Benzophenone-1 and nonylphenol stimulated MCF-7 breast cancer growth by regulating cell cycle and metastasis-related genes via an estrogen receptor α-Dependent Pathway

Journal of Toxicology and Environmental Health - Part A: Current Issues

Volumn 78, Issue 8, 2015, Pages 492-505

  In, Sol Ji ^a   Kim, Seung Hee ^a   Go, Ryeo Eun ^a   Hwang, Kyung A ^a   Choi, Kyung Chul ^a  

^a Chungbuk National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BENZOPHENONE DERIVATIVE; CATHEPSIN D; CYCLIN D1; DIMETHYL SULFOXIDE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; NONYLPHENOL; PROTEIN P21; 2,4-DIHYDROXYBENZOPHENONE; BIOLOGICAL MARKER; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR ALPHA, HUMAN; ESTROGEN RECEPTOR ANTAGONIST; MESSENGER RNA; PHENOL DERIVATIVE; PHOTOSENSITIZING AGENT; TUMOR PROTEIN;

ARTICLE; CANCER GROWTH; CELL CYCLE REGULATION; CELL MIGRATION; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MCF 7 CELL LINE; METASTASIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; ADENOCARCINOMA; AGONISTS; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL CYCLE; CELL MOTION; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OSMOLARITY;

MAMMALIA;

ADENOCARCINOMA; BENZOPHENONES; BIOLOGICAL MARKERS; BREAST NEOPLASMS; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; ENDOCRINE DISRUPTORS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ANTAGONISTS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; NEOPLASM PROTEINS; OSMOLAR CONCENTRATION; PHENOLS; PHOTOSENSITIZING AGENTS; RNA, MESSENGER;

EID: 84927628612     PISSN: 15287394     EISSN: 10872620     Source Type: Journal    
DOI: 10.1080/15287394.2015.1010464     Document Type: Article

References (55)

1. Aoki, M., Kurasaki, M., Saito, T., Seki, S., Hosokawa, T., Takahashi, Y., Fujita, H., and Iwakuma, T. 2004. Nonylphenol enhances apoptosis induced by serum deprivation in PC12 cells. Life Sci. 74: 2301-2312.
2. Bretschneider, N., Kangaspeska, S., Seifert, M., Reid,G., Gannon, F., and Denger, S. 2008. E2-mediated cathepsin D (CTSD) activation involves looping of distal enhancer elements. Mol. Oncol. 2: 182-190.
3. Cabaravdic, M. 2006. [Xenoestrogen effects of chemical compounds: Influence on the breast cancer]. Med. Arh. 60(suppl. 2): 97-100.
4. Chai, Y., Wu, W., Zhou, C., and Zhou, J. 2012. The potential prognostic value of cathepsin D protein in serous ovarian cancer. Arch. Gynecol. Obstet. 286: 465-471.
5. Choi, K. C., and Jeung, E. B. 2003. The biomarker and endocrine disruptors in mammals. J. Reprod. Dev. 49: 337-345.
6. Choi, S. M., Yoo, S. D., and Lee, B. M. 2004. Toxicological characteristics of endocrine disrupting chemicals: Developmental toxicity, carcinogenicity and mutagenicity. J. Toxicol. Environ. Health B 7: 1-24.
7. Chung, B. Y., Kyung, M., Lim, S. K., Choi, S. M., Lim, D. S., Kwack, S. J., Kim, H. S., and Lee, B. M. 2013. Uterotrophic and Hershberger assays for endocrine disruption properties of plastic food contact materials polypropylene (PP) and polyethylene terephthalate (PET). J. Toxicol. Environ. Health A 76: 624-634.
8. Dai, M., Al-Odaini, A. A., Fils-Aime, N., Villatoro, M. A., Guo, J., Arakelian, A., Rabbani, S. A., Ali, S., and Lebrun, J. 2013. Cyclin D1 cooperates with p21 to regulate TGFbeta-mediated breast cancer cell migration and tumor local invasion. Breast Cancer Res. 15: R49.
9. Gacci, G., Torre, G. C., Pedotti, G., and Gannizzo, G. 1977. [Endocrine therapy of the metastatic breast cancer. I. Ablative hormonal therapy (ovariectomy, adrenalectomy, hypophysectomy)]. Acta Obstet. Ginecol. Hisp. Lusit. 25: 519-528.
10. Garcia, M., Platet, N., Liaudet, E., Laurent, V., Derocq, D., Brouillet, J. P., and Rochefort, H. 1996. Biological and clinical significance of cathepsin D in breast cancer metastasis. Stem Cells 14: 642-650.
11. Hall, J. M., Couse, J. F., and Korach, K. S. 2001. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276: 36869-36872.
12. Han, E. H., Hwang, Y. P., Kim, H. G., Park, J. H., Jeong, T. C., and Jeong, H. G. 2010. Upregulation of cyclooxygenase-2 by 4-nonylphenol is mediated through the cyclic AMP response element activation pathway. J. Toxicol. Environ. Health A 73: 1451-1464.
13. Hayashi, T., Okamoto, Y., Ueda, K., and Kojima, N. 2006. Formation of estrogenic products from benzophenone after exposure to sunlight. Toxicol. Lett. 167: 1-7.
14. Hwang, K. A., Kang, N. H., Yi, B. R., Lee, H. R., Park, M. A., and Choi, K. C. 2013. Genistein, a soy phytoestrogen, prevents the growth of BG-1 ovarian cancer cells induced by 17beta-estradiol or bisphenol A via the inhibition of cell cycle progression. Int. J. Oncol. 42: 733-740.
15. Iwata, M., Eshima, Y., Kagechika, H., and Miyaura, H. 2004. The endocrine disruptors nonylphenol and octylphenol exert direct effects on T cells to suppress Th1 development and enhance Th2 development. Immunol. Lett. 94: 135-139.
16. Jarry, H., Christoffel, J., Rimoldi, G., Koch, L., and Wuttke, W. 2004. Multi-organic endocrine disrupting activity of the UV screen benzophenone 2 (BP2) in ovariectomized adult rats after 5 days treatment. Toxicology 205: 87-93.
17. Johnson, M. D., Torri, J. A., Lippman, M. E., and Dickson, R. B. 1993. The role of cathepsin D in the invasiveness of human breast cancer cells. Cancer Res. 53: 873-877.
18. Jothiramajayam, M., Sinha, S., Ghosh, M., Nag, A., Jana, A., and Mukherjee, A. 2014. Sodium fluoride promotes apoptosis by generation of reactive oxygen species in human lymphocytes. J. Toxicol. Environ. Health A 77: 1269-1280.
19. Kang, N. H., Hwang, K. A., Kim, T. H., Hyun, S. H., Jeung, E. B., and Choi, K. C. 2012. Induced growth of BG-1 ovarian cancer cells by 17beta-estradiol or various endocrine disrupting chemicals was reversed by resveratrol via downregulation of cell cycle progression. Mol. Med. Rep. 6: 151-156.
20. Kerdivel, G., Le Guevel, R., Habauzit, D., Brion, F., Ait-Aissa, S., and Pakdel, F. 2013. Estrogenic potency of benzophenone UV filters in breast cancer cells: Proliferative and transcriptional activity substantiated by docking analysis. PLoS ONE 8: e60567.
21. Kim, Y. S., Katase, T., Sekine, S., Inoue, T., Makino, M., Uchiyama, T., Fujimoto, Y., and Yamashita, N. 2004. Variation in estrogenic activity among fractions of a commercial nonylphenol by high performance liquid chromatography. Chemosphere 54: 1127-1134.
22. Kunisue, T., Chen, X., Buck Louis, G. M., Sundaram, R., Hediger, M. L., Sun, L., and Kannan, K. 2012. Urinary concentrations of benzophenone-type UV filters in U.S. women and their association with endometriosis. Environ. Sci. Technol. 46: 4624-4632.
23. Lee, H. R., and Choi, K. C. 2013. 4-tert-Octylphenol stimulates the expression of cathepsins in human breast cancer cells and xenografted breast tumors of a mouse model via an estrogen receptor-mediated signaling pathway. Toxicology 304: 13-20.
24. Lee, H. R., Hwang, K. A., Park, M. A., Yi, B. R., Jeung, E. B., and Choi, K. C. 2012a. Treatment with bisphenol A and methoxychlor results in the growth of human breast cancer cells and alteration of the expression of cell cycle-related genes, cyclin D1 and p21, via an estrogen receptor-dependent signaling pathway. Int. J. Mol. Med. 29: 883-890.
25. Lee, H. R., EJeung, E. B., Cho, M. H., Kim, T. H., Leung, P. C., and Choi, K. C. 2013. Molecular mechanism(s) of endocrinedisrupting chemicals and their potent oestrogenicity in diverse cells and tissues that express oestrogen receptors. J. Cell. Mol. Med. 17: 1-11.
26. Lee, H. R., Kim, T. H., and Choi, K. C. 2012b. Functions and physiological roles of two types of estrogen receptors, ER alpha and ER beta, identified by estrogen receptor knockout mouse. Lab Anim. Res. 28: 71-76.
27. Lee, P. C., and Lee, W. 1996. In vivo estrogenic action of nonylphenol in immature female rats. Bull. Environ. Contam. Toxicol. 57: 341-348.
28. Liaudet-Coopman, E., Beaujouin, M., Derocq, D., Garcia, M., Glondu-Lassis, M., Laurent-Matha, V., Prebois, C., Rochefort, H., and Vignon, F. 2006. Cathepsin D: Newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Lett. 237: 167-179.
29. Masuo, Y., and Ishido, M. 2011. Neurotoxicity of endocrine disruptors: Possible involvement in brain development and neurodegeneration. J. Toxicol. Environ. Health B 14: 346-369.
30. Meier, S., Andersen, T. E., Norberg, B., Thorsen, A., Taranger, G. L., Kjesbu, O. S., Dale, R., Morton, H. C., Klungsoyr, J., and Svardal, A. 2007. Effects of alkylphenols on the reproductive system of Atlantic cod (Gadus morhua). Aquat. Toxicol. 81: 207-218.
31. Montcourrier, P., Mangeat, P. H., Salazar, G., Morisset, M., Sahuquet, A., and Rochefort, H. 1990. Cathepsin D in breast cancer cells can digest extracellular matrix in large acidic vesicles. Cancer Res. 50: 6045-6054.
32. Montcourrier, P., Silver, I., Farnoud, R., Bird, I., and Rochefort, H. 1997. Breast cancer cells have a high capacity to acidify extracellular milieu by a dual mechanism. Clin. Exp. Metastasis 15:382-392.
33. Moody, R. P., Yip, A., and Chu, I. 2009. Effect of cold storage on in vitro human skin absorption of six 14C-radiolabeled environmental contaminants: Benzo[a]pyrene, ethylene glycol, methyl parathion, naphthalene, nonyl phenol, and toluene. J. Toxicol. Environ. Health A 72: 505-517.
34. Mundy, G. R. 2002. Metastasis to bone: Causes, consequences and therapeutic opportunities. Nat. Rev. Cancer 2: 584-593.
35. Nakagawa, Y., and Suzuki, T. 2002. Metabolism of 2-hydroxy-4-methoxybenzophenone in isolated rat hepatocytes and xenoestrogenic effects of its metabolites on MCF-7 human breast cancer cells. Chem. Biol. Interact. 139: 115-128.
36. Nakagawa, Y., and Tayama, K. 2002. Benzophenone-induced estrogenic potency in ovariectomized rats. Arch. Toxicol. 76: 727-731.
37. Nimrod, A. C., and Benson, W. H. 1996. Environmental estrogenic effects of alkylphenol ethoxylates. Crit. Rev. Toxicol. 26:335-364.
38. Nohynek, G. J., and Schaefer, H. 2001. Benefit and risk of organic ultraviolet filters. Regul. Toxicol. Pharmacol. 33: 285-299.
39. Oros, D. R., Jarman,W. M., Lowe, T., David, N., Lowe, S., and Davis, J. A. 2003. Surveillance for previously unmonitored organic contaminants in the San Francisco Estuary. Mar. Pollut. Bull. 46: 1102-1110.
40. Park, M. A., Hwang, K. A., Lee, H. R., Yi, B. R., and Choi, K. C. 2011. Cell growth of BG-1 ovarian cancer cells was promoted by 4-tert-octylphenol and 4-nonylphenol via downregulation of TGF-beta receptor 2 and upregulation of c-myc. Toxicol. Res. 27: 253-259.
41. Park, M. A., Hwang, K. A., Lee, H. R., Yi, B. R., Jeung, E. B., and Choi, K. C. 2013. Benzophenone-1 stimulated the growth of BG-1 ovarian cancer cells by cell cycle regulation via an estrogen receptor alphamediated signaling pathway in cellular and xenograft mouse models. Toxicology 305: 41-48.
42. Phillips, K. P., and Tanphaichitr, N. 2008. Human exposure to endocrine disrupters and semen quality. J. Toxicol. Environ. Health B 11: 188-220.
43. Pojana, G., Bonfa, A., Busetti, F., Collarin, A., and Marcomini, A. 2004. Estrogenic potential of the Venice, Italy, lagoon waters. Environ. Toxicol. Chem. 23: 1874-1880.
44. Schlumpf, M., Cotton, B., Conscience, M., Haller, V., Steinmann, B., and Lichtensteiger, W 2001. In vitro and in vivo estrogenicity of UV screens. Environ. Health Perspect. 109: 239-244.
45. Schlumpf, M., Durrer, S., Faass, O., Ehnes, C., Fuetsch, M., Gaille, C., Henseler, M., Hofkamp, L., Maerkel, K., Reolon, S., Timms, B., Tresguerres, J. A., and Lichtensteiger, W. 2008. Developmental toxicity of UV filters and environmental exposure: A review. Int. J. Androl. 31: 144-151.
46. Soares, A., Guieysse, B., Jefferson, B., Cartmell, E., and Lester, J. N. 2008. Nonylphenol in the environment: A critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ. Int. 34: 1033-1049.
47. Suzuki, T., Kitamura, S., Khota, R., Sugihara, K., Fujimoto, N., and Ohta, S. 2005. Estrogenic and antiandrogenic activities of 17 benzophenone derivatives used as UV stabilizers and sunscreens. Toxicol. Appl. Pharmacol. 203: 9-17.
48. Terasaka, S., Inoue, A., Tanji, M., and Kiyama, R. 2006. Expression profiling of estrogenresponsive genes in breast cancer cells treated with alkylphenols, chlorinated phenols, parabens, or bis-And benzoylphenols for evaluation of estrogenic activity. Toxicol. Lett. 163: 130-141.
49. Tollefsen, K. E., Sundt, R. C., Beyer, J., Meier, S., and Hylland, K. 2011. Endocrine modulation in Atlantic cod (Gadus morhua L.) exposed to alkylphenols, polyaromatic hydrocarbons, produced water and dispersed oil. J. Toxicol. Environ. Health A 74: 5289-542.
50. Tremoen, N. H., Fowler, P. A., Ropstad, E., Verhaegen, S., and Krogenaes, A. 2014. Exposure to the three structurally different PCB congeners (PCB 118, 153, and 126) results in decreased protein expression and altered steroidogenesis in the human adrenocortical carcinoma cell line H295R. J. Toxicol. Environ. Health A 77: 516-534.
51. Wang, J. L., Liu, C. S., Lin, K. L., Chou, C. T., Hsieh, C. H., Chang, C. H., Chen,W. C., Liu, S. I., Hsu, S. S., Chang, H. T., and Jan, C. R. 2005a. Nonylphenol-induced Ca2+ elevation and Ca2+-independent cell death in human osteosarcoma cells. Toxicol. Lett. 160: 76-83.
52. Wang, W., Goswami, S., Sahai, E., Wyckoff, J. B., Segall, J. E., and Condeelis, J. S. 2005b. Tumor cells caught in the act of invading: their strategy for enhanced cell motility. Trends Cell Biol. 15: 138-145.
53. Watanabe, J., Kamata, Y., Seo, N., Okayasu, I., and Kuramoto, H. 2007. Stimulatory effect of estrogen on the growth of endometrial cancer cells is regulated by cell-cycle regulators. J. Steroid Biochem. Mol. Biol. 107: 163-171.
54. Waye, A., and Trudeau, V. L. 2011. Neuroendocrine disruption: More than hormones are upset. J. Toxicol. Environ. Health B 14: 270-291.
55. Welboren, W. J., Sweep, F. C., Span, P. N., and Stunnenberg, H. G. 2009. Genomic actions of estrogen receptor alpha: What are the targets and how are they regulated? Endocr. Relat. Cancer 16: 1073-1089.