2,3,7,8-Tetrachlorodibenzo-p-dioxin modulates the induction of DNA strand breaks and poly(ADP-ribose) polymerase-1 activation by 17β-estradiol in human breast carcinoma cells through alteration of CYP1A1 and CYP1B1 expression

Chemical Research in Toxicology

Volumn 21, Issue 7, 2008, Pages 1337-1347

  Lin, Po Hsiung ^a   Lin, Chia Hua ^a   Huang, Chuan Chen ^a   Fang, Ju Pin ^a   Chuang, Ming Chieh ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; REACTIVE OXYGEN METABOLITE;

ARTICLE; BREAST CANCER; CANCER CELL; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; WESTERN BLOTTING;

BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; COMET ASSAY; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 ENZYME SYSTEM; DNA; DNA BREAKS; DRUG ANTAGONISM; ENZYME INDUCTION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GLUTATHIONE; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; TETRACHLORODIBENZODIOXIN;

EID: 49049103956     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx700396d     Document Type: Article

References (67)

1. IARC (International Agency for Research on Cancer) (1997) Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, pp33-344, IARC Monographs, Lyon, France.
2. Crump, K. S., Canady, R., and Kogevinas, M. (2003) Meta-analysis of dioxin cancer dose response for three occupational cohorts. Environ. Health Perspect. 111, 681-687.
3. Steenland, K., and Deddens, J. A. (2004) A practical guide to dose-response analyses and risk assessment in occupational epidemiology. Epidemiology 15, 63-70.
4. Grassman, J. A., Masten, S. A., Walker, N. J., and Lucier, G. W. (1998) Animal models of human response to dioxins. Environ. Health Perspect. 106, 761-775.
5. Warner, M., Eskenazi, B., Mocarelli, P., Gerthoux, P. M., Samuels, S., Needham, L., Patterson, D., and Brambilla, P. (2002) Serum dioxin concentrations and breast cancer risk in the seveso women's health study. Environ. Health Perspect. 110, 625-628.
6. Poland, A., and Knutson, J. C. (1982) 2,3,7,8-tetrachlorodibenzo -p-dioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 22, 517-554.
7. Poellinger, L. (2000) Mechanistic aspects-the dioxin (aryl hydrocarbon) receptor. Food Addit. Contam. 17, 261-266.
8. Yager, J. D. (2000) Endogenous estrogens as carcinogens through metabolic activation. J. Natl. Cancer. Inst. Monogr. 27, 67-73.
9. Hayes, C. L., Spink, D. C., Spink, B. C., Cao, J. Q., Walker, N. J., and Sutter, T. R. (1996) 17 Beta-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93, 9776-9781.
10. Pang, S., Cao, J. Q., Katz, B. H., Hayes, C. L., Sutter, T. R., and Spink, D. C. (1999) Inductive and inhibitory effects of non-orthosubstituted polychlorinated biphenyls on estrogen metabolism and human cytochromes P450 1A1 and 1B1. Biochem. Pharmacol. 58, 29-38.
11. Sanderson, J. T., Slobbe, L., Lansbergen, G. W., Safe, S., and van den Berg, M. (2001) 2,3,7,8-tetrachlorodibenzo-p-dioxin and diindolylmethanes differentially induce cytochrome P450 1A1, 1B1, and 19 in H295R human adrenocortical carcinoma cells. Toxicol. Sci. 61, 40-48.
12. Spencer, D. L., Masten, S. A., Lanier, K. M., Yang, X., Grassman, J. A., Miller, C. R., Sutter, T. R., Lucier, G. W., and Walker, N. J. (1999) Quantitative analysis of constitutive and 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced cytochrome P450 1B1 expression in human lymphocytes. Cancer Epidemiol. Biomarkers Prev. 8, 139-146.
13. Badawi, A. F., Cavalieri, E. L., and Rogan, E. G. (2000) Effect of chlorinated hydrocarbons on expression of cytochrome P450 1A1, 1A2 and 1B1 and 2- and 4-hydroxylation of 17beta-estradiol in female sprague-dawley rats. Carcinogenesis 21, 1593-1599.
14. Yager, J. D., and Liehr, J. G. (1996) Molecular mechanisms of estrogen carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 36, 203-232.
15. van Duursen, M. B., Sanderson, J. T., van der Bruggen, M., van der Linden, J., and van den Berg, M. (2003) Effects of several dioxin-like compounds on estrogen metabolism in the malignant MCF-7 and nontumorigenic MCF-10A human mammary epithelial cell lines. Toxicol. Appl. Pharmacol. 190, 241-250.
16. Lavigne, J. A., Goodman, J. E., Fonong, T., Odwin, S., He, P., Roberts, D. W., and Yager, J. D. (2001) The effects of catechol-O-methyl-transferase inhibition on estrogen metabolite and oxidative DNA damage levels in estradiol-treated MCF-7 cells. Cancer Res. 61, 7488-7494.
17. Han, X., and Liehr, J. G. (1994) DNA single-strand breaks in kidneys of Syrian hamsters treated with steroidal estrogens: Hormone-induced free radical damage preceding renal malignancy. Carcinogenesis 15, 997-1000.
18. Wang, M. Y., and Liehr, J. G. (1995) Induction by estrogens of lipid peroxidation and lipid peroxide-derived malonaldehyde-DNA adducts in male Syrian hamsters: Role of lipid peroxidation in estrogen-induced kidney carcinogenesis. Carcinogenesis 16, 1941-1945.
19. Yared, E., McMillan, T. J., and Martin, F. L. (2002) Genotoxic effects of oestrogens in breast cells detected by the micronucleus assay and the comet assay. Mutagenesis 17, 345-352.
20. Lu, F., Zahid, M., Saeed, M., Cavalieri, E. L., and Rogan, E. G. (2007) Estrogen metabolism and formation of estrogen-DNA adducts in estradiol-treated MCF-10F cells: The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin induction and catechol-O-methyltransferase inhibition. J. Steroid Biochem. Mol. Biol. 105, 150-158.
21. Martucci, C. P., and Fishman, J. (1993) P450 enzymes of estrogen metabolism. Pharmacol. Ther. 57, 237-257.
22. Yamazaki, H., Shaw, P. M., Guengerich, F. P., and Shimada, T. (1998) Roles of cytochromes P450 1A2 and 3A4 in the oxidation of estradiol and estrone in human liver microsomes. Chem. Res. Toxicol. 11, 659-665.
23. Spink, D. C., Spink, B. C., Cao, J. Q., Gierthy, J. F., Hayes, C. L., Li, Y., and Sutter, T. R. (1997) Induction of cytochrome P450 1B1 and catechol estrogen metabolism in ACHN human renal adenocarcinoma cells. J. Steroid Biochem. Mol. Biol. 62, 223-232.
24. Butterworth, M., Lau, S. S., and Monks, T. J. (1996) 17 beta-estradiol metabolism by hamster hepatic microsomes: Comparison of catechol estrogen O-methylation with catechol estrogen oxidation and glutathione conjugation. Chem. Res. Toxicol. 9, 793-799.
25. Cao, K., Stack, D. E., Ramanathan, R., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (1998) Synthesis and structure elucidation of estrogen quinones conjugated with cysteine, N-acetylcysteine, and glutathione. Chem. Res. Toxicol. 11, 909-916.
26. Iverson, S. L., Shen, L., Anlar, N., and Bolton, J. L. (1996) Bioactivation of estrone and its catechol metabolites to quinoid-glutathione conjugates in rat liver microsomes. Chem. Res. Toxicol. 9, 492-499.
27. Service, R. F. (1998) New role for estrogen in cancer? Science 279, 1631-1633.
28. 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.
29. Akanni, A., and Abul-Hajj, Y. J. (1999) Estrogen-nucleic acid adducts: Dissection of the reaction of 3,4-estrone quinone and its radical anion and radical cation with deoxynucleosides and DNA. Chem. Res. Toxicol. 12, 1247-1253.
30. Convert, O., Van Aerden, C., Debrauwer, L., Rathahao, E., Molines, H., Fournier, F., Tabet, J. C., and Paris, A. (2002) Reactions of estradiol-2,3-quinone with deoxyribonucleosides: Possible insights in the reactivity of estrogen quinones with DNA. Chem. Res. Toxicol. 15, 754-764.
31. Dwivedy, I., Devanesan, P., Cremonesi, P., Rogan, E., and Cavalieri, E. (1992) Synthesis and characterization of estrogen 2,3- and 3,4-quinones. Comparison of DNA adducts formed by the quinones versus horseradish peroxidase-activated catechol estrogens. Chem. Res. Toxicol. 5, 828-833.
32. Jankowiak, R., Zamzow, D., Stack, D. E., Todorovic, R., Cavalieri, E. L., and Small, G. J. (1998) Spectral characterization of fluorescently labeled catechol estrogen 3,4-quinone-derived N7 guanine adducts and their identification in rat mammary gland tissue. Chem. Res. Toxicol. 11, 1339-1345.
33. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., Ramanathan, R., Cerny, R. L., and Rogan, E. G. (1997) Molecular origin of cancer: Catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U.S.A. 94, 10937-10942.
34. Cavalieri, E. L., Devanesan, P., Bosland, M. C., Badawi, A. F., and Rogan, E. G. (2002) Catechol estrogen metabolites and conjugates in different regions of the prostate of noble rats treated with 4-hydroxyestradiol: Implications for estrogen-induced initiation of prostate cancer. Carcinogenesis 23, 329-333.
35. Zahid, M., Kohli, E., Saeed, M., Rogan, E. G., and Cavalieri, E. L. (2006) The greater reactivity of estradiol-3,4-quinone vs estradiol-2,3-quinone with DNA in the formation of depurinating adducts: implications for tumor-initiating activity. Chem. Res. Toxicol. 19, 164-172.
36. Chakravarti, D., Mailander, P. C., Li, K. M., Higginbotham, S., Zhang, H. L., Gross, M. L., Meza, J. L., Cavalieri, E. L., and Rogan, E. G. (2001) Evidence that a burst of DNA depurination in SENCAR mouse skin induces error-prone repair and forms mutations in the H-ras gene. Oncogene 20, 7945-7953.
37. Mailander, P. C., Meza, J. L., Higginbotham, S., and Chakravarti, D. (2006) Induction of A.T to G.C mutations by erroneous repair of depurinated DNA following estrogen treatment of the mammary gland of ACI rats. J. Steroid Biochem. Mol. Biol. 101, 204-215.
38. Burrows, C. J., and Muller, J. G. (1998) Oxidative nucleobase modifications leading to strand scission. Chem. Rev. 98, 1109-1152.
39. Breen, A. P., and Murphy, J. A. (1995) Reactions of oxyl radicals with DNA. Free Radical Biol. Med. 18, 1033-1077.
40. Miura, T., Muraoka, S., Fujimoto, Y., and Zhao, K. (2000) DNA strand break and 8-hydroxyguanine formation induced by 2-hydroxyestradiol dispersed in liposomes. J. Steroid Biochem. Mol. Biol. 74, 93-98.
41. Lin, P. H., Nakamura, J., Yamaguchi, S., Asakura, S., and Swenberg, J. A. (2003) Aldehydic DNA lesions induced by catechol estrogens in calf thymus DNA. Carcinogenesis 24, 1133-1141.
42. + as a metabolic link between DNA damage and cell death. J. Neurosci. Res. 79, 216-223.
43. Simonin, F., Poch, O., Delarue, M., and de Murcia, G. (1993) Identification of potential active-site residues in the human poly(ADP-ribose) polymerase. J. Biol. Chem. 268, 8529-8535.
44. Althaus, F. R., and Richter, C. (1987) ADP-ribosylation of proteins. Enzymology and biological significance. Mol. Biol. Biochem. Biophys. 37, 1-237.
45. Skidmore, C. J., Davies, M. I., Goodwin, P. M., Halldorsson, H., Lewis, P. J., Shall, S., and Zia'ee, A. A. (1979) The involvement of poly(ADP-ribose) polymerase in the degradation of NAD caused by gamma-radiation and N-methyl-N-nitrosourea. Eur. J. Biochem. 101, 135-142.
46. Nakamura, J., Asakura, S., Hester, S. D., de Murcia, G., Caldecott, K. W., and Swenberg, J. A. (2003) Quantitation of intracellular NAD(P)H can monitor an imbalance of DNA single strand break repair in base excision repair deficient cells in real time. Nucleic Acids Res. 31, e104.
47. Lin, P. H., Lin, C. H., Huang, C. C., Chuang, M. C., and Lin, P. (2007) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces oxidative stress, DNA strand breaks, and poly(ADP-ribose) polymerase-1 activation in human breast carcinoma cell lines. Toxicol. Lett. 172, 146-158.
48. Mobley, J. A., and Brueggemeier, R. W. (2004) Estrogen receptor-mediated regulation of oxidative stress and DNA damage in breast cancer. Carcinogenesis 25, 3-9.
49. Rajapakse, N., Butterworth, M., and Kortenkamp, A. (2005) Detection of DNA strand breaks and oxidized DNA bases at the single-cell level resulting from exposure to estradiol and hydroxylated metabolites. Environ. Mol. Mutagen. 45, 397-404.
50. Skehan, P., Storeng, R., Scudiero, D., Monks, A., McMahon, J., Vistica, D., Warren, J. T., Bokesch, H., Kenney, S., and Boyd, M. R. (1990) New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst. 82, 1107-1112.
51. Lin, C. H., Leow, H. T., Huang, S. C., Nakamura, J., Swenberg, J. A., and Lin, P. H. (2005) Induction of cytotoxicity, aldehydic DNA lesions, and poly(ADP-ribose) polymerase-1 activation by catechol derivatives of pentachlorophenol in calf thymus DNA and in human breast cancer cells. Chem. Res. Toxicol. 18, 257-264.
52. Sasaki, J. C., Arey, J., Eastmond, D. A., Parks, K. K., and Grosovsky, A. J. (1997) Genotoxicity induced in human lymphoblasts by atmospheric reaction products of naphthalene and phenanthrene. Mutat. Res. 393, 23-35.
53. Siraki, A. G., Chan, T. S., and O'Brien, P. J. (2004) Application of quantitative structure-toxicity relationships for the comparison of the cytotoxicity of 14 p-benzoquinone congeners in primary cultured rat hepatocytes versus PC12 cells. Toxicol. Sci. 81, 148-159.
54. Sing, N. P., McCoy, M. T., Tice, R. R., and Schneider, E. L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175, 84-191.
55. Vodenicharov, M. D., Ghodgaonkar, M. M., Halappanavar, S. S., Shah, R. G., and Shah, G. M. (2005) Mechanism of early biphasic activation of poly(ADP-ribose) polymerase-1 in response to ultraviolet B radiation. J. Cell Sci. 118, 589-599.
56. Chang, J. T., Chang, H., Chen, P. H., Lin, S. L., and Lin, P. (2007) Requirement of AhR overexpression for CYP1B1 up-regulation and cell growth in human lung adenocarcinomas. Clin. Cancer Res. 13, 38-45.
57. Coumoul, X., Diry, M., Robillot, C., and Barouki, R. (2001) Differential regulation of cytochrome P450 1A1 and 1B1 by a combination of dioxin and pesticides in the breast tumor cell line MCF-7. Cancer Res. 61, 3942-3948.
58. Spink, D. C., Spink, B. C., Cao, J. Q., DePasquale, J. A., Pentecost, B. T., Fasco, M. J., Li, Y., and Sutter, T. R. (1998) Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 19, 291-298.
59. Angus, W. G., Larsen, M. C., and Jefcoate, C. R. (1999) Expression of CYP1A1 and CYP1B1 depends on cell-specific factors in human breast cancer cell lines: Role of estrogen receptor status. Carcinogenesis 20, 947-955.
60. Cheng, Z., Rios, G. R., King, C. D., Coffman, B. L., Green, M. D., Mojarrabi, B., Mackenzie, P. I., and Tephly, T. R. (1998) Glucuronidation of catechol estrogens by expressed human UDP-glucuronosyltransferases (UGTs) 1A1, 1A3, and 2B7. Toxicol. Sci. 45, 52-57.
61. Guldberg, H. C., and Marsden, C. A. (1975) Catechol-O-methyl transferase: Pharmacological aspects and physiological role. Pharmacol. Rev. 27, 135-206.
62. Falany, J. L., and Falany, C. N. (1996) Expression of cytosolic sulfotransferases in normal mammary epithelial cells and breast cancer cell lines. Cancer Res. 56, 1551-1555.
63. Tenhunen, J., Salminen, M., Lundstrom, K., Kiviluoto, T., Savolainen, R., and Ulmanen, I. (1994) Genomic organization of the human catechol O-methyltransferase gene and its expression from two distinct promoters. Eur. J. Biochem. 223, 1049-1059.
64. Dohr, O., Vogel, C., and Abel, J. (1995) Different response of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-sensitive genes in human breast cancer MCF-7 and MDA-MB 231 cells. Arch. Biochem. Biophys. 321, 405-412.
65. Liu, X., Yao, J., Pisha, E., Yang, Y., Hua, Y., van Breemen, R. B., and Bolton, J. L. (2002) Oxidative DNA damage induced by equine estrogen metabolites: Role of estrogen receptor alpha. Chem. Res. Toxicol. 15, 512-519.
66. Gelinas, S., Bureau, G., Valastro, B., Massicotte, G., Cicchetti, F., Chiasson, K., Gagne, B., Blanchet, J., and Martinoli, M. G. (2004) Alpha and beta estradiol protect neuronal but not native PC12 cells from paraquat-induced oxidative stress. Neurotoxic. Res. 6, 141-148.
67. Lin, C. H., and Lin, P. H. (2006) Induction of ROS formation, poly (ADP-ribose) polymerase-1 activation and cell death by PCB126 and PCB153 in human T47D and MDA-MB-231 breast cancer cells. Chem.-Biol. Interact. 162, 181-194.