233.
21. Lancon, A., Hanet, N., Jannin, B., Delmas, D., Heydel, J. M., Lizard, G., Chagnon, M. C., Artur, Y. and Latruffe, N. (2007) Resveratrol in human hepatoma HepG2 cells: Metabolism and inducibility of detoxifying enzymes. Drug Metab. Dispos., 35, 699-703.
22. Jennen, D. G., Gaj, S., Giesbertz, P. J., van Delft, J. H., Evelo, C. T. and Kleinjans, J. C. (2010) Biotransformation pathway maps in WikiPathways enable direct visualization of drug metabolism related expression changes. Drug Discov. Today, 15, 851-858.
23. Natarajan, A. T. and Darroudi, F. (1991) Use of human hepatoma cells for in vitro metabolic activation of chemical mutagens/carcinogens. Mutagenesis, 6, 399-403.
24. Majer, B. J., Mersch-Sundermann, V., Darroudi, F., Laky, B., de Wit, K. and Knasmuller, S. (2004) Genotoxic effects of dietary and lifestyle related carcinogens in human derived hepatoma (HepG2, Hep3B) cells. Mutat. Res., 551, 153-166.
25. Hsu, I., Tokiwa, T., Bennett, W., Metcalf, R. A., Welsh, J. A., Sun, T. and Harris, C. C. (1993) p53 gene mutation and integrated hepatitis B viral DNA sequences in human liver cancer cell lines. Carcinogenesis, 14, 987-992.
26. Knasmüller, S., Parzefall, W. and Sanyal, R. (1998) Use of metabolically competent human hepatoma cells for the detection of mutagens and antimutagens. Mutat. Res., 402, 185-202.
27. Wilkening, S., Stahl, F. and Bader, A. (2003) Comparison of primary human hepatocytes and hepatoma cell line Hepg2 with regard to their biotransformation properties. Drug Metab. Dispos., 31, 1035-1042.
28. Jennen, D. G., Magkoufopoulou, C., Ketelslegers, H. B., van Herwijnen, M. H., Kleinjans, J. C. and van Delft, J. H. (2010) Comparison of HepG2 and HepaRG by whole-genome gene expression analysis for the purpose of chemical hazard identification. Toxicol. Sci., 115, 66-79.
29. van Delft, J. H., van Agen, E., van Breda, S. G., Herwijnen, M. H., Staal, Y. C. and Kleinjans, J. C. (2004) Discrimination of genotoxic from non-genotoxic carcinogens by gene expression profiling. Carcinogenesis, 25, 1265-1276.
30. van Delft, J. H., van Agen, E., van Breda, S. G., Herwijnen, M. H., Staal, Y. C. and Kleinjans, J. C. (2005) Comparison of supervised clustering methods to discriminate genotoxic from non-genotoxic carcinogens by gene expression profiling. Mutat. Res., 575, 17-33.
31. Westerink, W. M., Stevenson, J. C., Horbach, G. J. and Schoonen, W. G. (2010) The development of RAD51C, Cystatin A, p53 and Nrf2 luciferase-reporter assays in metabolically competent HepG2 cells for the assessment of mechanism-based genotoxicity and of oxidative stress in the early research phase of drug development. Mutat. Res., 696, 21-40.
32. O'Brien, P. J., Irwin, W. and Diaz, D. (2006) High concordance of druginduced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Arch. Toxicol., 80, 580-604.
33. Schoonen, W. G., de Roos, J. A., Westerink, W. M. and Debiton, E. (2005) Cytotoxic effects of 110 reference compounds on HepG2 cells and for 60 compounds on HeLa, ECC-1 and CHO cells. II mechanistic assays on NAD(P)H, ATP and DNA contents. Toxicol. In Vitro, 19, 491-503.
34. Harwood, M., Danielewska-Nikiel, B., Borzelleca, J. F., Flamm, G. W., Williams, G. W. and Lines, T. C. (2007) A critical review of the data related to the safety of quercetin and lack of evidence of in vivo toxicity, including lack of genotoxic/carcinogenic properties. Food Chem. Toxicol., 45, 2179-2205.
35. Andersen, A. (2006) Final amended report on the safety assessment of oxyquinoline and oxyquinoline sulfate as used in cosmetics. Int. J. Toxicol., 25 (Suppl. 1), 1-9.
36. Cavalieri, E., Frenkel, K., Liehr, J. G., Rogan, E. and Roy, D. (2000) Estrogens as endogenous genotoxic agents-DNA adducts and mutations. J Natl Cancer Inst Monogr, 27, 75-93.
37. National Toxicology Program. http://ntp-server.niehs.nih.gov (accessed 2011).
38. Kirkland, D., Kasper, P., Muller, L., Corvi, R. and Speit, G. (2008) Recommended lists of genotoxic and non-genotoxic chemicals for assessment of the performance of new or improved genotoxicity tests: A follow-up to an ECVAM workshop. Mutat. Res., 653, 99-108.
39. Corvi, R., Albertini, S., Hartung, T., Hoffmann, S., Maurici, D., Pfuhler, S., van Benthem, J. and van Parys, P. (2008) ECVAM retrospective validation of in vitro micronucleus test (MNT). Mutagenesis, 23, 271-283.
40. IARC (2002) Some Traditional Herbal Medicines, Some Mycotoxins, Naphthalene and Styrene, Monographs on the Evaluation of Carcinogenic Risks to Humans., Vol. 82. Lyon, France.
41. Muller-Tegethoff, K., Kasper, P. and Muller, L. (1995) Evaluation studies on the in vitro rat hepatocyte micronucleus assay. Mutat. Res., 335, 293-307.
42. IARC (1998) Polynuclear Aromatic Compounds, Part 1, Chemical, Environmental and Experimental Data, Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 32. Lyon, France.
43. Knerr, S. and Schrenk, D. (2006) Carcinogenicity of 2,3,7,8- tetrachlorodibenzo-p-dioxin in experimental models. Mol. Nutr. Food Res., 50, 897-907.
44. Ozbay, A., Karamperis, N. and Jorgensen, K. A. (2007) A review of the immunosuppressive activity of cyclosporine metabolites: New insights into an old issue. Curr. Clin. Pharmacol., 2, 244-248.
45. Mitchell, A. D., Auletta, A. E., Clive, D., Kirby, P. E., Moore, M. M. and Myhr, B. C. (1997) The L5178Y/tk+/-mouse lymphoma specific gene and chromosomal mutation assay a phase III report of the U.S. Environmental Protection Agency Gene-Tox Program. Mutat. Res., 394, 177-303.
46. Westerink, W. M., Stevenson, J. C., Lauwers, A., Griffioen, G., Horbach, G. J. and Schoonen, W. G. (2009) Evaluation of the Vitotox and RadarScreen assays for the rapid assessment of genotoxicity in the early research phase of drug development. Mutat. Res., 676, 113-130.
47. Drawz, S. M. and Bonomo, R. A. (2010) Three decades of beta-lactamase inhibitors. Clin. Microbiol. Rev., 23, 160-201.
48. Daniel, K. G., Kuhn, D. J., Kazi, A. and Dou, Q. P. (2005) Antiangiogenic and anti-tumor properties of proteasome inhibitors. Curr. Cancer Drug Targets, 5, 529-541.
49. Cahill, P. A., Billinton, N., Barker, M. G., Walsh, L., Keenan, P. O., Williams, C. V., Tweats, D. J. and Walmsley, R. M. (2004) The GreenScreen genotoxicity assay: A screening validation programme. Mutagenesis, 19, 105-119.
50. Kirkland, D. and Speit, G. (2008) Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens III. Appropriate follow-up testing in vivo. Mutat. Res., 654, 114-132.
51. IARC (1999) Some Chemicals that Cause Tumours of the Kidney or Urinary Bladder in Rodents and Some Other Substances, Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 73. Lyon, France.
52. Bischoff, S. C. (2008) Quercetin: Potentials in the prevention and therapy of disease. Curr. Opin. Clin. Nutr. Metab. Care, 11, 733-740.
53. Kirkland, D., Aardema, M., Muller, L. and Makoto, H. (2006) Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens II. Further analysis of mammalian cell results, relative predictivity and tumour profiles. Mutat. Res., 608, 29-42.
54. Nadal, A., Alonso-Magdalena, P., Ripoll, C. and Fuentes, E. (2005) Disentangling the molecular mechanisms of action of endogenous and environmental estrogens. Pflugers Arch., 449, 335-343.
55. IARC (1987) Steroidal estrogens. Summaries and Evaluations. IARC, (Suppl. 7), Monographs on the Evaluation of Carcinogenic Risks to Humans, Lyon, France.
56. Watters, G. P., Smart, D. J., Harvey, J. S. and Austin, C. A. (2009) H2AX phosphorylation as a genotoxicity endpoint. Mutat. Res., 679, 50-58.
57. Dickey, J. S., Redon, C. E., Nakamura, A. J., Baird, B. J., Sedelnikova, O. A. and Bonner, W. M. (2009) H2AX: Functional roles and potential applications. Chromosoma, 118, 683-692.
58. Skladanowski, A., Bozko, P. and Sabisz, M. (2009) DNA structure and integrity checkpoints during the cell cycle and their role in drug targeting and sensitivity of tumor cells to anticancer treatment. Chem. Rev., 109, 2951-2973.
59. Seki, Y., Toba, K., Fuse, I., Sato, N., Niwano, H., Tanabe, N. and Aizawa, Y. (2005) In vitro effect of cyclosporin A, mitomycin C and prednisolone on cell kinetics in cultured human umbilical vein endothelial cells. Thromb. Res., 115, 219-228.
60. Barhoover, M. A., Hall, J. M., Greenlee, W. F. and Thomas, R. S. (2010) Aryl hydrocarbon receptor regulates cell cycle progression in human breast cancer cells via a functional interaction with cyclin-dependent kinase 4. Mol. Pharmacol., 77, 195-201.
61. Mathijs, K., Brauers, K. J., Jennen, D. G., Boorsma, A., van Herwijnen, M. H., Gottschalk, R. W., Kleinjans, J. C. and van Delft, J. H. (2009) Discrimination for genotoxic and non-genotoxic carcinogens by gene expression profiling in primary mouse hepatocytes improves with exposure time. Toxicol. Sci, 112, 374-384.
62. Staal, Y. C., Hebels, D. G., van Herwijnen, M. H., Gottschalk, R. W., van Schooten, F. J. and van Delft, J. H. (2007) Binary PAH mixtures cause additive or antagonistic effects on gene expression but synergistic effects on DNA adduct formation. Carcinogenesis, 28, 2632-2640.
63. Dai, M., Wang, P., and Boyd, A. D. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res, 33, e175.
64. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U. and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
65. De Groot, P. J., Reiff, C., Mayer, C. and Muller, M. (2008) NuGO contributions to GenePattern. Genes Nutr., 3, 143-146.
66. Guo, L., Lobenhofer, E. K. and Wang, C. (2006) Rat toxicogenomic study reveals analytical consistency across microarray platforms. Nat. Biotechnol., 24, 1162-1169.
67. Tong, W., Cao, X. and Harris, S. (2003) ArrayTrack-supporting toxicogenomic research at the U.S. Food and Drug Administration National Center for Toxicological Research. Environ. Health Perspect., 111, 1819-1826.
68. Tibshirani, R., Hastie, T., Narasimhan, B. and Chu, G. (2002) Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc. Natl Acad. Sci. USA, 99, 6567-6572.
69. Dennis, G., Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol., 4, P3.
70. Baird, W. M., Hooven, L. A. and Mahadevan, B. (2005) Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen., 45, 106-114.
71. Bedard, L. L. and Massey, T. E. (2006) Aflatoxin B1-induced DNA damage and its repair. Cancer Lett., 241, 174-183.
72. Andrysik, Z., Vondracek, J. and Machala, M. (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.
73. Ricordy, R., Gensabella, G., Cacci, E. and Augusti-Tocco, G. (2002) Impairment of cell cycle progression by aflatoxin B1 in human cell lines. Mutagenesis, 17, 241-249.
74. Mandal, P. K. (2005) Dioxin: A review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. B, 175, 221-230.
75. Ye, R., Goodarzi, A. A., Kurz, E. U., Saito, S., Higashimoto, Y., Lavin, M. F., Appella, E., Anderson, C. W. and Lees-Miller, S. P. (2004) The isoflavonoids genistein and quercetin activate different stress signaling pathways as shown by analysis of site-specific phosphorylation of ATM, p53 and histone H2AX. DNA Repair (Amst.), 3, 235-244.
76. Choi, E. J., Bae, S. M. and Ahn, W. S. (2008) Antiproliferative effects of quercetin through cell cycle arrest and apoptosis in human breast cancer MDA-MB-453 cells. Arch. Pharm. Res., 31, 1281-1285.
77. Shan, B. E., Wang, M. X. and Li, R. Q. (2009) Quercetin inhibit human SW480 colon cancer growth in association with inhibition of cyclin D1 and survivin expression through Wnt/beta-catenin signaling pathway. Cancer Invest., 27, 604-612.
78. Tan, J., Wang, B. and Zhu, L. (2009) Regulation of survivin and Bcl-2 in HepG2 cell apoptosis induced by quercetin. Chem. Biodivers., 6, 1101-1110.
79. Zhang, Q., Zhao, X. H. and Wang, Z. J. (2009) Cytotoxicity of flavones and flavonols to a human esophageal squamous cell carcinoma cell line (KYSE-510) by induction of G2/M arrest and apoptosis. Toxicol. In Vitro, 23, 797-807.
80. Tanigawa, S., Fujii, M. and Hou, D. X. (2008) Stabilization of p53 is involved in quercetin-induced cell cycle arrest and apoptosis in HepG2 cells. Biosci. Biotechnol. Biochem., 72, 797-804.
81. Ruiz, P. A., Braune, A., Holzlwimmer, G., Quintanilla-Fend, L. and Haller, D. (2007) Quercetin inhibits TNF-induced NF-kappaB transcription factor recruitment to proinflammatory gene promoters in murine intestinal epithelial cells. J. Nutr., 137, 1208-1215.
82. van der Woude, H., Alink, G. M., van Rossum, B. E., Walle, K., van Steeg, H., Walle, T. and Rietjens, I. M. (2005) Formation of transient covalent protein and DNA adducts by quercetin in cells with and without oxidative enzyme activity. Chem. Res. Toxicol., 18, 1907-1916.
83. Shuck, S. C., Short, E. A. and Turchi, J. J. (2008) Eukaryotic nucleotide excision repair: From understanding mechanisms to influencing biology. Cell Res., 18, 64-72.
84. Gupta, C., Vikram, A., Tripathi, D. N., Ramarao, P. and Jena, G. B. (2010) Antioxidant and antimutagenic effect of quercetin against DEN induced hepatotoxicity in rat. Phytother. Res., 24, 119-128.
85. Ramos, A. A., Lima, C. F., Pereira, M. L., Fernandes-Ferreira, M. and Pereira-Wilson, C. (2008) Antigenotoxic effects of quercetin, rutin and ursolic acid on HepG2 cells: Evaluation by the comet assay. Toxicol. Lett., 177, 66-73.
86. Edenharder, R., Krieg, H., Kottgen, V. and Platt, K. L. (2003) Inhibition of clastogenicity of benzo[a]pyrene and of its trans-7,8-dihydrodiol in mice in vivo by fruits, vegetables, and flavonoids. Mutat. Res., 537, 169-181.
87. Leanderson, P. and Tagesson, C. (1996) Iron bound to the lipophilic iron chelator, 8-hydroxyquinoline, causes DNA strand breakage in cultured lung cells. Carcinogenesis, 17, 545-550.
88. IARC (1990) Summaries & Evaluations-Ampicillin, Vol. 50. Lyon, France.
89. Iso, T., Watanabe, T., Iwamoto, T., Shimamoto, A. and Furuichi, Y. (2006) DNA damage caused by bisphenol A and estradiol through estrogenic activity. Biol. Pharm. Bull., 29, 206-210.
90. Liu,H., Lee, E. S. andGajdos, C. (2003)Apoptotic actionof 17beta-estradiol in raloxifene-resistant MCF-7 cells in vitro and in vivo. J. Natl Cancer Instit., 95, 1586-1597.
91. IARC (1997) Pharmaceutical Drugs. Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 50. Lyon, France.
92. Rubanyi, G. M., Johns, A. and Kauser, K. (2002) Effect of estrogen on endothelial function and angiogenesis. Vascul. Pharmacol., 38, 89-98.
93. Fotsis, T., Zhang, Y., Pepper, M. S., Adlercreutz, H., Montesano, R., Nawroth, P. P. and Schweigerer, L. (1994) The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth. Nature, 368, 237-239.
94. Tsuchiya, Y., Nakajima, M. and Yokoi, T. (2005) Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Lett., 227, 115-124.
95. Shatalova, E. G., Walther, S. E., Favorova, O. O., Rebbeck, T. R. and Blanchard, R. L. (2005) Genetic polymorphisms in human SULT1A1 and UGT1A1 genes associate with breast tumor characteristics: A case-series study. Breast Cancer Res., 7, R909-R921.
96. Zahid, M., Kohli, E., Saeed, M., Rogan, E. and Cavalieri, E. (2006) The greater reactivity of estradiol-3,4-quinone vs estradiol-2,3-quinone with DNA in the formation of depurinating adducts: Implications for tumorinitiating activity. Chem. Res. Toxicol., 19, 164-172.
97. Salama, S. A., Kamel, M., Awad, M., Nasser, A. H., Al-Hendy, A., Botting, S. and Arrastia, C. (2008) Catecholestrogens induce oxidative stress and malignant transformation in human endometrial glandular cells: Protective effect of catechol-O-methyltransferase. Int. J. Cancer, 123, 1246-1254.
98. Iwahori, S., Yasui, Y., Kudoh, A., Sato, Y., Nakayama, S., Murata, T., Isomura, H. and Tsurumi, T. (2008) Identification of phosphorylation sites on transcription factor Sp1 in response to DNA damage and its accumulation at damaged sites. Cell Signal., 20, 1795-1803.
99. Castaneda, F., Rosin-Steiner, S. and Jung, K. (2007) Functional genomics analysis of low concentration of ethanol in human hepatocellular carcinoma (HepG2) cells. Role of genes involved in transcriptional and translational processes. Int. J. Med. Sci., 4, 28-35.
100. Harris, A. J., Dial, S. L. and Casciano, D. A. (2004) Comparison of basal gene expression profiles and effects of hepatocarcinogens on gene expression in cultured primary human hepatocytes and HepG2 cells. Mutat. Res., 549, 79-99.
101. Hockley, S. L., Mathijs, K., Staal, Y. C., Brewer, D., Giddings, I., van Delft, J. H. and Phillips, D. H. (2009) Interlaboratory and interplatform comparison of microarray gene expression analysis of HepG2 cells exposed to benzo(a)pyrene. OMICS, 13, 115-125.
102. Kawata, K., Shimazaki, R. and Okabe, S. (2009) Comparison of gene expression profiles in HepG2 cells exposed to arsenic, cadmium, nickel, and three model carcinogens for investigating the mechanisms of metal carcinogenesis. Environ. Mol. Mutagen., 50, 46-59.