Induction of cytochrome P450 1A1 in MCF-7 human breast cancer cells by 4-chlorobiphenyl (PCB3) and the effects of its hydroxylated metabolites on cellular apoptosis

Environment International

Volumn 36, Issue 8, 2010, Pages 935-941

  Ptak, Anna ^a   Ludewig, Gabriele ^b   Rak, Agnieszka ^a   Nadolna, Weronika ^a   Bochenek, Michał ^c   Gregoraszczuk, Ewa L ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b UNIVERSITY OF IOWA   (United States)

^c NATIONAL RESEARCH INSTITUTE OF ANIMAL PRODUCTION   (Poland)

Author keywords

3,4diOH PCB3; 4OH PCB3; Apoptosis; CYPs activity; MCF 7 cell line; PCB3

Indexed keywords

ASSAYS; BIOMOLECULES; CELL CULTURE; CELL DEATH; CYTOLOGY; DISEASES; ENZYME ACTIVITY; ENZYMES; HYDROXYLATION; METABOLITES; ORGANIC POLLUTANTS; POLYCHLORINATED BIPHENYLS; PROTEINS;

3,4DIOH-PCB3; 4OH-PCB3; ANTI-APOPTOTIC EFFECTS; CYTOCHROME P450 ENZYMES; HYDROXYLATED METABOLITES; MCF-7 CELLS; MCF-7 HUMAN BREAST CANCER CELLS; PCB3;

CELLS;

3',4' DIHYDROXY 4 CHLOROBIPHENYL; 4 CHLOROBIPHENYL; 4' HYDROXY 4 CHLOROBIPHENYL; CASPASE 8; CASPASE 9; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; ESTRADIOL; ESTROGEN; POLYCHLORINATED BIPHENYL DERIVATIVE; STAUROSPORINE; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER; CARCINOGEN; CYTOCHROME; ENZYME ACTIVITY; METABOLITE; PCB;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CELL GROWTH; CELL LEVEL; CELL STRAIN MCF 7; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INDUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; NICK END LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

EID: 77957234995     PISSN: 01604120     EISSN: 18736750     Source Type: Journal    
DOI: 10.1016/j.envint.2009.06.012     Document Type: Article

References (51)

1. Amaro A.R., Oakley G.G., Bauer U., Spielmann H.P., Robertson L.W. Metabolic activation of PCBs to quinones: reactivity toward nitrogen and sulfur nucleophiles and influence of superoxide dismutase. Chem Res Toxicol 1996, 9:623-629.
2. Aoyama T., Korzekwa K., Nagata K., Gillette J., Gelboin H.V., Gonzalez F.J. Estradiol metabolism by complementary deoxyribonucleic acid-expressed human cytochrome P450s. Endocrinology 1990, 126:3101-3106.
3. Bandiera S., Safe S., Okey A.B. Binding of polychlorinated biphenyls classified as either phenobarbitone-, 3-methylcholanthrene- or mixed-type inducers to cytosolic Ah receptor. Chem Biol Interact 1982, 39:259-277.
4. Bauer U., Amaro A.R., Robertson L.W. A new strategy for the synthesis of polychlorinated biphenyl metabolites. Chem Res Toxicol 1995, 8:92-95.
5. Bohnenberger S., Wagner B., Schmitz H.J., Schrenk D. Inhibition of apoptosis in rat hepatocytes treated with 'non-dioxin-like' polychlorinated biphenyls. Carcinogenesis 2001, 22:1601-1606.
6. Bröker L.E., Kruyt F.A., Giaccone G. Cell death independent of caspases: a review. Clin Cancer Res 2005, 11:3155-3162.
7. Chun Y.J., Kim S., Kim D., Lee S.K., Guengerich F.P. A new selective and potent inhibitor of human cytochrome P450 1B1 and its application to antimutagenesis. Cancer Res 2001, 61:8164-8170.
8. Ciolino H.P., MacDonald C.J., Yeh G.C. Inhibition of carcinogen-activating enzymes by 16alpha-fluoro-5-androsten-17-one. Cancer Res 2002, 62:3685-3690.
9. de Bruin E.C., Medema J.P. Apoptosis and non-apoptotic deaths in cancer development and treatment response. Cancer Treatment Reviews 2008, 34:737-749.
10. Dorgan J.F., Brock J.W., Rothman N., Needham L.L., Miller R., Stephenson H.E., et al. Serum organochlorine pesticides and PCBs and breast cancer risk: results from a prospective analysis (USA). Cancer Causes Control 1999, 10:1-11.
11. Espandiari P., Glauert H.P., Lehmler H.J., Lee E.Y., Srinivasan C., Robertson L.W. Initiating activity of 4-chlorobiphenyl metabolites in the resistant hepatocyte model. Toxicol Sci 2004, 79:41-46.
12. Gregoraszczuk E.L., Sowa M., Kajta M., Ptak A., Wójtowicz A. Effect of PCB 126 and PCB 153 on incidence of apoptosis in cultured theca and granulosa cells collected from small, medium and large preovulatory follicles. Reprod Toxicol 2003, 17:465-471.
13. Gregoraszczuk E.L., Zemla M., Ptak A., Grabic R. The action of low- and high-chlorinated biphenyl mixture on prepubertal porcie ovary: steroid secretion and cells apoptosis. Endocr Regul 2005, 39:33-41.
14. Gregoraszczuk E.L., Rak A., Ludewig G., Gasińska A. Effects of estradiol, PCB3, and their hydroxylated metabolites on proliferation, cell cycle, and apoptosis of human breast cancer cells. Environ Toxicol Pharmacol 2008, 25:227-233.
15. Güttes S., Failing K., Neumann K., Kleinstein J., Georgii S., Brunn H. Chlororganic pesticides and polychlorinated biphenyls in breast tissue of women with benign and malignant breast disease. Arch Environ Contam Toxicol 1998, 35:140-147.
16. Haag-Grönlund M., Conolly R., Scheu G., Wärngård L., Fransson-Steen R. Analysis of rat liver foci growth with a quantitative two-cell model after treatment with 2, 4, 5, 3', 4'-pentachlorobiphenyl. Toxicol Sci 2000, 57:32-42.
17. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
18. Harrad S., Hazrati S., Ibarra C. Concentrations of polychlorinated biphenyls in indoor air and polybrominated diphenyl ethers in indoor air and dust In Birmingham, United Kingdom: implications for human exposure. Environ Sci Technol 2006, 40:4633-4638.
19. Hayes C.L., Spink D.C., Spink B.C., Cao J.Q., Walker N.J., Sutter T.R. 17 beta-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc Natl Acad Sci U S A 1996, 93:9776-9781.
20. Ishikawa Y., Noma Y., Mori Y., Sakai S. Congener profiles of PCB and a proposed new set of indicator congeners. Chemosphere 2007, 67:1838-1851.
21. Johnstone R.W., Rueflim A.A., Lowe S.W. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002, 108:153-164. Jan.
22. Kolaja K.L., Engelken D.T., Klaassen C.D. Inhibition of gap-junctional intercellular communication in intact rat liver by nongenotoxic hepatocarcinogens. Toxicology 2000, 146:15-22. Apr.
23. Laden F., Ishibe N., Hankinson S.E., Wolff M.S., Gertig D.M., Hunter D.J., et al. Polychlorinated biphenyls, cytochrome P450 1A1, and breast cancer risk in the Nurses' Health Study. Cancer Epidemiol Biomarkers Prev 2002, 11:1560-1565.
24. Layton A.C., Sanseverino J., Gregory B.W., Easter J.P., Sayler G.S., Schultz T.W. In vitro estrogen receptor binding of PCBs: measured activity and detection of hydroxylated metabolites in a recombinant yeast assay. Toxicol Appl Pharmacol 2002, 180:157-163.
25. Lehmler H.J., Robertson L.W. Synthesis of hydroxylated PCB metabolites with the Suzuki-coupling. Chemosphere 2001, 45:1119-1127.
26. Li Y., Millikan R.C., Bell D.A., Cui L., Tse C.K., Newman B., et al. Polychlorinated biphenyls, cytochrome P450 1A1 (CYP1A1) polymorphisms, and Brest cancer risk among African American women and white women in North Carolina: a population-based case-control study. Breast Cancer Res 2005, 7:12-18.
27. Lucena R.A., Allam M.F., Costabeber I.H., Villarejo M.L., Navajas R.F. Breast cancer risk factors: PCB congeners. Eur J Cancer Prev 2001, 10:117-119.
28. Machala M., Blaha L., Lehmler H.J., Pliskova M., Majkova Z., Kapplova P., et al. Toxicity of hydroxylated and quinoid PCB metabolites: inhibition of gap junctional intercellular communication and activation of aryl hydrocarbon and estrogen receptors in hepatic and mammary cells. Chem Res Toxicol 2004, 17:340-347.
29. Martucci C.P., Fishman J. P450 enzymes of estrogen metabolism. Pharmacol Ther 1993, 57:237-257.
30. McLean M.R., Bauer U., Amaro A.R., Robertson L.W. Identification of catechol and hydroquinone metabolites of monochlorobiphenyl. Chem Res Toxicol 1996, 9:158-164.
31. Mortensen A.S., Arukwe A. Interactions between estrogen- and Ah-receptor signalling pathways in primary culture of salmon hepatocytes exposed to nonylphenol and 3,3',4,4'-tetrachlorobiphenyl (congener 77). Comp Hepatol 2007, 6(2).
32. Moysich K.B., Shields P.G., Freudenheim J.L., Schisterman E.F., Vena J.E., Kostyniak P., et al. Polychlorinated biphenyls, cytochrome P4501A1 polymorphism, and postmenopausal breast cancer risk. Cancer Epidemiol Biomarkers Prev 1999, 8:41-44.
33. Oakley G.G., Devanaboyina U., Robertson L.W., Gupta R.C. Oxidative DNA damage induced by activation of polychlorinated biphenyls (PCBs): implications for PCB-induced oxidative stress in breast cancer. Chem Res Toxicol 1996, 9:1285-1292.
34. Pang S., Cao J.Q., Katz B.H., Hayes C.L., Sutter T.R., Spink D.C. Inductive and inhibitory effects of non-ortho-substituted polychlorinated biphenyls on estrogen metabolism and human cytochromes P450 1A1 and 1B1. Biochem Pharmacol 1999, 58:29-38.
35. Perillo B., Sasso A., Abbondanza C., Palumbo G. 17beta-estradiol inhibits apoptosis in MCF-7 cells, inducing bcl-2 expression via two estrogen-responsive elements present in the coding sequence. Mol Cell Biol 2000, 20:2890-2901.
36. Pocar P., Nestler D., Risch M., Fischer B. Apoptosis in bovine cumulus-oocyte complexes after exposure to polychlorinated biphenyl mixtures during in vitro maturation. Reproduction 2005, 130:857-868.
37. Ptak A., Ludewig G., Lehmler H.J., Wojtowicz A.K., Robertson L.W., Gregoraszczuk E.L. Comparison of the actions of 4-chlorobiphenyl and its hydroxylated metabolites on estradiol secretion by ovarian follicles in primary cells in culture. Reprod Toxicol 2005, 20:57-64.
38. Ptak A., Ludewig G., Kapiszewska M., Magnowska Z., Lehmler H.J., Robertson L.W., et al. Induction of cytochromes P450, caspase-3 and DNA damage by PCB3 and its hydroxylated metabolites in porcine ovary. Toxicol Lett 2006, 166:200-211.
39. Russo J., Russo I.H. The role of estrogen in the initiation of breast cancer. J Steroid Biochem Mol Biol 2006, 102:89-96.
40. Safe S. Polychlorinated biphenyls (PCBs): mutagenicity and carcinogenicity. Mutat Res 1989, 220:31-47.
41. Seeger H., Wallwiener D., Kraemer E., Mueck A.O. Comparison of possibile carcinogenic estradiol metabolites: effects on proliferation, apoptosis and metastasis of human breast cancer cells. Maturitas 2006, 54:72-77.
42. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guengerich F.P., et al. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res 1996, 56:2979-2984.
43. Srinivasan A., Lehmler H.J., Robertson L.W., Ludewig G. Production of DNA strand breaks in vitro and reactive oxygen species in vitro and in HL-60 cells by PCB metabolites. Toxicol Sci 2001, 60:92-102.
44. Tharappel J.C., Lee E.Y., Robertson L.W., Spear B.T., Glauert H.P. Regulation of cell proliferation, apoptosis, and transcription factor activities during the promotion of liver carcinogenesis by polychlorinated biphenyls. Toxicol Appl Pharmacol 2002, 179:172-184.
45. Whysner J., Wang C.X. Hepatocellular iron accumulation and increased cell proliferation In polychlorinated biphenyl-exposed Sprague-Dawley rats and the development of hepatocarcinogenesis. Toxicol Sci 2001, 62:36-45.
46. Wolff M.S., Zeleniuch-Jacquotte A., Dubin N., Toniolo P. Risk of breast cancer and organochlorine=exposure. Cancer Epidemiol Biomarkers Prev 2000, 9:271-277.
47. Wu F., Khan S., Wu Q., Barhoumi R., Burghardt R., Safe S. Ligand structure-dependent activation of estrogen receptor alpha/Sp by estrogens and xenoestrogens. J Steroid Biochem Mol Biol. 2008, 110:104-115.
48. Zhang B.F., Peng F.F., Zhang J.Z., Wu D.C. Staurosporine induces apoptosis in NG108-15 cells. Acta Pharmacol Sin 2003, 24:663-669.
49. Zhang Y., Wise J.P., Holford T.R., Xie H., Boyle P., Zahm S.H., et al. Serum polychlorinated biphenyls, cytochrome P-450 1A1 polymorphisms, and risk of breast cancer in Connecticut women. Am J Epidemiol 2004, 160:1177-1183.
50. Zhao S., Narang A., Ding X., Eadon G. Characterization and quantitative analysis of DNA adducts formed from Lower chlorinated PCB-derived quinones. Chem Res Toxicol 2004, 17:502-511.
51. Zheng T., Holford T.R., Tessari J., Mayne S.T., Owens P.H., Ward B., et al. Breast cancer risk associated with congeners of polychlorinated biphenyls. Am J Epidemiol 2000, 152:150-158.