Perinatal exposure to xenoestrogens impairs mammary gland differentiation and modifies milk composition in Wistar rats

Reproductive Toxicology

Volumn 33, Issue 3, 2012, Pages 390-400

  Kass, Laura ^a   Altamirano, Gabriela A ^a   Bosquiazzo, Verónica L ^a   Luque, Enrique H ^a   Muñoz de Toro, Mónica ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Bisphenol A; Lactation; Mammary gland differentiation; Milk proteins

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ALPHA LACTALBUMIN; BETA CASEIN; DIETHYLSTILBESTROL; MILK PROTEIN; PROLACTIN RECEPTOR; STAT5A PROTEIN; STAT5B PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; BREAST DISEASE; CONTROLLED STUDY; FEMALE; GESTATION PERIOD; LACTATION; MAMMARY GLAND; MILK; MILK LEVEL; MILK YIELD; NONHUMAN; PERINATAL DRUG EXPOSURE; PREGNANCY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; TISSUE DIFFERENTIATION; WEANING;

ANIMALS; CASEINS; DIETHYLSTILBESTROL; ESTROGENS; FEMALE; LACTATION; MAMMARY GLANDS, ANIMAL; MATERNAL-FETAL EXCHANGE; MILK; PHENOLS; PREGNANCY; RATS; RATS, WISTAR;

RATTUS; RATTUS NORVEGICUS;

EID: 84859771825     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.02.002     Document Type: Article

References (56)

1. NTP-CERHR NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. NTP CERHR MON 2008, i-III1.
2. Dodds E.C., Fitzgerald M.E.H., Lawson W. Oestrogenic activity of some hydrocarbon derivatives of ethylene. Nature 1937, 140:772.
3. Muñoz-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.
4. Durando M., Kass L., Piva J., Sonnenschein C., Soto A.M., Luque E.H., et al. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 2007, 115:80-86.
5. 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. Environ Health Perspect 2009, 117:910-915.
6. 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. Environ Health Perspect 2010, 118:1614-1619.
7. Swan S.H. Intrauterine exposure to diethylstilbestrol: long-term effects in humans. APMIS 2000, 108:793-804.
8. Rothschild T.C., Boylan E.S., Calhoon R.E., Vonderhaar B.K. Transplacental effects of diethylstilbestrol on mammary development and tumorigenesis in female ACI rats. Cancer Res 1987, 47:4508-4516.
9. Hovey R.C., Asai-Sato M., Warri A., Terry-Koroma B., Colyn N., Ginsburg E., et al. Effects of neonatal exposure to diethylstilbestrol, tamoxifen, and toremifene on the BALB/c mouse mammary gland. Biol Reprod 2005, 72:423-435.
10. Vorderstrasse B.A., Fenton S.E., Bohn A.A., Cundiff J.A., Lawrence B.P. A novel effect of dioxin: exposure during pregnancy severely impairs mammary gland differentiation. Toxicol Sci 2004, 78:248-257.
11. Rayner J.L., Enoch R.R., Fenton S.E. Adverse effects of prenatal exposure to atrazine during a critical period of mammary gland growth. Toxicol Sci 2005, 87:255-266.
12. Teglund S., McKay C., Schuetz E., van Deursen J.M., Stravopodis D., Wang D., et al. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 1998, 93:841-850.
13. Rosen J.M., Wyszomierski S.L., Hadsell D. Regulation of milk protein gene expression. Annu Rev Nutr 1999, 19:407-436.
14. Farrell H.M. Milk, composition and synthesis. Encyclopedia of reproduction 1999, 256-263. Academic Press, San Diego. E. Knobil, J.D. Neill (Eds.).
15. Akers R.M. Lactogenesis. Encyclopedia of reproduction 1999, 979-985. Academic Press, San Diego. E. Knobil, J.D. Neill (Eds.).
16. Brisken C., Rajaram R.D. Alveolar and lactogenic differentiation. J Mammary Gland Biol Neoplasia 2006, 11:239-248.
17. Collier R.J. Lactation, nonhuman. Encyclopedia of reproduction 1999, 973-979. Academic Press, San Diego. E. Knobil, J.D. Neill (Eds.).
18. Imagawa W., Bandyopadhyay G.K., Nandi S. Regulation of mammary epithelial cell growth in mice and rats. Endocr Rev 1990, 11:494-523.
19. Miyoshi K., Shillingford J.M., Smith G.H., Grimm S.L., Wagner K.U., Oka T., et al. Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J Cell Biol 2001, 155:531-542.
20. Naylor M.J., Li N., Cheung J., Lowe E.T., Lambert E., Marlow R., et al. Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J Cell Biol 2005, 171:717-728.
21. 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.
22. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007, 24:199-224.
23. Maranghi F., Tassinari R., Moracci G., Macri C., Mantovani A. Effects of a low oral dose of diethylstilbestrol (DES) on reproductive tract development in F1 female CD-1 mice. Reprod Toxicol 2008, 26:146-150.
24. Kubo K., Arai O., Omura M., Watanabe R., Ogata R., Aou S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res 2003, 45:345-356.
25. Hammes B., Laitman C.J. Diethylstilbestrol (DES) update: recommendations for the identification and management of DES-exposed individuals. J Midwifery Womens Health 2003, 48:19-29.
26. Varayoud J., Ramos J.G., Bosquiazzo V.L., Lower M., Munoz-de-Toro M., Luque E.H. Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology 2011, 152:1101-1111.
27. Mello P.R., Okay T.S., Botelho C. The effects of exposing rats to cigarette smoke on milk production and growth of offspring. J Pediatr (Rio J) 2007, 83:267-273.
28. Bruder E.D., Hoof J.V., Young J.B., Raff H. Epidermal growth factor and parathyroid hormone-related peptide mRNA in the mammary gland and their concentrations in milk: effects of postpartum hypoxia in lactating rats. Horm Metab Res 2008, 40:446-453.
29. Hapon M.B., Varas S.M., Jahn G.A., Gimenez M.S. Effects of hypothyroidism on mammary and liver lipid metabolism in virgin and late-pregnant rats. J Lipid Res 2005, 46:1320-1330.
30. Kass L., Durando M., Ramos J.G., Varayoud J., Powell C.E., Luque E.H., et al. Association of increased estrogen receptor beta2 expression with parity-induced alterations in the rat mammary gland. J Steroid Biochem Mol Biol 2004, 91:29-39.
31. Varayoud J., Ramos J.G., Bosquiazzo V.L., Muñoz-de-Toro M., Luque E.H. Developmental exposure to bisphenol a impairs the uterine response to ovarian steroids in the adult. Endocrinology 2008, 149:5848-5860.
32. Ramos J.G., Varayoud J., Kass L., Rodriguez H., Costabel L., Muñoz-de-Toro M., et al. Bisphenol a induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 2003, 144:3206-3215.
33. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
34. Dobolyi A. Novel potential regulators of maternal adaptations during lactation: tuberoinfundibular Peptide 39 and amylin. J Neuroendocrinol 2011, 23:1002-1008.
35. Jasarevic E., Sieli P.T., Twellman E.E., Welsh T.H., Schachtman T.R., Roberts R.M., et al. Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proc Natl Acad Sci USA 2011, 108:11715-11720.
36. Galea L.A., Barha C.K. Maternal bisphenol A (BPA) decreases attractiveness of male offspring. Proc Natl Acad Sci USA 2011, 108:11305-11306.
37. Kundakovic M., Champagne F.A. Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav Immun 2011, 25:1084-1093.
38. Rubin B.S., Bisphenol A. An endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 2011, 127:27-34.
39. Brummelte S., Galea L.A. Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:766-776.
40. White S.S., Stanko J.P., Kato K., Calafat A.M., Hines E.P., Fenton S.E. Gestational and chronic low-dose PFOA exposures and mammary gland growth and differentiation in three generations of CD-1 mice. Environ Health Perspect 2011, 119:1070-1076.
41. 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. Environ Health Perspect 2011, 119:1053-1061.
42. Cowie A.T., Forsyth I.A., Hart I.C. Hormonal control of lactation. Monogr Endocrinol 1980, 15:I-275.
43. Haslam S.Z., Shyamala G. Progesterone receptors in normal mammary gland: receptor modulations in relation to differentiation. J Cell Biol 1980, 86:730-737.
44. Robinson G.W., McKnight R.A., Smith G.H., Hennighausen L. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development 1995, 121:2079-2090.
45. Neville M.C., McFadden T.B., Forsyth I. Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol Neoplasia 2002, 7:49-66.
46. Nakhasi H.L., Quasba P.K. Quantitation of milk proteins and their mRNAs in rat mammary gland at various stages of gestation and lactation. J Biol Chem 1979, 254:6016-6025.
47. Quirk S.J., Gannell J.E., Fullerton M.J., Funder J.W. Progestins specifically suppress alpha-lactalbumin synthesis and secretion. J Steroid Biochem 1985, 23:901-905.
48. Buser A.C., Obr A.E., Kabotyanski E.B., Grimm S.L., Rosen J.M., Edwards D.P. Progesterone receptor directly inhibits beta-casein gene transcription in mammary epithelial cells through promoting promoter and enhancer repressive chromatin modifications. Mol Endocrinol 2011, 25:955-968.
49. Ormandy C.J., Binart N., Kelly P.A. Mammary gland development in prolactin receptor knockout mice. J Mammary Gland Biol Neoplasia 1997, 2:355-364.
50. Brisken C., Kaur S., Chavarria T.E., Binart N., Sutherland R.L., Weinberg R.A., et al. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol 1999, 210:96-106.
51. Wu W.J., Lee C.F., Hsin C.H., Du J.Y., Hsu T.C., Lin T.H., et al. TGF-beta inhibits prolactin-induced expression of beta-casein by a Smad3-dependent mechanism. J Cell Biochem 2008, 104:1647-1659.
52. Cocolakis E., Dai M., Drevet L., Ho J., Haines E., Ali S., et al. Smad signaling antagonizes STAT5-mediated gene transcription and mammary epithelial cell differentiation. J Biol Chem 2008, 283:1293-1307.
53. Fukushima A., Funabashi T., Kawaguchi M., Mitsushima D., Bisphenol Kimura F. A induces transforming growth factor-beta3 mRNA in the preoptic area: a cDNA expression array and Northern blot study. Neurosci Lett 2007, 411:81-85.
54. Alcaraz J., Xu R., Mori H., Nelson C.M., Mroue R., Spencer V.A., et al. Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J 2008, 27:2829-2838.
55. Xu R., Spencer V.A., Bissell M.J. Extracellular matrix-regulated gene expression requires cooperation of SWI/SNF and transcription factors. J Biol Chem 2007, 282:14992-14999.
56. Morrison B., Cutler M.L. The contribution of adhesion signaling to lactogenesis. J Cell Commun Signal 2010, 4:131-139.