The male mammary gland: A target for the xenoestrogen bisphenol A

Reproductive Toxicology

Volumn 37, Issue , 2013, Pages 15-23

  Vandenberg, Laura N ^a   Schaeberle, Cheryl M ^b   Rubin, Beverly S ^b   Sonnenschein, Carlos ^b   Soto, Ana M ^b  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Endocrine disruptor; Histology; Morphometric analysis; Non monotonic dose response; Proliferation

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL STRUCTURES; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST DEVELOPMENT; BREAST EPITHELIUM; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HISTOLOGY; LACTATION; MALE; MAMMARY GLAND; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PROGENY; PROTEIN EXPRESSION; REPRODUCTIVE TOXICITY;

AGE FACTORS; ANIMALS; BENZHYDRYL COMPOUNDS; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIUM; ESTROGENS; FEMALE; MALE; MAMMARY GLANDS, ANIMAL; MICE; PHENOLS; PREGNANCY;

EID: 84874431908     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2013.01.002     Document Type: Article

References (54)

1. Hennighausen L., Robinson G.W. Think globally, act locally: the making of a mouse mammary gland. Genes and Development 1998, 12:449-455.
2. Iuanow E., Kettler M., Slanetz P.J. Spectrum of disease in the male breast. Am J Roentgenology 2011, 196:W247-W259.
3. Rudel R.A., Fenton S.E., Ackerman J.M., Euling S.Y., Makris S.L. Environmental exposures and mammary gland development: state of the science, public health implications, and research recommendations. Environmental Health Perspectives 2011, 119:1053-1061.
4. Soto A.M., Vandenberg L.N., Maffini M.V., Sonnenschein C. Does breast cancer start in the womb?. Basic and Clinical Pharmacology and Toxicology 2008, 102:125-133.
5. Markey C.M., Coombs M.A., Sonnenschein C., Soto A.M. Mammalian development in a changing environment: exposure to endocrine disruptors reveals the developmental plasticity of steroid-hormone target organs. Evolution and Development 2003, 5:67-75.
6. Markey C.M., Luque E.H., Munoz-de-Toro M., Sonnenschein C., Soto A.M. In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biology of Reproduction 2001, 65:1215-1223.
7. Munoz-de-Toro M., Markey C.M., Wadia P.R., Luque E.H., Rubin B.S., Sonnenschein C., et al. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146:4138-4147.
8. Vandenberg L.N., Maffini M.V., Schaeberle C.M., Ucci A.A., Sonnenschein C., Rubin B.S., et al. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reproductive Toxicology 2008, 26:210-219.
9. Vandenberg L.N., Maffini M.V., Wadia P.R., Sonnenschein C., Rubin B.S., Soto A.M. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 2007, 148:116-127.
10. Wadia P.R., Vandenberg L.N., Schaeberle C.M., Rubin B.S., Sonnenschein C., Soto A.M. Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environmental Health Perspectives 2007, 115:592-598.
11. Jones L.P., Sampson A., Kang H.J., Kim H.J., Yi Y.W., Kwon S.Y., et al. Loss of BRCA1 leads to an increased sensitivity to bisphenol A. Toxicology Letters 2010, 199:261-268.
12. Betancourt A.M., Eltoum I.A., Desmond R.A., Russo J., Lamartiniere C.A. In utero exposure to bisphenol A shifts the window of susceptibility for mammary carcinogenesis in the rat. Environmental Health Perspectives 2010, 118:1614-1619.
13. Betancourt A.M., Mobley J.A., Russo J., Lamartiniere C.A. Proteomic analysis in mammary glands of rat offspring exposed in utero to bisphenol A. Journal of Proteomics 2010, 73:1241-1253.
14. Jenkins S., Raghuraman N., Eltoum I., Carpenter M., Russo J., Lamartiniere C.A. Oral exposure to bisphenol A increases dimethylbenzanthracene-induced mammary cancer in rats. Environmental Health Perspectives 2009, 117:910-915.
15. Jenkins S., Wang J., Eltoum I., Desmond R., Lamartiniere C.A. Chronic oral exposure to bisphenol A results in a non-monotonic dose response in mammary carcinogenesis and metastasis in MMTV-erbB2 mice. Environmental Health Perspectives 2011, 119:1604-1609.
16. Lamartiniere C.A., Jenkins S., Betancourt A.M., Wang J., Russo J. Exposure to the endocrine disruptor bisphenol A alters susceptibility for mammary cancer. Hormone Molecular Biology and Clinical Investigation 2011, 5:45-52.
17. Moral R., Wang R., Russo I.H., Lamartiniere C.A., Pereira J., Russo J. Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. Journal of Endocrinology 2008, 196:101-112.
18. Ayyanan A., Laribi O., Schuepbach-Mallepell S., Schrick C., Gutierrez M., Tanos T., et al. Perinatal exposure to bisphenol A increases adult mammary gland progesterone response and cell number. Molecular Endocrinology 2011, Epub 2011 Sep 8.
19. Basrur P.K. Disrupted sex differentiation and feminization of man and domestic animals. Environmental Research 2006, 100:18-38.
20. Kratochwil K. Development and loss of androgen responsiveness in the embryonic rudiment of the mouse mammary gland. Developmental Biology 1977, 61:358-365.
21. Kratochwil K., Schwartz P. Tissue interaction in androgen response of embryonic mammary rudiment of mouse: identification of target tissue for testosterone. Proceedings of National Academic Science U S A 1976, 73:4041-4044.
22. Wasner G., Hennermann I., Kratochwil K. Ontogeny of mesenchymal androgen receptors in the embryonic mouse mammary gland. Endocrinology 1983, 113:1771-1780.
23. Drews U. Regression of mouse mammary gland anlagen in recombinants of Tfm and wild-type tissues: testosterone acts via the mesenchyme. Cell 1977, 10:401-404.
24. Kohlerova E., Skarda J. Mouse bioassay to assess oestrogenic and anti-oestrogenic compounds: hydroxytamoxifen, diethylstilbestrol and genistein. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 2004, 51:209-217.
25. Skarda J. Sensitivity and specificity of the bioassay of estrogenicity in mammary gland and seminal vesicles of male mice. Physiological Research 2002, 51:267-276.
26. Skarda J. Bioassay of steroid hormone agonist and antagonist activities of anti-androgens on mammary gland, seminal vesicles and spleen of male mice. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 2003, 50:204-212.
27. Skarda J., Kohlerova E. Mouse bioassay for in vivo screening of oestrogen and progesterone antagonists. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 2006, 53:145-153.
28. Cardy R.H. Sexual dimorphism of the normal rat mammary gland. Veterinary Pathology 1991, 28:139-145.
29. Latendresse J.R., Bucci T.J., Olson G., Mellick P., Weis C.C., Thorn B., et al. Genistein and ethinyl estradiol dietary exposure in multigenerational and chronic studies induce similar proliferative lesions in mammary gland of male Sprague-Dawley rats. Reproductive Toxicology 2009, 28:342-353.
30. Delclos K.B., Bucci T.J., Lomax L.G., Latendresse J.R., Warbritton A., Weis C.C., et al. Effects of dietary genistein exposure during development on male and female CD (Sprague-Dawley) rats. Reproductive Toxicology 2001, 15:647-663.
31. Soto A.M., Lin T.-M., Justicia H., Silvia R.M., Sonnenschein C. An " in culture" bioassay to assess the estrogenicity of xenobiotics. Chemically induced alterations in sexual development: the wildlife/human connection 1992, Princeton Scientific Publishing, Princeton, 295-309.
32. Hennighausen L., Robinson G.W. Signaling pathways in mammary gland development. Developmental Cell 2001, 1:467-475.
33. Robinson G.W., Karpf A.B.C., Kratochwil K. Regulation of mammary gland development by tissue interaction. Journal of Mammary Gland Biology and Neoplasia 1999, 4:9-19.
34. Vandenberg L.N., Chahoud I., Heindel J.J., Padmanabhan V., Paumgartten F.J.R., Schoenfelder G. Urine, serum and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environmental Health Perspectives 2010, 118:1055-1070.
35. Vandenberg L.N., Hauser R., Marcus M., Olea N., Welshons W.V. Human exposure to bisphenol A (BPA). Reproductive Toxicology 2007, 24:139-177.
36. Vom Saal F.S., Akingbemi B.T., Belcher S.M., Birnbaum L.S., Crain D.A., Eriksen M., et al. 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. Reproductive Toxicology 2007, 24:131-138.
37. Vandenberg L.N., Colborn T., Hayes T.B., Heindel J.J., Jacobs D.R., Lee D-H., et al. Hormones and endocrine disrupting chemicals: low dose effects and non-monotonic dose responses. Endocrine Reviews 2012, 33:378-455.
38. Murray T.J., Maffini M.V., Ucci A.A., Sonnenschein C., Soto A.M. Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reproductive Toxicology 2007, 23:383-390.
39. Alonso-Magdalena P., Ropero A.B., Carrera M.P., Cederroth C.R., Baquie M., Gauthier B.R., et al. Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS ONE 2008, 3:e2069.
40. Wetherill Y.B., Akingbemi B.T., Kanno J., McLachlan J.A., Nadal A., Sonnenschein C., et al. In vitro molecular mechanisms of bisphenol A action. Reproductive Toxicology 2007, 24:178-198.
41. Wozniak A.L., Bulayeva N.N., Watson C.S. Xenoestrogens at picomolar to nanomolar concentrations trigger membrane estrogen receptor-alpha mediated Ca++ fluxes and prolactin release in GH3/B6 pituitary tumor cells. Environmental Health Perspectives 2005, 113:431-439.
42. Vandenberg L.N., Wadia P.R., Schaeberle C.M., Rubin B.S., Sonnenschein C., Soto A.M. The mammary gland response to estradiol: monotonic at the cellular level, non-monotonic at the tissue-level of organization. Journal of Steroid Biochemistry and Molecular Biology 2006, 101:263-274.
43. Maidment S.L. Question 2. Which medications effectively reduce pubertal gynaecomastia?. Archives of Disease in Childhood 2010, 95:237-239.
44. Haynes B.A., Mookadam F. Male gynecomastia. Mayo Clinic Proceedings 2009, 84:672.
45. Yeh S., Hu Y.C., Wang P.H., Xie C., Xu Q., Tsai M.Y., et al. Abnormal mammary gland development and growth retardation in female mice and MCF7 breast cancer cells lacking androgen receptor. Journal of Experimental Medicine 2003, 198:1899-1908.
46. Kawai K., Nozaki T., Nishikata H., Aou S., Takii M., Kubo C. Aggressive behavior and serum testosterone concentration during the maturation process of male mice: the effects of fetal exposure to bisphenol A. Environmental Health Perspectives 2003, 111:175-178.
47. Braunstein G.D. Gynecomastia. New England Journal of Medicine 1993, 328:490-495.
48. Braunstein G.D. Environmental gynecomastia. Endocrine Practice 2008, 14:409-411.
49. Clemons J., Glode L.M., Gao D., Flaig T.W. Low-dose diethylstilbestrol for the treatment of advanced prostate cancer. Urologic Oncology 2011.
50. Nebesio T.D., Eugster E.A. Current concepts in normal and abnormal puberty. Current Problems in Pediatric and Adolescent Health Care 2007, 37:50-72.
51. Durmaz E., Ozmert E.N., Erkekoglu P., Giray B., Derman O., Hincal F., et al. Plasma phthalate levels in pubertal gynecomastia. Pediatrics 2010, 125:e122-e129.
52. Tate-Ostroff B.A., Bridges R.S. Nipple development and pup-induced prolactin release in male rats treated prenatally with the antiandrogen flutamide. Psychoneuroendocrinology 1988, 13:309-316.
53. Nation T., Balic A., Buraundi S., Farmer P., Newgreen D., Southwell B., et al. The antiandrogen flutamide perturbs inguinoscrotal testicular descent in the rat and suggests a link with mammary development. Journal of Pediatric Surgery 2009, 44:2330-2334.
54. Wang X.J., Bartolucci-Page E., Fenton S.E., You L. Altered mammary gland development in male rats exposed to genistein and methoxychlor. Toxicological Sciences 2006, 91:93-103.