Differential effects of a complex organochlorine mixture on the proliferation of breast cancer cell lines

Environmental Research

Volumn 111, Issue 3, 2011, Pages 337-347

  Aubé, Michel ^a   Larochelle, Christian ^a   Ayotte, Pierre ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b INSTITUT NATIONAL DE SANTÉ PUBLIQUE DU QUÉBEC   (Canada)

Author keywords

Antiandrogens; Breast cancer; Cell proliferation; Chlorinated pesticides; Polychlorinated biphenyls; Sex steroids; Xenoestrogens

Indexed keywords

ALDRIN; ANDROSTANOLONE; BETA HEXACHLOROCYCLOHEXANE; CAMPHECLOR; CHLORPHENOTANE; DIELDRIN; ESTRADIOL; FLAME RETARDANT; ORGANOCHLORINE DERIVATIVE; POLYCHLORINATED BIPHENYL DERIVATIVE;

BIOASSAY; CANCER; CYTOLOGY; DOSE-RESPONSE RELATIONSHIP; FATTY ACID; PCB; PESTICIDE RESIDUE; STEROID;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL CYCLE PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; ENDOCRINE FUNCTION; ESTROGEN ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SIMULATION;

BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DIHYDROTESTOSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; HUMANS; HYDROCARBONS, CHLORINATED; NEOPLASMS, HORMONE-DEPENDENT; RECEPTORS, ANDROGEN; REGRESSION ANALYSIS;

EID: 79952901094     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2011.01.010     Document Type: Article

References (64)

1. Andersen H.R., Andersson A.M., Arnold S.F., Autrup H., Barfoed M., Beresford N.A., et al. Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals. Environ. Health Perspect. 1999, 107(Suppl 1):89-108.
2. Ando S., De Amicis F., Rago V., Carpino A., Maggiolini M., Panno M.L., et al. Breast cancer: from estrogen to androgen receptor. Mol. Cell Endocrinol. 2002, 193:121-128.
3. Arcaro K.F., Vakharia D.D., Yang Y., Gierthy J.F. Lack of synergy by mixtures of weakly estrogenic hydroxylated polychlorinated biphenyls and pesticides. Environ. Health Perspect. 1998, 106(Suppl 4):1041-1046.
4. Aubé M., Larochelle C., Ayotte P. 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene (p,p'-DDE) disrupts the estrogen-androgen balance regulating the growth of hormone-dependent breast cancer cells. Breast Cancer Res. 2008, 10:R16.
5. Bigsby R.M., Caperell-Grant A., Madhukar B.V. Xenobiotics released from fat during fasting produce estrogenic effects in ovariectomized mice. Cancer Res. 1997, 57:865-869.
6. Birkhoj M., Nellemann C., Jarfelt K., Jacobsen H., Andersen H.R., Dalgaard M., et al. The combined antiandrogenic effects of five commonly used pesticides. Toxicol. Appl. Pharmacol. 2004, 201:10-20.
7. Birrell S.N., Bentel J.M., Hickey T.E., Ricciardelli C., Weger M.A., Horsfall D.J., et al. Androgens induce divergent proliferative responses in human breast cancer cell lines. J. Steroid Biochem. Mol. Biol. 1995, 52:459-467.
8. Buteau-Lozano H., Velasco G., Cristofari M., Balaguer P., Perrot-Applanat M. Xenoestrogens modulate vascular endothelial growth factor secretion in breast cancer cells through an estrogen receptor-dependent mechanism. J. Endocrinol. 2008, 196:399-412.
9. Cappelletti V., Saturno G., Miodini P., Korner W., Daidone M.G. Selective modulation of ER-beta by estradiol and xenoestrogens in human breast cancer cell lines. Cell Mol. Life Sci. 2003, 60:567-576.
10. Charles G.D., Gennings C., Zacharewski T.R., Gollapudi B.B., Carney E.W. Assessment of interactions of diverse ternary mixtures in an estrogen receptor-alpha reporter assay. Toxicol. Appl. Pharmacol. 2002, 180:11-21.
11. Connor K., Ramamoorthy K., Moore M., Mustain M., Chen I., Safe S., et al. Hydroxylated polychlorinated biphenyls (PCBs) as estrogens and antiestrogens: structure-activity relationships. Toxicol. Appl. Pharmacol. 1997, 145:111-123.
12. Coumoul X., Diry M., Robillot C., Barouki R. 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. 2001, 61:3942-3948.
13. Cruz S., Lino C., Silveira M.I. Evaluation of organochlorine pesticide residues in human serum from an urban and two rural populations in Portugal. Sci. Total Environ 2003, 317:23-35.
14. Davis C., Bhana S., Shorrocks A.J., Martin F.L. Oestrogens induce G(1) arrest in benzo[a]pyrene-treated MCF-7 breast cells whilst enhancing genotoxicity and clonogenic survival. Mutagenesis 2002, 17:431-438.
15. Demers A., Ayotte P., Brisson J., Dodin S., Robert J., Dewailly E. Risk and aggressiveness of breast cancer in relation to plasma organochlorine concentrations. Cancer Epidemiol. Biomarkers Prev. 2000, 9:161-166.
16. Desaulniers D., Leingartner K., Russo J., Perkins G., Chittim B.G., Archer M.C., et al. Modulatory effects of neonatal exposure to TCDD, or a mixture of PCBs, p,p'-DDT, and p-p'-DDE, on methylnitrosourea-induced mammary tumor development in the rat. Environ. Health Perspect. 2001, 109:739-747.
17. Dunning A.M., Healey C.S., Pharoah P.D., Teare M.D., Ponder B.A., Easton D.F. A systematic review of genetic polymorphisms and breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 1999, 8:843-854.
18. Enmark E., Pelto-Huikko M., Grandien K., Lagercrantz S., Lagercrantz J., Fried G., et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J. Clin. Endocrinol. Metab. 1997, 82:4258-4265.
19. Fang H., Tong W., Perkins R., Soto A.M., Prechtl N.V., Sheehan D.M. Quantitative comparisons of in vitro assays for estrogenic activities. Environ. Health Perspect. 2000, 108:723-729.
20. Garcia A.M. Pesticide exposure and women's health. Am. J. Ind Med. 2003, 44:584-594.
21. Gelbke H.P., Kayser M., Poole A. OECD test strategies and methods for endocrine disruptors. Toxicology 2004, 205:17-25.
22. Gray L.E., Ostby J., Furr J., Wolf C.J., Lambright C., Parks L., et al. Effects of environmental antiandrogens on reproductive development in experimental animals. Hum. Reprod. Update 2001, 7:248-264.
23. Hall J.M., McDonnell D.P. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 1999, 140:5566-5578.
24. Hewitt R., Forero A., Luncsford P.J., Martin F.L. Enhanced micronucleus formation and modulation of BCL-2:BAX in MCF-7 cells after exposure to binary mixtures. Environ. Health Perspect. 2007, 115(Suppl 1):129-136.
25. Ito K., Suzuki T., Akahira J., Moriya T., Kaneko C., Utsunomiya H., et al. Expression of androgen receptor and 5alpha-reductases in the human normal endometrium and its disorders. Int. J. Cancer 2002, 99:652-657.
26. Kamarudin R., Shah S.A., Hidayah N. Lifestyle factors and breast cancer: a case-control study in Kuala Lumpur, Malaysia. Asian Pac. J. Cancer Prev. 2006, 7:51-54.
27. Kelce W.R., Stone C.R., Laws S.C., Gray L.E., Kemppainen J.A., Wilson E.M. Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist. Nature 1995, 375:581-585.
28. Kramer V.J., Helferich W.G., Bergman A., Klasson-Wehler E., Giesy J.P. Hydroxylated polychlorinated biphenyl metabolites are anti-estrogenic in a stably transfected human breast adenocarcinoma (MCF7) cell line. Toxicol. Appl. Pharmacol. 1997, 144:363-376.
29. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
30. Kutz F.W., Wood P.H., Bottimore D.P. Organochlorine pesticides and polychlorinated biphenyls in human adipose tissue. Rev. Environ. Contam. Toxicol. 1991, 120:1-82.
31. Lapointe J., Labrie C. Role of the cyclin-dependent kinase inhibitor p27(Kip1) in androgen-induced inhibition of CAMA-1 breast cancer cell proliferation. Endocrinology 2001, 142:4331-4338.
32. Lazennec G., Bresson D., Lucas A., Chauveau C., Vignon F. ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology 2001, 142:4120-4130.
33. Lemaire G., Mnif W., Mauvais P., Balaguer P., Rahmani R. Activation of alpha- and beta-estrogen receptors by persistent pesticides in reporter cell lines. Life Sci. 2006, 79:1160-1169.
34. Lin C.H., Lin P.H. 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. 2006, 162:181-194.
35. Lipman M.L., Stevens A.C., Bleackley R.C., Helderman J.H., McCune T.R., Harmon W.E., et al. The strong correlation of cytotoxic T lymphocyte-specific serine protease gene transcripts with renal allograft rejection. Transplantation 1992, 53:73-79.
36. Llabjani V., Trevisan J., Jones K.C., Shore R.F., Martin F.L. Binary mixture effects by PBDE congeners (47, 153, 183, or 209) and PCB congeners (126 or 153) in MCF-7 cells: biochemical alterations assessed by IR spectroscopy and multivariate analysis. Environ. Sci. Technol. 2010, 44:3992-3998.
37. MacIndoe J.H., Etre L.A. An antiestrogenic action of androgens in human breast cancer cells. J. Clin. Endocrinol. Metab. 1981, 53:836-842.
38. Magklara A., Brown T.J., Diamandis E.P. Characterization of androgen receptor and nuclear receptor co-regulator expression in human breast cancer cell lines exhibiting differential regulation of kallikreins 2 and 3. Int. J. Cancer 2002, 100:507-514.
39. Margolin S., Lindblom A. Familial breast cancer, underlying genes, and clinical implications: a review. Crit. Rev. Oncog. 2006, 12:75-113.
40. Matthews J., Celius T., Halgren R., Zacharewski T. Differential estrogen receptor binding of estrogenic substances: a species comparison. J. Steroid. Biochem. Mol. Biol. 2000, 74:223-234.
41. McFadyen M.C., Breeman S., Payne S., Stirk C., Miller I.D., Melvin W.T., et al. Immunohistochemical localization of cytochrome P450 CYP1B1 in breast cancer with monoclonal antibodies specific for CYP1B1. J. Histochem. Cytochem. 1999, 47:1457-1464.
42. Muckle G., Ayotte P., Dewailly E., Jacobson S.W., Jacobson J.L. Prenatal exposure of the northern Québec Inuit infants to environmental contaminants. Environ. Health Perspect. 2001, 109:1291-1299.
43. Mumtaz M.M., Tully D.B., El Masri H.A., De Rosa C.T. Gene induction studies and toxicity of chemical mixtures. Environ. Health Perspect. 2002, 110(Suppl 6):947-956.
44. Mundy W.R., Freudenrich T.M., Crofton K.M., DeVito M.J. Accumulation of PBDE-47 in primary cultures of rat neocortical cells. Toxicol. Sci. 2003, 82:164-169.
45. Paruthiyil S., Parmar H., Kerekatte V., Cunha G.R., Firestone G.L., Leitman D.C. Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res. 2004, 64:423-428.
46. Payne J., Jones C., Lakhani S., Kortenkamp A. Improving the reproducibility of the MCF-7 cell proliferation assay for the detection of xenoestrogens. Sci. Total Environ. 2000, 248:51-62.
47. Rajapakse N., Silva E., Kortenkamp A. Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environ. Health Perspect. 2002, 110:917-921.
48. Rasmussen T.H., Nielsen F., Andersen H.R., Nielsen J.B., Weihe P., Grandjean P. Assessment of xenoestrogenic exposure by a biomarker approach: application of the E-Screen bioassay to determine estrogenic response of serum extracts. Environ. Health 2003, 2:12.
49. 2-induced expression of BRCA1 by persistent organochlorines. Breast Cancer Res. 2002, 4:R12.
50. Rudel R.A., Attfield K.R., Schifano J.N., Brody J.G. Chemicals causing mammary gland tumors in animals signal new directions for epidemiology, chemicals testing, and risk assessment for breast cancer prevention. Cancer 2007, 109:2635-2666.
51. Sandanger T.M., Sinotte M., Dumas P., Marchand M., Sandau D., Pereg D., et al. Plasma concentrations of selected organobromine compounds and polychlorinated biphenyls in postmenopausal women of Quebec, Canada. Environ. Health Perspect. 2007, 115:1429-1434.
52. Schrader T.J., Cooke G.M. Effects of Aroclors and individual PCB congeners on activation of the human androgen receptor in vitro. Reprod. Toxicol. 2003, 17:15-23.
53. Shantakumar S., Terry M.B., Teitelbaum S.L., Britton J.A., Millikan R.C., Moorman P.G., et al. Reproductive factors and breast cancer risk among older women. Breast Cancer Res. Treat. 2006, 102:365-374.
54. Shiraishi F., Okumura T., Nomachi M., Serizawa S., Nishikawa J., Edmonds J.S., et al. Estrogenic and thyroid hormone activity of a series of hydroxy-polychlorinated biphenyls. Chemosphere 2003, 52:33-42.
55. Silva E., Rajapakse N., Kortenkamp A. Something from "nothing"-eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environ. Sci. Technol. 2002, 36:1751-1756.
56. Sohoni P., Sumpter J.P. Several environmental oestrogens are also anti-androgens. J. Endocrinol. 1998, 158:327-339.
57. Spink D.C., Spink B.C., Cao J.Q., DePasquale J.A., Pentecost B.T., Fasco M.J., et al. Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 1998, 19:291-298.
58. Stelzer A., Chan H.M. The relative estrogenic activity of technical toxaphene mixture and two individual congeners. Toxicology 1999, 138:69-80.
59. Valerón P.F., Pestano J.J., Luzardo O.P., Zumbado M.L., Almeida M., Boada L.D. Differential effects exerted on human mammary epithelial cells by environmentally relevant organochlorine pesticides either individually or in combination. Chem. Biol. Interact. 2009, 180:485-491.
60. Van Duursen M.B., Sanderson J.T., van der Bruggen M., van der Linden J., van den Berg M. 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. 2003, 190:241-250.
61. Willingham E. Endocrine-disrupting compounds and mixtures: unexpected dose-response. Arch. Environ. Contam. Toxicol 2004, 46:265-269.
62. Yared E., McMillan T.J., Martin F.L. Genotoxic effects of oestrogens in breast cells detected by the micronucleus assay and the Comet assay. Mutagenesis 2002, 17:345-352.
63. Zava D.T., Blen M., Duwe G. Estrogenic activity of natural and synthetic estrogens in human breast cancer cells in culture. Environ. Health Perspect. 1997, 105(Suppl 3):637-645.
64. Zumbado M., Goethals M., Alvarez-Leon E.E., Luzardo O.P., Cabrera F., Serra-Majem L., et al. Inadvertent exposure to organochlorine pesticides DDT and derivatives in people from the Canary Islands (Spain). Sci. Total Environ. 2005, 339:49-62.