In utero exposure to bisphenol a shifts the window of susceptibility for mammary carcinogenesis in the rat

Environmental Health Perspectives

Volumn 119, Issue 2, 2011, Pages 1614-1619

  Betancourt, Angela M ^a   Eltoum, Isam A ^a,b   Desmond, Renee A ^b,c   Russo, Jose ^d   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 FOX CHASE CANCER CENTER   (United States)

Author keywords

Bisphenol A; Cell proliferation; Endocrine disruptors; Mammary cancer; Susceptibility

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR ALPHA; NUCLEAR RECEPTOR COACTIVATOR 2; PROGESTERONE RECEPTOR A; PROTEIN BCL 2; RAF PROTEIN; SOMATOMEDIN C RECEPTOR; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; CANCER INCIDENCE; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; NONHUMAN; PERINATAL PERIOD; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

RATTUS;

EID: 79959635753     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Baylin SB, Herman JG, Graff JR, Vertino PM, Issa JP. 1998. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res 72:141-196.
2. Betancourt AM, Mobley JA, Russo J, Lamartiniere CA. 2010. Proteomic analysis in mammary glands of rat offspring exposed in utero to bisphenol A. J Proteomics 73(6):1241-1253.
3. Biles JE, McNeal TP, Begley TH. 1997. Determination of bisphenol A migrating from epoxy can coatings to infant formula liquid concentrates. J Agric Food Chem 45:4697-4700.
4. 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):903-90
5. Bradley CJ, Kledzik GS, Meites J. 1976. Prolactin and estrogen dependency of rat mammary cancers at early and late stages of development. Cancer Res 36:319-324.
6. Brotons JA, Olea-Serrano MF, Villalobos M, Olea N. 1994. Xenoestrogens released from lacquer coating in food cans. Environ Health Perspect 103:608-612.
7. Brown NM, Manzolillo PA, Zhang J-X, Wang J, Lamartiniere CA. 1998. Prenatal TCDD and predisposition for mammary cancer. Carcinogenesis 19(9):1623-1629.
8. Burridge E. 2003. Bisphenol A: product profile. Eur Chem News 14-20:17.
9. 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.
10. Collette D. 2003. Modeling Survival Data in Medical Research. 2nd ed. NewYork:Chapman and Hall/CRC.
11. Dandekar AM, Robinson EA, Appella E, Qasba PK. 1982. Complete sequence analysis of cDNA clones encoding rat whey phosphoprotein: homology to a protease inhibitor. Proc Natl Acad Sci USA 79:3987-3991.
12. 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.
13. Everett JW. 1989. Neurobiology of reproduction in the female rat. A fifty-year perspective. Monogr Endocrinol 32:1-133.
14. Haslam SZ, Bern HA. 1977. Histopathogenesis of 7,12-dimethylbenz[a]anthracene-induced rat mammary tumors. Proc Natl Acad Sci 74(9):4020-4024.
15. Henriksen KL, Rasmussen BB, Lykkesfeldt AE, Møller S, Ejlertsen B, Mouridsen HT. 2009. An ER activity profile including ER, PR, Bcl-2 and IGF-IR may have potential as selection criterion for letrozole or tamoxifen treatment of patients with advanced breast cancer. Acta Oncol 48(4):522-531.
16. Ho S-M, Tang W-Y, de Frausto JB, 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 66:5624-5632.
17. Hsu P-Y, Hsu H-K, Singer GAC, Yan PS, Rodriguez BAT, Liu JC, et al. 2010. Estrogen-mediated epigenetic repression of large chromosomal regions through DNA looping. Genome Res 20(6):733-744.
18. Hu YF, Russo IH, Ao X, Russo J. 1997. Mammary derived growth inhibitor MDGI cloned from human breast epithelial cells is expressed in fully differentiated lobular structures. Int J Oncol 11:5-11.
19. Jenkins S, Raghuraman N, Eltoum I, Carpenter M, Russo J, Lamartiniere CA. 2009. Oral exposure to bisphenol A increases chemically-induced mammary cancer in rats. Environ Health Perspect 117:910-915.
20. Kang JH, Kondo F, Katayama Y. 2006. Human exposure to bisphenol A. Toxicology 226(2-3):79-89.
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. 14C-bisphenol A in male, female, pregnant, fetal, and neonatal rats. Arch Toxicol 79:243-252.
23. Kuroda N, Kinoshita Y, Sun Y, Wada M, Kishikawa N, Nakashima K, et al. 2003. Measurement of bisphenol A levels in human blood serum and ascitic fluid by HPLC using a fluorescent labeling reagent. J Pharm Biomed Anal 30:1743-1749.
24. Lamartiniere CA. 2002. Timing of exposure and mammary cancer risk. J Mammary Gland Biol Neoplasia 7(1):67-76.
25. Lamartiniere CA, Sloop CA, Clark J, Tilson HA, Lucier GW. 1982. Organizational effects of hormones and hormonally-active xenobiotics on postnatal development. In: 12th Conference on Environmental Toxicology, 3-5 November 1981, Dayton, OH. AFAMRL-TR-81-149. Dayton, OH:U.S. Air Force, 96-121.
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. McCormick GM, Moon RC. 1965. Effect of pregnancy and lactation on growth of mammary tumors induced by 7,12-dimethylbenz(a)anthracene (DMBA). Br J Cancer 19:160-166.
28. McIlroy 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.
29. 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 18:1067-1078.
30. Moral R, Wang R, Russo IH, Lamartiniere CA, Pereira J, Russo J. 2008. Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J Endocrinol 196:101-112.
31. Murad T, von Haam E. 1972. Studies of mammary carcinoma induced by 7,12-dimethylbenz(a)anthracene administration. Cancer Res 32:1404-1415.
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 23:383-390.
33. Olea N, Pulgar R, Perez P, Olea-Serrano MF, Rivas A, Novillo-Fertrell A, et al. 1996. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104:298-305.
34. O'Malley BW, Kumar R. 2009. Nuclear receptor coregulators in cancer biology. Cancer Res 69(21):8217-8222
35. Rowell C, Carpenter DM, Lamartiniere CA. 2005. Chemoprevention of breast cancer, proteomic discovery of genistein action in the rat mammary gland. J Nutr 135:2953S-2959S.
36. Russo J, Gusterson BA, Rogers AE, Russo IH, Wellings SR, Van Zwieten MJ. 1990. Comparative study of human and rat mammary tumorigenesis. Lab Invest 62:1-32.
37. 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):1451-1457.
38. Russo J, Saby J, Isenberg W, Russo IH. 1977. Pathogenesis of mammary carcinomas induced in rats by 7,12-dimethylbenz(a)anthracene. J Natl Cancer Inst 49:435-445.
39. Russo J, Tay LK, Ciocca DR, Russo I. 1983. Molecular and cellular basis of the mammary gland susceptibility to carcinogenesis. Environ Health Perspect 49:185-199.
40. Russo J, Wilgu G, Russo IH. 1979. Susceptibility of the mammary gland to carcinogenesis. I. Differentiation of the mammary gland as determinant of tumor incidence and type of lesion. Am J Pathol 96:721-736.
41. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. 2002. Parent bisphenol A accumulation in human maternal-fetal-placental unit. Environ Health Perspect 110:A703-A707.
42. Shina D, Dao TL. 1975. Site of origin of mammary tumors induced by DMBA in the rat. J Natl Cancer Inst (54):1007-1009.
43. Snyder RW, Maness SC, Gaido KW, Welsch F, Sumner SC, Fennell TR. 2000. Metabolism and disposition of bisphenol A in female rats. Toxicol Appl Pharmacol 168:225-234.
44. U.S. EPA (U.S. Environmental Protection Agency). 1988. Bisphenol A (CASRN 80-05-7). Available: http://www.epa.gov/iris/subst/0356.htm [accessed 18 July 2009].
45. Vivanco I, Sawyers CL. 2002. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2:489-501.
46. Welsch CW. 1985. Host factors affecting the growth of carcinogen-induced rat mammary carcinomas: a review and tribute to Charles Brenton Huggins. Cancer Res 45:3415-3443.
47. Welshons WV, Nagel SC, vom Saal FS. 2006. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 147:S56-S69.
48. 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.
49. Yang Y, Spitzer E, Kenney N, Zschiesche W, Li M, Kromminga A, et al. 1994. Members of the fatty acid binding protein family are differentiation factors for the mammary gland. J Cell Biol 127:1097-1109.