Low-Dose BPA Exposure Alters the Mesenchymal and Epithelial Transcriptomes of the Mouse Fetal Mammary Gland

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Wadia, Perinaaz R ^a   Cabaton, Nicolas J ^a   Borrero, Michael D ^a   Rubin, Beverly S ^a   Sonnenschein, Carlos ^a   Shioda, Toshi ^b   Soto, Ana M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ETHINYLESTRADIOL; G PROTEIN COUPLED RECEPTOR 30; MESSENGER RNA;

ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CONTROLLED STUDY; FEMALE; FETUS; FOCAL ADHESION; GENE EXPRESSION; MAMMARY GLAND; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENATAL EXPOSURE; STROMA; TRANSCRIPTOMICS;

ANIMALS; APOPTOSIS; BENZHYDRYL COMPOUNDS; CLUSTER ANALYSIS; EPITHELIUM; ESTROGEN RECEPTOR ALPHA; ETHINYL ESTRADIOL; FEMALE; FETUS; FOCAL ADHESIONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MAMMARY GLANDS, ANIMAL; MESODERM; MICE; MICE, INBRED C57BL; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRINCIPAL COMPONENT ANALYSIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; TROPONIN C;

EID: 84877990245     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063902     Document Type: Article

References (52)

1. Dodds EC, Lawson W, (1936) Synthetic estrogenic agents without the phenanthrene nucleus. Nature 137: 996.
2. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM, (2009) Bisphenol-A and the great divide: A review of controversies in the field of endocrine disruption. Endocr Rev 30: 75-95.
3. Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, vom Saal FS, (2009) Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond B Biol Sci 364: 2079-2096.
4. Vandenberg LN, Chauhoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, et al. (2010) Urinary, circulating and tissue biomonitoring studies indicate widespread exposure to Bisphenol A. Environ Health Perspect. 118: 1055-1070.
5. 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.
6. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV, (2007) Human exposure to bisphenol A (BPA). Reproductive Toxicology 24: 139-177.
7. Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, et al. (2006) Evidence of altered brain sexual differentiation in mice exposed perinatally to low environmentally relevant levels of bisphenol A. Endocrinology. 147: 3681-3691.
8. 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: 1344-1351.
9. Munoz de Toro MM, Markey CM, Wadia PR, Luque EH, Rubin BS, et al. (2005) Perinatal exposure to Bisphenol A alters peripubertal mammary gland development in mice. Endocrinology 146: 4138-4147.
10. Markey CM, Luque EH, Munoz de Toro MM, 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.
11. Fenton SE, (2006) Endocrine-disrupting compounds and mammary gland development: Early exposure and later life consequences. Endocrinology 147: S18-S24.
12. Ayyanan A, Laribi O, Schuepbach-Mallepell S, Schrick C, Gutierrez M, et al. (2011) Perinatal exposure to bisphenol a increases adult mammary gland progesterone response and cell number. Mol Endocrinol 25: 1915-1923.
13. Vandenberg LN, Maffini MV, Wadia PR, Sonnenschein C, Rubin BS, et al. (2007) Exposure to the xenoestrogen bisphenol-A alters development of the fetal mammary gland. Endocrinology 148: 116-127.
14. Wadia PR, Vandenberg LN, Schaeberle CM, Rubin BS, Sonnenschein C, et al. (2007) Perinatal Bisphenol-A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ Health Perspect 115: 592-598.
15. Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, et al. (2008) Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reproductive Toxicology 26: 210-219.
16. 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. Reproductive Toxicology 23: 383-390.
17. Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, et al. (2007) Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115: 80-86.
18. Lamartiniere CA, Jenkins S, Betancourt AM, Wang J, Russo J, (2011) Exposure to the endocrine disruptor Bisphenol A alters susceptibility for mammary cancer. Horm Mol Biol Clin Investig 5: 45-52.
19. Soto AM, Sonnenschein C, (2010) Environmental causes of cancer: endocrine disruptors as carcinogens. Nat Rev Endocrinol 6: 363-370.
20. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, et al. (2000) Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127: 4277-4291.
21. Soto AM, Lin T-M, Justicia H, Silvia RM, Sonnenschein C (1992) An "in culture" bioassay to assess the estrogenicity of xenobiotics, In: Colborn T and Clement C editors. Chemically induced alterations in sexual development: the wildlife/human connection. Princeton: Princeton Scientific Publishing. 295-309.
22. Barker M, Rayens W, (2003) Partial least squares for discrimination. Journal of Chemometrics 17: 166-173.
23. Quintas G, Portillo N, Garcia-Canaveras JC, Castell JV, Ferrer A, et al. (2011) Chemometric approaches to improve PLSDA model outcome for predicting human non-alcoholic fatty liver disease using UPLC-MS as a metabolic profiling tool. Metabolomics 8: 86-98.
24. Vandenberg LN, Maffini MV, Wadia PR, Sonnenschein C, Rubin BS, et al. (2007) Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 148: 116-127.
25. Lemmen JG, Broekhof JLM, Kuiper GGJM, Gustafsson JA, Van Der Saag PT, et al. (1999) Expression of estrogen receptor alpha and beta during mouse embryogenesis. Mech Dev 81: 163-167.
26. Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, et al. (2007) In vitro molecular mechanisms of bisphenol A action. Reproductive Toxicology 24: 178-198.
27. 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 Molec Biol 102: 175-179.
28. Simian M, Hirai Y, Navre M, Werb Z, Lochter A, et al. (2001) The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128: 3117-3131.
29. Mangala LS, Arun B, Sahin AA, Mehta K, (2005) Tissue transglutaminase-induced alterations in extracellular matrix inhibit tumor invasion. Mol Cancer 9: 33.
30. Garcia Y, Wilkins B, Collighan RJ, Griffin M, Pandit A, (2008) Towards development of a dermal rudiment for enhanced wound healing response. Biomaterials 29: 857-868.
31. Hirata H, Tatsumi H, Sokabe M, (2008) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J Cell Sci 121: 2795-2804.
32. Ryo A, Wulf G, Lee TH, Lu KP, (2009) Pinning down HER2-ER crosstalk in SMRT regulation. Trends Biochem Sci 34: 162-165.
33. Schlomm T, Luebke AM, Sultmann H, Hellwinkel OJ, Sauer U, et al. (2005) Extraction and processing of high quality RNA from impalpable and macroscopically invisible prostate cancer for microarray gene expression analysis. Int J Oncol 27: 713-720.
34. Liu J, Welm B, Boucher KM, Ebbert MT, Bernard PS, (2012) TRIM29 functions as a tumor suppressor in nontumorigenic breast cells and invasive ER+ breast cancer. Am J Pathol 180: 839-847.
35. Integrated Risk Information System: Bisphenol A. (CASRN 80-05-7) website. Available: http://www.epa.gov/iris/subst/0356.htm. Accessed 2013 April 22.
36. Soriano S, Alonso-Magdalena P, Garcia-Arevalo M, Novials A, Muhammed SJ, et al. (2012) Rapid insulinotropic action of low doses of Bisphenol-A on mouse and human Islets of Langerhans: Role of estrogen receptor beta. PLoS ONE 7: e31109.
37. Veltmaat JM, Mailleux AA, Thiery JP, Bellusci S, (2003) Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation 71: 1-17.
38. Saji S, Jensen EV, Nilsson S, Rylander T, Warner M, et al. (2000) Estrogen receptors-α and β in the rodent mammary gland. Proc Nat Acad Sci USA 97: 337-342.
39. Prasanth GK, Divya LM, Sadasivan C, (2010) Bisphenol-A can bind to human glucocorticoid receptor as an agonist: an in silico study. J Appl Toxicol 30: 769-774.
40. Lee HJ, Chattopadhyay S, Gong EY, Ahn RS, Lee K, (2003) Antiandrogenic Effects of bisphenol A and nonphenol on the function of androgen receptor. Toxicol Sci 75: 40-46.
41. Zoeller RT, Bansal R, Parris C, (2005) Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology 146: 607-612.
42. Sohoni P, Sumpter JP, (1998) Several environmental oestrogens are also anti-androgens. J Endocrinol 158: 327-339.
43. Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, et al. (2002) Thyroid hormone action is disrupted by Bisphenol A as an antagonist. J Clin Endocrinol Metab 87: 5185-5190.
44. Chung CY, Murphy-Ullrich JE, Erickson HP, (1996) Mitogenesis, cell migration, and loss of focal adhesions induced by tenascin-C interacting with its cell surface receptor, annexin II. Mol Biol Cell 7: 883-892.
45. Ricciardelli C, Brooks JH, Suwiwat S, Sakko AJ, Mayne K, et al. (2002) Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with node-negative primary breast cancer. Clin Cancer Res 8: 1054-1060.
46. Chiquet-Ehrismann R, Tucker RP, (2004) Connective tissues: signalling by tenascins. Int J Biochem Cell Biol 36: 1085-1089.
47. Kimata K, Sakakura T, Inaguma Y, Kato M, Nishizuka Y, (1985) Participation of two different mesenchymes in the developing mouse mammary gland: synthesis of basement membrane components by fat pad precursor cells. Journal of Embryology & Experimental Morphology 89: 243-257.
48. Markey CM, Coombs MA, Sonnenschein C, Soto AM, (2003) Mammalian development in a changing environment: exposure to endocrine disruptors reveals the developmental plasticity of steroid-hormone target organs. Evolution and Development 5: 1-9.
49. Mallepell S, Krust A, Chambon P, Brisken C, (2006) Paracrine signaling through the epithelial estrogen receptor α is required for proliferation and morphogenesis in the mammary gland. Proc Nat Acad Sci USA 103: 2196-2201.
50. Paszek MJ, Weaver VM, (2004) The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 9: 325-342.
51. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
52. Bern HA (1992) The fragile fetus, In: Colborn T and Clement C editors. Chemically-Induced Alterations in Sexual and Functional Development: The Wildlife/Human Connection. Princeton: Princeton Scientific Publishing Co.,Inc. 9-15.