Deregulation of cell proliferation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotoxic events

Toxicological Sciences

Volumn 83, Issue 2, 2005, Pages 246-256

  Plíšková, Martina ^a   Vondráček, Jan ^a,b   Vojtěšek, Bořivoj ^c   Kozubík, Alois ^b   Machala, Miroslav ^a  

^a VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^b INSTITUTE OF BIOPHYSICS   (Czech Republic)

^c MASARYK MEMORIAL CANCER INSTITUTE   (Czech Republic)

Author keywords

Cell cycle; Cell proliferation; Estrogen receptor; p53; PAHs

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; BENZ[A]ANTHRACENE; BENZO[A]PYRENE; CARCINOGEN; DNA; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; MUTAGENIC AGENT; PIFITHRIN ALPHA; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN INHIBITOR; PROTEIN P53; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; CARCINOGENICITY; CELL CYCLE S PHASE; CELL DEATH; CELL PROLIFERATION; CELL SYNCHRONIZATION; CHEMICAL CARCINOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA SYNTHESIS; GENOTOXICITY; HORMONE SENSITIVITY; HUMAN; HUMAN CELL; METABOLITE; MITOSIS INHIBITION; MUTAGENICITY; PROTEIN EXPRESSION;

BENZ(A)ANTHRACENES; BENZO(A)PYRENE; BENZOTHIAZOLES; BREAST NEOPLASMS; BROMODEOXYURIDINE; CARCINOGENS; CARCINOMA; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DNA REPLICATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EPIGENESIS, GENETIC; ESTRADIOL; ESTROGEN ANTAGONISTS; FEMALE; HUMANS; RECEPTORS, ESTROGEN; THIAZOLES; TOLUENE; TUMOR SUPPRESSOR PROTEIN P53;

MINK CELL FOCUS-FORMING VIRUS;

EID: 13644263678     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/kfi040     Document Type: Article

References (42)

1. Arcaro, K. F., O'Keefe, P. W., Yang, Y., Clayton, W., and Gierthy, J. F. (1999). Antiestrogenicity of environmental polycyclic aromatic hydrocarbons in human breast cancer cells. Toxicology 133, 115-127.
2. Binková, B., Černá, M., Pastorková, A., Jelínek, R., Beneš, I., Novák, J., and Šrám, R. J. (2003). Biological activities of organic compounds adsorbed onto ambient air particles: Comparison between the cities of Teplice and Prague during the summer and winter seasons 2000-2001. Mutat. Res. 525, 43-59.
3. Binková B, and Šrám, R. J. (2004). The genotoxic effect of carcinogenic PAHs, their artificial and environmental mixtures (EOM) on human diploid lung fibroblasts. Mutat. Res. 547, 109-121.
4. Bolton, J. L., Trush, M. A., Penning, T. M., Dryhurst, G., and Monks, T. J. (2000). Role of quinones in toxicology. Chem. Res. Toxicol. 13, 135-160.
5. Burdick, A. D., Davis, J. W., 2nd, Liu, K. J., Hudson, L. G., Shi, H., Monske, M. L., and Burchiel, S. W. (2003). Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Res. 63, 7825-7833.
6. Chaloupka, K., Krishnan, V., and Safe, S. (1992). Polynuclear aromatic hydrocarbon carcinogens as antiestrogens in MCF-7 human breast cancer cells: Role of the Ah receptor. Carcinogenesis 13, 2233-2239.
7. Charles, G. D., Bartels, M. J., Zacharewski, T. R., Gollapudi, B. B., Freshour, N. L., and Carney, E. W. (2000). Activity of benzo[a]pyrene and its hydroxylated metabolites in an estrogen receptor-alpha reporter gene assay. Toxicol. Sci. 55, 320-326.
8. Chen, S., Nguyen, N., Tamura, K., Karin, M., and Tukey, R. H. (2003). The role of the Ah receptor and p38 in benzo[alpyrene-7,8-dihydrodiol and benzo[a]pyrene-7,8-dihydrodiol-9,10-epoxide-induced apoptosis. J. Biol. Chem. 278, 19526-19533.
9. Chramostová, K., Vondráček, J., Š indlerová, L., Vojtěšek, B., Kozubík, A., and Machala, M. (2004). Polycyclic aromatic hydrocarbons modulate cell proliferation in rat hepatic epithelial stem-like WB-F344 cells. Toxicol. Appl. Pharmacol. 196, 136-148.
10. 10 air particulate material using in vitro gene expression assays. Environ. Sci. Technol. 32, 1853-1860.
11. Dipple, A., Khan, Q. A., Page, J. E., Ponten, I., and Szeliga, J. (1999). DNA reactions, mutagenic action and stealth properties of polycyclic aromatic hydrocarbon carcinogens (review). Int. J. Oncol. 14, 103-111.
12. Fertuck, K. C., Kumar, S., Sikka, H. C., Matthews, J. B., and Zacharewski, T. R. (2001). Interaction of PAH-related compounds with the alpha and beta isoforms of the estrogen receptor. Toxicol. Lett. 121, 167-177.
13. Foster, J. S., Henley, D. C., Ahamed, S., and Wimalasena, J. (2001). Estrogens and cell-cycle regulation in breast cancer. Trends Endocrinol. Metab. 12, 320-327.
14. Gábelová, A., Valovičová, Z., Horváthová, E., Slameňová, D., Binková, B., Šrám, R. J., and Farmer, P. B. (2004). Genotoxicity of environmental air pollution in three European cities: Prague, Kosice and Sofia. Mutat. Res. 563, 49-59.
15. Gozgit, J. M., Nestor, K. M., Fasco, M. J., Pentecost, B. T., and Arcaro, K. F. (2004). Differential action of polycyclic aromatic hydrocarbons on endogenous estrogen-responsive genes and on a transfected estrogen-responsive reporter in MCF-7 cells. Toxicol. Appl. Pharmacol. 196, 58-67.
16. Hecht, S. S. (2002). Tobacco smoke constituents and breast cancer. Environ. Mol. Mutagen. 39, 119-126.
17. Hoffmann, D., Hoffmann, I., and El-Bayoumy, K. (2001). The less harmful cigarette: A controversial issue. A tribute to Ernst L. Wynder. Chem. Res. Toxicol. 14, 767-790.
18. Jeffy, B. D., Chirnomas, R. B., Chen, E. J., Gudas, J. M., and Romagnolo, D. F. (2002). Activation of the aromatic hydrocarbon receptor pathway is not sufficient for transcriptional repression of BRCA-1: requirements for metabolism of benzo[a]pyrene to 7r,8t-dihydroxy-9t,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene. Cancer Res. 62, 113-121.
19. Jeffy, B. D., Schultz, E. U., Selmin, O., Gudas, J. M., Bowden, G. T., and Romagnolo, D. (1999). Inhibition of BRCA-1 expression by benzo[a]pyrene and its diol epoxide. Mol. Carcinogenesis 26, 100-118.
20. Jones, J. M., Anderson, J. W., and Tukey, R. H. (2000). Using the metabolism of PAHs in a human cell line to characterize environmental samples. Environ. Toxicol. Pharmacol. 8, 119-126.
21. 1 arrest in MCF-7 cells. Carcinogenesis 21, 1611-1618.
22. Klaunig, J. E., Kamendulis, L. M., and Xu, Y. (2000). Epigenetic mechanisms of chemical carcinogenesis. Hum. Exp. Toxicol. 19, 543-555.
23. Komarov, P. G., Komarova, E. A., Kondratov, R. V., Christov-Tselkov, K., Coon, J. S., Chernov, M. V., and Gudkov, A. V. (1999). A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285, 1733-1737.
24. Levitzki, A., and Gazit, A. (1995). Tyrosine kinase inhibition: an approach to drug development. Science 267, 1782-1788.
25. Machala, M., Vondráček, J., Bláha, L., Ciganek, M., and Neča, J. (2001). Aryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay. Murat. Res. 497, 49-62.
26. Melendez-Colon, V. J., Luch, A., Seidel, A., and Baird, W. M. (1999). Comparison of cytochrome P450- and peroxidase-dependent metabolic activation of the potent carcinogen dibenzo[a,1]pyrene in human cell lines: Formation of stable DNA adducts and absence of a detectable increase in apurinic sites. Cancer Res. 59, 1412-1416.
27. Melendez-Colon, V. J., Luch, A., Seidel, A., and Baird, W. M. (2000). Formation of stable DNA adducts and apurinic sites upon metabolic activation of bay and fjord region polycyclic aromatic hydrocarbons in human cell cultures. Chem. Res. Toxicol. 13, 10-17.
28. Pearce, S. T., Liu, H., Radhakrishnan, I., Abdelrahim, M., Safe, S., and Jordan, V. C. (2004). Interaction of the aryl hydrocarbon receptor ligand 6-methyl 1,3,8-trichlorodibenzofuran with estrogen receptor alpha. Cancer Res. 64, 2889-2897.
29. Ramet, M., Castren, K., Jarvinen, K., Pekkala, K., Turpeenniemi-Hujanen, T., Soini, Y., Paakko, P., and Vahakangas, K. (1995). p53 protein expression is correlated with benzo[a]pyrene-DNA adducts in carcinoma cell lines. Carcinogenesis 16, 2117-2124.
30. Roberts, R. A., Nebert, D. W., Hickman, J. A., Richburg, J. H., and Goldsworthy, T. L. (1997). Perturbation of the mitosis/apoptosis balance: A fundamental mechanism in toxicology. Fundam. Appl. Toxicol. 38, 107-115.
31. Safe, S., and Wörmke, M. (2003). Inhibitory aryl hydrocarbon receptor-estrogen receptor alpha cross-talk and mechanisms of action. Chem. Res. Toxicol. 16, 807-816.
32. Shimada, T., and Fujii-Kuriyama, Y. (2004). Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci. 95, 1-6.
33. Soto, A. M., Sonnenschein, C., Chung, K. L., Fernandez, M. F., Olea, N., and Serrano, F. O. (1995). The E-SCREEN assay as a tool to identify estrogens: An update on estrogenic environmental pollutants. Environ. Health Perspect. 103(Suppl. 7), 113-122.
34. Tsai, K. S., Yang, R. S., and Liu, S. H. (2004). Benzo[a]pyrene regulates osteoblast proliferation through an estrogen receptor-related cyclooxygen-2 pathway. Chem. Res. Toxicol. 17, 679-684.
35. Vindelov, L. L. (1977). Flow microfluorometric analysis of nuclear DNA in cells from solid tumors and cell suspensions. A new method for rapid isolation and straining of nuclei. Virchows Arch. B. Cell. Pathol. 24, 227-242.
36. Vojtěšek, B., Bártek, J., Midgley, C. A., and Lane, D. P. (1992). An immunochemical analysis of the human nuclear phosphoprotein p53. New monoclonal antibodies and epitope mapping using recombinant p53. J. Immunol. Methods 151, 237-244.
37. 1-S-phase transition by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells. Toxicol. Sci. 70, 193-201.
38. Vousden, K. H. (2000). p53: Death star. Cell 103, 691-694.
39. Wakeling, A. E. (1995). Use of pure antioestrogens to elucidate the mode of action of oestrogens. Biochem. Pharmacol. 49, 1545-1549.
40. Wang, W. L., Smith, R., and Safe, S. (1998). Aryl hydrocarbon receptor-mediated antiestrogenicity in MCF-7 cells: Modulation of hormone-induced cell cycle enzymes. Arch. Biochem. Biophys. 356, 239-248.
41. WHO (1998). Selected Non-heterocyclic Polycyclic Aromatic Hydrocarbons. WHO Geneva.
42. Zhou, B. B, and Elledge, S. J. (2000). The DNA damage response: Putting checkpoints in perspective. Nature 408, 433-439.