Benzophenone-1 stimulated the growth of BG-1 ovarian cancer cells by cell cycle regulation via an estrogen receptor alpha-mediated signaling pathway in cellular and xenograft mouse models

Toxicology

Volumn 305, Issue , 2013, Pages 41-48

  Park, Min Ah ^a   Hwang, Kyung A ^a   Lee, Hye Rim ^a   Yi, Bo Rim ^a   Jeung, Eui Bae ^a   Choi, Kyung Chul ^a  

^a Chungbuk National University   (South Korea)

Author keywords

Benzophenone; BP 1; Cell cycle; Endocrine disrupting chemicals; Estrogen

Indexed keywords

BENZOPHENONE DERIVATIVE; BENZORESORCINOL; CYCLIN D1; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; PROTEIN P21; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE REGULATION; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIMETABOLITES; BENZOPHENONES; BLOTTING, WESTERN; BROMODEOXYURIDINE; CELL CYCLE; CELL PROLIFERATION; COLORING AGENTS; CYCLIN D1; ESTROGEN RECEPTOR ALPHA; FEMALE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED BALB C; OVARIAN NEOPLASMS; P21-ACTIVATED KINASES; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, NEOPLASM; SIGNAL TRANSDUCTION; STIMULATION, CHEMICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84873430440     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.12.021     Document Type: Article

References (45)

1. Choi S.M., Yoo S.D., Lee B.M. Toxicological characteristics of endocrine-disrupting chemicals: developmental toxicity, carcinogenicity, and mutagenicity. J. Toxicol. Environ. Health B: Crit. Rev. 2004, 7:1-24.
2. Diamanti-Kandarakis E., Palioura E., Kandarakis S.A., Koutsilieris M. The impact of endocrine disruptors on endocrine targets. Horm. Metab. Res. 2010, 42:543-552.
3. Fernandez S.V., Russo J. Estrogen and xenoestrogens in breast cancer. Toxicol. Pathol. 2010, 38:110-122.
4. Gonzalez H., Farbrot A., Larko O., Wennberg A.M. Percutaneous absorption of the sunscreen benzophenone-3 after repeated whole-body applications, with and without ultraviolet irradiation. Br. J. Dermatol. 2006, 154:337-340.
5. Harris H.A., Bapat A.R., Gonder D.S., Frail D.E. The ligand binding profiles of estrogen receptors alpha and beta are species dependent. Steroids 2002, 67:379-384.
6. Hayashi T., Okamoto Y., Ueda K., Kojima N. Formation of estrogenic products from benzophenone after exposure to sunlight. Toxicol. Lett. 2006, 167:1-7.
7. Heneweer M., Muusse M., Van Den Berg M., Sanderson J.T. Additive estrogenic effects of mixtures of frequently used UV filters on pS2-gene transcription in MCF-7 cells. Toxicol. Appl. Pharmacol. 2005, 208:170-177.
8. Hofmann P.J., Schomburg L., Kohrle J. Interference of endocrine disrupters with thyroid hormone receptor-dependent transactivation. Toxicol. Sci. 2009, 110:125-137.
9. Hwang K.A., Park S.H., Yi B.R., Choi K.C. Gene alterations of ovarian cancer cells expressing estrogen receptors by estrogen and bisphenol A using microarray analysis. Lab. Anim. Res. 2011, 27:99-107.
10. Janjua N.R., Mogensen B., Andersson A.M., Petersen J.H., Henriksen M., Skakkebaek N.E., Wulf H.C. Systemic absorption of the sunscreens benzophenone-3, octyl-methoxycinnamate, and 3-(4-methyl-benzylidene) camphor after whole-body topical application and reproductive hormone levels in humans. J. Invest. Dermatol. 2004, 123:57-61.
11. Jarry H., Christoffel J., Rimoldi G., Koch L., Wuttke W. Multi-organic endocrine disrupting activity of the UV screen benzophenone 2 (BP2) in ovariectomized adult rats after 5 days treatment. Toxicology 2004, 205:87-93.
12. Kang N.H., Hwang K.A., Kim T.H., Hyun S.H., Jeung E.B., Choi K.C. 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. 2012, 6:151-156.
13. Kang N.H., Hwang K.A., Yi B.R., Lee H.J., Jeung E.B., Kim S.U., Choi K.C. Human amniotic fluid-derived stem cells expressing cytosine deaminase and thymidine kinase inhibits the growth of breast cancer cells in cellular and xenograft mouse models. Cancer Gene Ther. 2012, 19:412-419.
14. Kang N.H., Yi B.R., Lim S.Y., Hwang K.A., Baek Y.S., Kang K.S., Choi K.C. Human amniotic membrane-derived epithelial stem cells display anticancer activity in BALB/c female nude mice bearing disseminated breast cancer xenografts. Int. J. Oncol. 2012, 40:2022-2028.
15. Kashima H., Shiozawa T., Miyamoto T., Suzuki A., Uchikawa J., Kurai M., Konishi I. Autocrine stimulation of IGF1 in estrogen-induced growth of endometrial carcinoma cells: involvement of the mitogen-activated protein kinase pathway followed by up-regulation of cyclin D1 and cyclin E. Endocr. Relat. Cancer 2009, 16:113-122.
16. Kawamura Y., Mutsuga M., Kato T., Lida M., Tanamoto K. Estrogenic and antiandrogenic activities of benzophenones in human estrogen and androgen receptor mediated mammalian reporter gene assays. J. Health Sci. 2005, 51:48-54.
17. Kawamura Y., Ogawa Y., Nishimura T., Kikuchi Y., Nishikawa J., Nishihara T. Estrogenic activities of UV stabilizers used in food contact plastics and benzophenone derivatives tested by the yeast two-hybrid assay. J. Health Sci. 2003, 49:205-212.
18. Kim K.Y., Yi B.R., Lee H.R., Kang N.H., Jeung E.B., Kim S.U., Choi K.C. Stem cells with fused gene expression of cytosine deaminase and interferon-beta migrate to human gastric cancer cells and result in synergistic growth inhibition for potential therapeutic use. Int. J. Oncol. 2012, 40:1097-1104.
19. Kunz P.Y., Fent K. Estrogenic activity of UV filter mixtures. Toxicol. Appl. Pharmacol. 2006, 217:86-99.
20. Kunz P.Y., Galicia H.F., Fent K. Comparison of in vitro and in vivo estrogenic activity of UV filters in fish. Toxicol. Sci. 2006, 90:349-361.
21. Lee H.R., Hwang K.A., Park M.A., Yi B.R., Jeung E.B., Choi K.C. 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. 2012, 29:883-890.
22. Lee H.R., Kim T.H., Choi K.C. Treatment with bisphenol A leads to the promotion of human breast cancer cells and alteration of cell cycle-related gene expression, cyclin E and p27. J. Biomed. Res. 2011, 12:215-233.
23. Liehr J.G. Is estradiol a genotoxic mutagenic carcinogen?. Endocr. Rev. 2000, 21:40-54.
24. Liu Y.S., Ying G.G., Shareef A., Kookana R.S. Biodegradation of the ultraviolet filter benzophenone-3 under different redox conditions. Environ. Toxicol. Chem. 2012, 31:289-295.
25. Matsumoto H., Adachi S., Suzuki Y. Estrogenic activity of ultraviolet absorbers and the related compounds. Yakugaku Zasshi 2005, 125:643-652.
26. Miller D., Wheals B.B., Beresford N., Sumpter J.P. Estrogenic activity of phenolic additives determined by an in vitro yeast bioassay. Environ. Health Perspect. 2001, 109:133-138.
27. Molina-Molina J.M., Escande A., Pillon A., Gomez E., Pakdel F., Cavailles V., Olea N., Ait-Aissa S., Balaguer P. Profiling of benzophenone derivatives using fish and human estrogen receptor-specific in vitro bioassays. Toxicol. Appl. Pharmacol. 2008, 232:384-395.
28. Olsen C.M., Meussen-Elholm E.T., Samuelsen M., Holme J.A., Hongslo J.K. Effects of the environmental oestrogens bisphenol A, tetrachlorobisphenol A, tetrabromobisphenol A, 4-hydroxybiphenyl and 4,4'-dihydroxybiphenyl on oestrogen receptor binding, cell proliferation and regulation of oestrogen sensitive proteins in the human breast cancer cell line MCF-7. Pharmacol. Toxicol. 2003, 92:180-188.
29. Park M.A., Hwang K.A., Lee H.R., Yi B.R., Jeung E.B., Choi K.C. Cell growth of BG-1 ovarian cancer cells is promoted by di-n-butyl phthalate and hexabromocyclododecane via upregulation of the cyclin D and cyclin-dependent kinase-4 genes. Mol. Med. Rep. 2012, 5:761-766.
30. Poiger T., Buser H.R., Balmer M.E., Bergqvist P.A., Muller M.D. Occurrence of UV filter compounds from sunscreens in surface waters: regional mass balance in two Swiss lakes. Chemosphere 2004, 55:951-963.
31. Schlecht C., Klammer H., Frauendorf H., Wuttke W., Jarry H. Pharmacokinetics and metabolism of benzophenone 2 in the rat. Toxicology 2008, 245:11-17.
32. Shanle E.K., Xu W. Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action. Chem. Res. Toxicol. 2011, 24:6-19.
33. Shim E.Y., Walker A.K., Shi Y., Blackwell T.K. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev 2002, 16:2135-2146.
34. Sommer S., Fuqua S.A. Estrogen receptor and breast cancer. Semin. Cancer Biol. 2001, 11:339-352.
35. Spillman M.A., Manning N.G., Dye W.W., Sartorius C.A., Post M.D., Harrell J.C., Jacobsen B.M., Horwitz K.B. Tissue-specific pathways for estrogen regulation of ovarian cancer growth and metastasis. Cancer Res. 2010, 70:8927-8936.
36. Sumpter J.P., Johnson A.C. Lessons from endocrine disruption and their application to other issues concerning trace organics in the aquatic environment. Environ. Sci. Technol. 2005, 39:4321-4332.
37. Suzuki T., Kitamura S., Khota R., Sugihara K., Fujimoto N., Ohta S. Estrogenic and antiandrogenic activities of 17 benzophenone derivatives used as UV stabilizers and sunscreens. Toxicol. Appl. Pharmacol. 2005, 203:9-17.
38. Takamiya M., Lambard S., Huhtaniemi I.T. Effect of bisphenol A on human chorionic gonadotrophin-stimulated gene expression of cultured mouse Leydig tumour cells. Reprod. Toxicol. 2007, 24:265-275.
39. Watanabe J., Kamata Y., Seo N., Okayasu I., Kuramoto H. Stimulatory effect of estrogen on the growth of endometrial cancer cells is regulated by cell-cycle regulators. J. Steroid Biochem. Mol. Biol. 2007, 107:163-171.
40. Weisbrod C.J., Kunz P.Y., Zenker A.K., Fent K. Effects of the UV filter benzophenone-2 on reproduction in fish. Toxicol. Appl. Pharmacol. 2007, 225:255-266.
41. Wetherill Y.B., Hess-Wilson J.K., Comstock C.E., Shah S.A., Buncher C.R., Sallans L., Limbach P.A., Schwemberger S., Babcock G.F., Knudsen K.E. Bisphenol A facilitates bypass of androgen ablation therapy in prostate cancer. Mol. Cancer Ther. 2006, 5:3181-3190.
42. Yamasaki K., Takeyoshi M., Sawaki M., Imatanaka N., Shinoda K., Takatsuki M. Immature rat uterotrophic assay of 18 chemicals and Hershberger assay of 30 chemicals. Toxicology 2003, 183:93-115.
43. Yanowitz J., Fire A. Cyclin D involvement demarcates a late transition in C. elegans embryogenesis. Dev. Biol. 2005, 279:244-251.
44. Yi B.R., Kang N.H., Hwang K.A., Kim S.U., Jeung E.B., Choi K.C. Antitumor therapeutic effects of cytosine deaminase and interferon-beta against endometrial cancer cells using genetically engineered stem cells in vitro. Anticancer Res. 2011, 31:2853-2861.
45. Yi B.R., O S.N., Kang N.H., Hwang K.A., Kim S.U., Jeung E.B., Kim Y.B., Heo G.J., Choi K.C. Genetically engineered stem cells expressing cytosine deaminase and interferon-beta migrate to human lung cancer cells and have potentially therapeutic anti-tumor effects. Int. J. Oncol. 2011, 39:833-839.