Oral exposure to bisphenol a increases dimethylbenzanthracene-induced mammary cancer in rats

Environmental Health Perspectives

Volumn 119, Issue 2, 2011, Pages 910-915

  Jenkins, Sarah ^a   Raghuraman, Nandini ^a   Eltoum, Isam ^b,c   Carpenter, Mark ^d   Russo, Jose ^e   Lamartiniere, Coral A ^a,b  

^a Department of Pharmacology and Toxicology ^*  (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

^d AUBURN UNIVERSITY   (United States)

^e FOX CHASE CANCER CENTER   (United States)

Author keywords

Apoptosis; Bisphenol a; Mammary cancer; Proliferation; Steroid receptor coactivators

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; DIMETHYLBENZ[A]ANTHRACENE; EPIDERMAL GROWTH FACTOR RECEPTOR 3; NUCLEAR RECEPTOR COACTIVATOR 2; PROGESTERONE RECEPTOR A; PROTEIN KINASE B; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; LACTATION; NEWBORN; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PUERPERIUM; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

RATTUS; RODENTIA;

EID: 79959679130     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Aupperlee MD, Smith KT, Kariagina A, Haslam SZ. 2005. Progesterone receptor isoforms A and B: temporal and spatial differences in expression during murine mammary gland development. Endocrinology 146(8):3577-3588.
2. Bouras T, Southey MC, Venter DJ. 2001. Overexpression of the steroid receptor coactivator AIB1 in breast cancer correlates with the absence of estrogen and progesterone receptors and positivity for p53 and HER2/neu. Cancer Res 61(3):903-907.
3. Brede C, Fjeldal P, Skjevrak I, Herikstad H. 2003. Increased migration levels of bisphenol A from polycarbonate baby bottles after dishwashing, boiling and brushing. Food Addit Contam 20(7):684-689.
4. Brown NM, Manzolillo PA, Zhang J-X, Wang J, Lamartiniere CA. 1998. Prenatal TCDD and predisposition for mammary cancer. Carcinogenesis 19(9):1623-1629.
5. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL. 2005. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113:391-395.
6. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. 2008. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 116:39-44.
7. Colditz GA, Frazier AL. 1995. Models of breast cancer show that risk is set by events of early life: prevention efforts must shift focus. Cancer Epidemiol Biomarkers Prev 4(5):567-571.
8. Collette D. 2003. Modelling Survival Data in Medical Research. 2nd ed. Boca Raton, FL:Chapman & Hall/CRC.
9. Dairkee SH, Seok J, Champion S, Sayeed A, Mindrinos M, Xiao W, et al. 2008. Bisphenol A induces a profile of tumor aggressiveness in high-risk cells from breast cancer patients. Cancer Res 68(7):2076-2080.
10. Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, et al. 2007. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115:80-86.
11. European Commission. 2003. 4,4'-Isopropylidenediphenol (Bisphenol-A), CAS No: 80-05-7. Summary Risk Assessment Report. Available: http://ecb.jrc.it/Documents/Existing-Chemicals/RISK_ASSESSMENT/SUMMARY/b isphenolasum325.pdf [accessed 29 April 2009].
12. European Food Safety Authority. 2006. Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food. Eur Food Saf Auth J 428:1-75.
13. Fleming FJ, Myers E, Kelly G, Crotty TB, McDermott EW, O'Higgins NJ, et al. 2004. Expression of SRC-1, AIB1, and PEA3 in HER2 mediated endocrine resistant breast cancer; a predictive role for SRC-1. J Clin Pathol 57(10):1069-1074.
14. Herbst AL, Ulfelder H, Poskanzer DC, Longo LD. 1999. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. 1971. Am J Obstet Gynecol 181(6):1574-1575.
15. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. 2006. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 66(11):5624-5632.
16. Howdeshell KL, Hotchkiss AK, Thayer KA, Vandenbergh JG, vom Saal FS. 1999. Exposure to bisphenol A advances puberty. Nature 401(6755):763-764.
17. Kang JH, Kito K, Kondo F. 2003. Factors influencing the migration of bisphenol A from cans. J Food Prot 66(8):1444-1447.
18. Kang JH, Kondo F, Katayama Y. 2006. Human exposure to bisphenol A. Toxicology 226(2-3):79-89.
19. Karamouzis MV, Badra FA, Papavassiliou AG. 2007. Breast cancer: the upgraded role of HER-3 and HER-4. Int J Biochem Cell Biol 39(5):851-856.
20. Kariagina A, Aupperlee MD, Haslam SZ. 2007. Progesterone receptor isoforms and proliferation in the rat mammary gland during development. Endocrinology 148(6):2723-2736.
21. Kirkegaard T, McGlynn LM, Campbell FM, Muller S, Tovey SM, Dunne B, et al. 2007. Amplified in breast cancer 1 in human epidermal growth factor receptor-positive tumors of tamoxifen-treated breast cancer patients. Clin Cancer Res 13(5):1405-1411.
22. Kuang SQ, Liao L, Wang S, Medina D, O'Malley BW, Xu J. 2005. Mice lacking the amplified in breast cancer 1/steroid receptor coactivator-3 are resistant to chemical carcinogen-induced mammary tumorigenesis. Cancer Res 65(17):7993-8002.
23. Lahusen T, Fereshteh M, Oh A, Wellstein A, Riegel AT. 2007. Epidermal growth factor receptor tyrosine phosphorylation and signaling controlled by a nuclear receptor coactivator, amplified in breast cancer 1. Cancer Res 67(15):7256-7265.
24. Le HH, Carlson EM, Chua JP, Belcher SM. 2008. Bisphenol A is released from polycarbonate drinking bottles and mimics the neurotoxic actions of estrogen in developing cerebellar neurons. Toxicol Lett 176(2):149-156.
25. Liu B, Ordonez-Ercan D, Fan Z, Edgerton SM, Yang X, Thor AD. 2007. Downregulation of erbB3 abrogates erbB2-mediated tamoxifen resistance in breast cancer cells. Int J Cancer 120(9):1874-1882.
26. Markey CM, Luque EH, Munoz de Toro M, Sonnenschein C, Soto AM. 2001. In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 65(4):1215-1223.
27. Markey CM, Wadia PR, Rubin BS, Sonnenschein C, Soto AM. 2005. Long-term effects of fetal exposure to low doses of the xenoestrogen bisphenol-A in the female mouse genital tract. Biol Reprod 72(6):1344-1351.
28. McCullagh P, Nelder JA. 1989. Generalized Linear Models. 2nd ed. London:Chapman & Hall.
29. Mc Ilroy M, Fleming FJ, Buggy Y, Hill AD, Young LS. 2006. Tamoxifen-induced ER-alpha-SRC-3 interaction in HER2 positive human breast cancer; a possible mechanism for ER isoform specific recurrence. Endocr Relat Cancer 13(4):1135-1145.
30. Meyer JS, Alvarez C, Milikowski C, Olson N, Russo I, Russo J, et al. 2005. Breast carcinoma malignancy grading by Bloom-Richardson system vs proliferation index: reproducibility of grade and advantages of proliferation index. Mod Pathol 18(8):1067-1078.
31. Munoz-de-Toro M, Markey CM, Wadia PR, Luque EH, Rubin BS, Sonnenschein C, et al. 2005. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 146(9):4138-4147.
32. Murray TJ, Maffini MV, Ucci AA, Sonnenschein C, Soto AM. 2007. Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod Toxicol 23(3):383-390.
33. National Toxicology Program. 1982. Carcinogenesis Bioassay of Bisphenol A (CAS No. 80-05-7) in F344 Rats and B6C3F1 Mice (Feed Study). TR 215. Research Triangle Park, NC:National Toxicology Program. Available: http://ntp.niehs.nih.gov/ntp/htdocs/LT_rpts/tr215.pdf [accessed 24 April 2009].
34. Osborne CK, Bardou V, Hopp TA, Chamness GC, Hilsenbeck SG, Fuqua SA, et al. 2003. Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J Natl Cancer Inst 95(5):353-361.
35. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. 2001. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Envrion Health Perspect 109:675-680.
36. Russo IH, Russo J. 1978. Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenz[a]anthracene. J Natl Cancer Inst 61(6):1439-1449.
37. Russo J, Gusterson BA, Rogers AE, Russo IH, Wellings SR, van Zwieten MJ. 1990. Comparative study of human and rat mammary tumorigenesis. Lab Invest 62(3):244-278.
38. Russo J, Russo IH. 1978. DNA labeling index and structure of the rat mammary gland as determinants of its susceptibility to carcinogenesis. J Natl Cancer Inst 61(6):1451-1459.
39. Schiff R, Massarweh S, Shou J, Osborne CK. 2003. Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clin Cancer Res 9(1 pt 2):447S-454S.
40. Shyamala G, Yang X, Silberstein G, Barcellos-Hoff MH, Dale E. 1998. Transgenic mice carrying an imbalance in the native ratio of A to B forms of progesterone receptor exhibit developmental abnormalities in mammary glands. Proc Natl Acad Sci USA 95(2):696-701.
41. Sun Y, Irie M, Kishikawa N, Wada M, Kuroda N, Nakashima K. 2004. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 18(8):501-507.
42. Torres-Arzayus MI, Font de Mora J, Yuan J, Vazquez F, Bronson R, Rue M, et al. 2004. High tumor incidence and activation of the PI3K/AKT pathway in transgenic mice define AIB1 as an oncogene. Cancer Cell 6(3):263-274.
43. Troisi R, Hatch EE, Titus-Ernstoff L, Hyer M, Palmer JR, Robboy SJ, et al. 2007. Cancer risk in women prenatally exposed to diethylstilbestrol. Int J Cancer 121(2):356-360.
44. Wadia PR, Vandenberg LN, Schaeberle CM, Rubin BS, Sonnenschein C, Soto AM. 2007. Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ Health Perspect 115:592-598.
45. Wilson NK, Chuang JC, Morgan MK, Lordo RA, Sheldon LS. 2007. An observational study of the potential exposures of preschool children to pentachlorophenol, bisphenol-A, and nonylphenol at home and daycare. Environ Res 103(1):9-20.
46. Wolff MS, Teitelbaum SL, Windham G, Pinney SM, Britton JA, Chelimo C, et al. 2007. Pilot study of urinary biomarkers of phytoestrogens, phthalates, and phenols in girls. Environ Health Perspect 115:116-121.
47. Xu J, Liao L, Ning G, Yoshida-Komiya H, Deng C, O'Malley BW. 2000. The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc Natl Acad Sci USA 97(12):6379-6384.
48. Xu J, Qiu Y, DeMayo FJ, Tsai SY, Tsai MJ, O'Malley BW. 1998. Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science 279(5358):1922-1925.
49. Xu X, Liu Y, Sadamatsu M, Tsutsumi S, Akaike M, Ushijima H, et al. 2007. Perinatal bisphenol A affects the behavior and SRC-1 expression of male pups but does not influence on the thyroid hormone receptors and its responsive gene. Neurosci Res 58(2):149-155.
50. Ye X, Kuklenyik Z, Needham LL, Calafat AM. 2006. Measuring environmental phenols and chlorinated organic chemicals in breast milk using automated on-line column-switching-high performance liquid chromatography-isotope dilution tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 831(1-2):110-115.