Perinatally administered bisphenol A as a potential mammary gland carcinogen in rats

Environmental Health Perspectives

Volumn 121, Issue 9, 2013, Pages 1040-1046

  Acevedo, Nicole ^a   Davis, Barbara ^b   Schaeberle, Cheryl M ^a   Sonnenschein, Carlos ^a   Soto, Ana M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4, 4' ISOPROPYLIDENEDIPHENOL; UNCLASSIFIED DRUG; 4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; CARCINOGEN; PHENOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST ADENOCARCINOMA; BREAST CARCINOMA; BREAST FIBROADENOMA; BREAST LESION; CANCER INCIDENCE; CONTROLLED STUDY; DRUG BLOOD LEVEL; FEMALE; FETUS; GESTATION PERIOD; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOPATHOLOGY; INTRADUCTAL CARCINOMA; LACTATION; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MAMMARY GLAND; NONHUMAN; PERINATAL DRUG EXPOSURE; PRIORITY JOURNAL; RAT; SOLID PHASE EXTRACTION; TANDEM MASS SPECTROMETRY; ANIMAL; BLOOD; CHEMICALLY INDUCED; ENVIRONMENTAL EXPOSURE; EXPERIMENTAL MAMMARY NEOPLASM; HYPERPLASIA; PAGET NIPPLE DISEASE; PREGNANCY; SPRAGUE DAWLEY RAT; TOXICITY; WISTAR FURTH RAT;

PRIMATES; RATTUS; RODENTIA;

ANIMALS; BENZHYDRYL COMPOUNDS; CARCINOGENS, ENVIRONMENTAL; CARCINOMA, DUCTAL; ENVIRONMENTAL EXPOSURE; FEMALE; HYPERPLASIA; MAMMARY NEOPLASMS, ANIMAL; PHENOLS; PREGNANCY; RATS; RATS, INBRED WF; RATS, SPRAGUE-DAWLEY;

EID: 84883305886     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1306734     Document Type: Article

References (56)

1. Ayyanan A, Laribi O, Schuepbach-Mallepell S, Schrick C, Gutierrez M, Tanos T, et al. 2011. Perinatal exposure to bisphenol A increases adult mammary gland progesterone response and cell number. Mol Endocrinol 25:1915-1923.
2. Betancourt AM, Eltoum IA, Desmond RA, Russo J, Lamartiniere CA. 2010. In utero exposure to bisphenol A shifts the window of susceptibility for mammary carcinogenesis in the rat. Environ Health Perspect 118:1614-1619; doi:10.1289/ehp.1002148.
3. Biegel LB, Flaws JA, Hirshfield AN, O'Connor JC, Elliot GS, Ladics GS, et al. 1998. 90-day feeding and one-generation reproduction study in Crl:CD BR rats with 17β-estradiol. Toxicol Sci 44:116-142.
4. Braun MM, Ahlbom A, Floderus B, Brinton LA, Hoover RN. 1995. Effect of twinship on incidence of cancer of the testis, breast, and other sites (Sweden). Cancer Causes Control 6:519-524.
5. Burridge E. 2008. Chemical profile: bisphenol A. ICIS Chem Business 274:48.
6. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham JL. 2005. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113:391-395; doi:10.1289/ehp.7534.
7. Davis B, Fenton S. 2013. Mammary gland. In: Haschek and Rousseaux's Handbook of Toxicologic Pathology, Vol 3 (Haschek WM, Rousseaux CG, Wallig MA, eds). New York:Elsevier Academic Press, 2665-2694.
8. Doerge DR, Vanlandingham M, Twaddle NC, Delclos KB. 2010. Lactational transfer of bisphenol A in Sprague-Dawley rats. Toxicol Lett 199:372-376.
9. 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; doi:10.1289/ehp.9282.
10. Ekbom A, Trichopoulos D, Adami HO, Hsieh CC, Lan SJ. 1992. Evidence of prenatal influences on breast cancer risk. Lancet 340:1015-1018.
11. Fernandez MF, Arrebola JP, Taoufiki J, Nafalón A, Ballesteros O, Pulgar R et al. 2007. Bisphenol-A and chlorinated derivatives in adipose tissue of women. Reprod Toxicol 24:259-264.
12. Herbst AL, Ulfelder H, Poskanzer DC. 1971. Adenocarcinoma of the vagina: association of maternal stilbestrol therapy with tumor appearance in young women. New Engl J Med 284:878-881.
13. Hoover RN, Hyer M, Pfeiffer RM, Adam E, Bond B, Cheville AL, et al. 2011. Adverse health outcomes in women exposed in utero to diethylstilbestrol. N Engl J Med 365:1304-1314.
14. Ikezaki S, Takagi M, Tamura K. 2011. Natural occurrence of neoplastic lesions in young Sprague-Dawley rats. J Toxicol Pathol 24:37-40.
15. Ikezuki Y, Tsutsumi O, Takai Y, Kamei Y, Taketani Y. 2002. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 17:2839-2841.
16. Institute of Laboratory Animal Resources, National Research Council. 2011. Guide for the Care and Use of Laboratory Animals. 8th ed. Washington, DC:National Academies Press. Available: http://www.nap.edu/catalog.php?record_id=12910 [accessed 25 July 2013].
17. Jenkins S, Raghuraman N, Eltoum I, Carpenter M, Russo J, Lamartiniere CA. 2009. Oral exposure to bisphenol A increases dimethylbenzanthracene-induced mammary cancer in rats. Environ Health Perspect 117:910-915; doi:10.1289/ehp.11751.
18. Lotz W, Krause R. 1978. Correlation between the effects of neuroleptics on prolactin release, mammary stimulation and the vaginal cycle in rats. J Endocrinol 76:507-515.
19. Lucas JN, Rudmann DG, Credille KM, Irizarry AR, Peter A, Snyder PW. 2007. The rat mammary gland: morphologic changes as an indicator of systemic hormonal perturbations induced by xenobiotics. Toxicol Pathol 35:199-207.
20. Maffini MV, Soto AM, Calabro JM, Ucci AA, Sonnenschein C. 2004. The stroma as a crucial target in rat mammary gland carcinogenesis. J Cell Sci 117:1495-1502.
21. Markey CM, Luque EH, Munoz de Toromm, Sonnenschein C, Soto AM. 2001. In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 65:1215-1223.
22. Munoz de Toro MM, 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 146:4138-4147.
23. 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.
24. Murray TJ, Ucci AA, Maffini MV, Sonnenschein C, Soto AM. 2009. Histological analysis of low dose NMU effects in the rat mammary gland. BMC Cancer 9:267-275.
25. National Toxicology Program. 2007. Toxicology and Carcinogenesis Study of Genistein (CAS No. 446-72-0) in Sprague-Dawley Rats (Feed Study). NTP TR 545. Research Triangle Park, NC:National Toxicology Program. Available: http://ntp.niehs.nih.gov/ntp/htdocs/LT_rpts/TR545.pdf [accessed 24 July 2013].
26. National Toxicology Program. 2010. Toxicology and Carcinogenesis Study of Ethinyl Estradiol (CAS No. 57-63-6) in Sprague-Dawley Rats (Feed Study). NTP TR 548. Research Triangle Park, NC:National Toxicology Program. Available: http://ntp.niehs.nih.gov/ntp/htdocs/LT_rpts/TR548.pdf [accessed 24 July 2013].
27. Potischman N, Troisi R. 1999. In utero and early life exposures in relation to risk of breast cancer. Cancer Causes Control 10:561-573.
28. Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM. 2006. Evidence of altered brain sexual differentiation in mice exposed perinatally to low environmentally relevant levels of bisphenol A. Endocrinology 147:3681-3691.
29. 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. Environ Health Perspect 109:675-680.
30. Schönfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. 2002. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 110:A703-A707.
31. Son WC, Gopinath C. 2004. Early occurrence of spontaneous tumors in CD-1 mice and Sprague-Dawley rats. Toxicol Pathol 32:371-374.
32. Soto AM, Lin TM, Justicia H, Silvia RM, Sonnenschein C. 1992. An "in culture" bioassay to assess the estrogenicity of xenobiotics. In: Chemically Induced Alterations in Sexual Development: The Wildlife/Human Connection (Colborn T, Clement C, eds). Princeton, NJ:Princeton Scientific Publishing, 295-309.
33. Soto AM, Sonnenschein C. 2011. The tissue organization field theory of cancer: a testable replacement for the somatic mutation theory. BioEssays 33:332-340.
34. Takahashi O, Oishi S. 2000. Disposition of orally administered 2,2-bis(4-hydroxyphenyl) propane (bisphenol A) in pregnant rats and placental transfer to fetuses. Environ Health Perspect 108:931-935.
35. Taylor JA, vom Saal FS, Welshons WV, Drury B, Rottinghaus G, Hunt PA, et al. 2011. Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ Health Perspect 119:422-430; doi:10.1289/ehp.1002514.
36. Tharp AP, Maffini MV, Hunt PA, Vandevoort CA, Sonnenschein C, Soto AM. 2012. Bisphenol A alters the development of the rhesus monkey mammary gland. Proc Natl Acad Sci USA 109:8190-8195.
37. Thomas P, Dong J. 2006. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J Steroid Biochem Mol Biol 102:175-179.
38. 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 121:356-360.
39. U.S. EPA (U.S. Environmental Protection Agency). 1993. Bisphenol A. (CASRN 80-05-7). Available: http://www.epa.gov/iris/subst/0356.htm [accessed 3 June 2013].
40. U.S. EPA (U.S. Environmental Protection Agency). 2005. Technology Transfer Network Air Toxics: 2005 National-Scale Air Toxics Assessment. Glossary of Key Terms. Available: http://www.epa.gov/ttn/atw/natamain/gloss1.html [accessed 3 June 2013].
41. Vandenberg LN, Chauhoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. 2010. Urinary, circulating and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 118:1055-1070; doi:10.1289/ehp.0901716.
42. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, et al. 2013. Regulatory decisions on endocrine disrupting chemicals should be based on the principles of endocrinology. Reprod Toxicol 38:1-15.
43. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. 2007a. Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139-177.
44. Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, Rubin BS, et al. 2008. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol 26:210-219.
45. Vandenberg LN, Maffini MV, Wadia PR, Sonnenschein C, Rubin BS, Soto AM. 2007b. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 148:116-127.
46. vom Saal FS, Akingbemi BT, Belcher SM, Birnbaum LS, Crain DA, Eriksen M et al. 2007. Chapel Hill bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol 24:131-138.
47. Wadia PR, Cabaton NJ, Borrero MD, Rubin BS, Sonnenschein C, Shioda T, et al. 2013. Low-dose BPA exposure alters the mesenchymal and epithelial transcriptomes of the mouse fetal mammary gland. PLoS One 8:e63902; doi:10.1371/journal.pone.0063902.
48. 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; doi:10.1289/ehp.9640.
49. Watson CS, Bulayeva NN, Wozniak AL, Finnerty CC. 2005. Signaling from the membrane via membrane estrogen receptor-α: estrogens, xenoestrogens, and phytoestrogens. Steroids 70:364-371.
50. Weber Lozada K, Keri RA. 2011. Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol Reprod 85:490-497.
51. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, vom Saal FS. 2003. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ Health Perspect 111:994-1006; doi:10.1289/ehp.5494.
52. White SS, Calafat AM, Kuklenyik Z, Villanueva L, Zehr RD, Helfant L, et al. 2007. Gestational PFOA exposure of mice is associated with altered mammary gland development in dams and female offspring. Toxicol Sci 96:133-144.
53. Ye X, Tao LJ, Needham LL, Calafat AM. 2008. Automated on-line column-switching HPLC-MS/MS method for measuring environmental phenols and parabens in serum. Talanta 76:865-871.
54. Yokota H, Iwano H, Endo M, Kobayashi T, Inoue H, Ikushiro S, et al. 1999. Glucuronidation of the environmental oestrogen bisphenol A by an isoform of UDP-glucuronosyltransferase, UGT2B1, in the rat liver. Biochem J 340:405-409.
55. Zalko D, Jacques C, Duplan H, Bruel S, Perdu E. 2011. Viable skin efficiently absorbs and metabolizes bisphenol A. Chemosphere 82:424-430.
56. Zalko D, Soto AM, Dolo L, Dorio C, Ratahao E, Debrauwer L, et al. 2003. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect 111:309-319; doi:10.1289/ehp.5603.