Prenatal Origins of Endocrine Disruption

Critical Windows

• Overview
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• For the beginner
• What you can do
• How we created the timeline
• Why is this important?
• Chemicals in the timeline
  • Bisphenol A
  • Dioxin
  • Phthalates
• Scientific references

Normal Human Development

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Chan S, Rovet J. 2003. Thyroid hormones in fetal central nervous system development. Fetal & Maternal Medicine Review 14(3):177-208.

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Evans OB, Hutchins JB. 1997. Development of the Nervous System. Chapter 5 In: Haines DE, ed. Fundamental Neuroscience. New York: Churchill Livingstone.

Fisher DA, Dussault JH, Sack J, Chopra IJ. 1976. Ontogenesis of hypothalamic-pituitary-thyroid function and metabolism in man, sheep, and rat. Recent Prog Horm Res 33:59-116. [PubMed Link]

Fisher DA, Klein AH. 1981. Thyroid development and disorders of thyroid function in the newborn. N Engl J Med 304(12):702-712. [PubMed Link]

Fisher DA. 1997. Fetal thyroid function: Diagnosis and management of fetal thyroid disorders. Clinical Obstetrics & Gynecology 40(1):16-31. [PubMed Link]

Forest, MG, Ducharme JR. 1993. Gonadotropic and gonadal hormones. In: Bertrand J, Rappaport R, Sizonenko PC, eds. Pediatric Endocrinology. Baltimore, MD: Williams & Wilkins.

Glatstein IZ, Yeh J. 1995. Ontogeny of the estrogen receptor in the human fetal uterus. Journal of Clinical Endocrinology & Metabolism 80(3):958-964. [PubMed Link]

Gould DA, Moscoso GJ, Young MP, Barton DP. 2000. Human first trimester fetal ovaries express oncofetal antigens and steroid receptors. J Soc Gynecol Investig 7(2):131-138. [PubMed Link]

Greenberg AH, Czernichow P, Reba RC, Tyson J, Blizzard RM. 1970 Oct. Observations on the maturation of thyroid function in early fetal life. J Clin Invest 49(10):1790-803. [PubMed Link]

Hahn von Dorsche H, Falkmer S. 2000. Ontogenesis of human islets of Langerhans. Review of light and electron microscopic data, immunohistochemical and functional data on fetal development of the endocrine pancreas. Journal of Evolutionary Biochemistry and Physiology 36(6):701-718.

Hannema SE, Hughes IA. 2007. Regulation of Wolffian duct development. Horm Res 67(3):142-151. [PubMed Link]

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Herschkowitz N, Kagan J, Zilles K. 1997. Neurobiological bases of behavioral development in the first year. Neuropediatrics 28(6):296-306. [PubMed Link]

Howdeshell KL. 2002. A model of the development of the brain as a construct of the thyroid system. Environ Health Perspect 110 (suppl 3):337-348. [PubMed Link]

Kaplan SL, Grumbach MM, Aubert ML. 1976. The ontogenesis of pituitary hormones and hypothalamic factors in the human fetus: maturation of central nervous system regulation of anterior pituitary function. Recent Prog Horm Res 32:161-243. [PubMed Link]

Kilby MD. 2003. Thyroid hormones and fetal brain development. Clinical Endocrinology (Oxford) 59(3):280-281. [PubMed Link]

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Marker PC, Donjacour AA, Dahiya R, Cunha GR. 2003. Hormonal, cellular, and molecular control of prostatic development. Dev Biol 253(2):165-174. [PubMed Link]

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Nussey SS, Whitehead SA. 2001. Endocrinology: An Integrated Approach. Oxford, UK: BIOS Scientific Publishers, Ltd.

O'Rahilly R, Muller F. 1999. The embryonic human brain. An atlas of developmental stages. Second edition. New York: Wiley-Liss.

O'Rahilly R, Muller F. 2001. Human embryology & teratology. Third edition. New York: Wiley-Liss.

Picton HM. 2001. Activation of follicle development: the primordial follicle. Theriogenology 55(6):1193-1210. [PubMed Link]

Piper K, Brickwood S, Turnpenny LW, Cameron IT, Ball SG, Wilson DI, Hanley NA. 2004 Apr. Beta cell differentiation during early human pancreas development. J Endocrinol 181(1):11-23. [PubMed Link]

Pryor JL, Hughes C, Foster W, Hales BF, Robaire B. 2000. Critical windows of exposure for children's health: the reproductive system in animals and humans. Environ Health Perspect 108 (Suppl 3):491-503. [PubMed Link]

Rajpert-De Meyts E, Jorgensen N, Graem N, Muller J, Cate RL, Skakkebaek NE. 1999. Expression of anti-Mullerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. Journal of Clinical Endocrinology & Metabolism 84(10):3836-3844. [PubMed Link]

Sadler TW. 2000. Susceptible periods during embryogenesis of the heart and endocrine glands. Environ Health Perspect 108 (suppl 3):555-561. [PubMed Link]

Sadler TW. 2004. Langman's Medical Embryology. Ninth Edition. Maryland: Lippincott Williams & Wilkins.

Shepard TH. 1967. Onset of function in the human fetal thyroid: Biochemical and radioautographic studies from organ culture. Journal of Clinical Endocrinology & Metabolism 27(7):945-958. [PubMed Link]

Simard M, Manthos H, Giaid A, Lefebvre Y, Goodyer CG. 1996 Aug. Ontogeny of growth hormone receptors in human tissues: an immunohistochemical study. J Clin Endocrinol Metab 81(8):3097-102. [PubMed Link]

Sizonenko PC. 1993. Sexual differentiation. In: Bertrand J, Rappaport R, Sizonenko PC, eds. Pediatric Endocrinology. Baltimore, MD: Williams & Wilkins.

Spencer SJ, Mesiano S, Lee JY, Jaffe RB. 1999 Mar. Proliferation and apoptosis in the human adrenal cortex during the fetal and perinatal periods: implications for growth and remodeling. J Clin Endocrinol Metab 84(3):1110-5. [PubMed Link]

Thliveris JA, Currie RW. 1980. Observations on the hypothalamo-hypophyseal portal vasculature in the developing human fetus. Am J Anat 157(4):441-444. [PubMed Link]

Vaskivuo TE, Maentausta M, Torn S, Oduwole O, Lonnberg A, Herva R, Isomaa V, Tapanainen JS. 2005. Estrogen receptors and estrogen-metabolizing enzymes in human ovaries during fetal development. Journal of Clinical Endocrinology & Metabolism 90(6):3752-3756. [PubMed Link]

vom Saal FS, Montano MM, Wang MH. 1992. Sexual differentiation in mammals. In: Colborn T, Clement C, eds. Chemically Induced Alterations in Sexual and Functional Development: The Wildlife/Human ConnectionVolume XXI. Princeton, NJ: Princeton Scientific Publishing Co., Inc. p 17-83. (Mehlman MA, ed. Advances in Modern Environmental Toxicology; 21).

West LJ. 2002 Sep-Oct. Defining critical windows in the development of the human immune system. Hum Exp Toxicol 21(9-10):499-505. [PubMed Link]

Williams CB. 2003. Development of the immune system. In Rudolph's Pediatrics 21st Edition, Rudolph CD & Rudolph AM, Editors. New York: McGraw-Hill.

Winters AJ, Eskay RL, Porter JC. 1974. Concentration and distribution of TRH and LRH in the human fetal brain. Journal of Clinical Endocrinology & Metabolism 39(5):960-963. [PubMed Link]

Xia TG, Blackburn WR, Gardner WA Jr. 1990. Fetal prostate growth and development. Pediatr Pathol 10(4):527-37. [PubMed Link]

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Bisphenol A

Adriani W, Della Seta D, Dessi-Fulgheri F, Farabollini F, Laviola G. 2003. Altered profiles of spontaneous novelty seeking, impulsive behavior, and response to D-amphetamine in rats perinatally exposed to bisphenol A. Environ Health Perspect 111(4):395-401. [PubMed Link]

Aikawa H, Koyama S, Matsuda M, Nakahashi K, Akazome Y, Mori T. 2004. Relief effect of vitamin A on the decreased motility of sperm and the increased incidence of malformed sperm in mice exposed neonatally to bisphenol A. Cell & Tissue Research 315(1):119-124. [PubMed Link]

Akingbemi BT, Sottas CM, Koulova AI, Klinefelter GR, Hardy MP. 2004. Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 145(2):592-603. [PubMed Link]

Aloisi AM, Della Seta D, Rendo C, Ceccarelli I, Scaramuzzino A, Farabollini F. 2002. Exposure to the estrogenic pollutant bisphenol A affects pain behavior induced by subcutaneous formalin injection in male and female rats. Brain Res 937(1-2):1-7. [PubMed Link]

Dessi-Fulgheri F, Porrini S, Farabollini F. 2002. Effects of perinatal exposure to bisphenol A on play behavior of female and male juvenile rats. Environ Health Perspect 110 (suppl 3):403-407. [PubMed Link]

Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque E, Munoz-de-Toro M. 2007. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115(1):80-86. [PubMed Link]

Facciolo RM, Alo R, Madeo M, Canonaco M, Dessi-Fulgheri F. 2002. Early cerebral activities of the environmental estrogen bisphenol A appear to act via the somatostatin receptor subtype sst2. Environ Health Perspect 110 (suppl 3):397-402. [PubMed Link]

Farabollini F, Porrini S, Della Seta D, Bianchi F, Dessi-Fulgheri F. 2002. Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ Health Perspect 110 (suppl 3):409-413. [PubMed Link]

Farabollini F, Porrini S, Dessi-Fulgherit F. 1999. Perinatal exposure to the estrogenic pollutant bisphenol A affects behavior in male and female rats. Pharmacology, Biochemistry & Behavior 64(4):687-694. [PubMed Link]

Gioiosa L, Fissore E, Ghirardelli G, Parmigiani S, Palanza P. 2007. Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Hormones & Behavior 52(3):307-16. [PubMed Link]

Gupta C. 2000. Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals. Proceedings of the Society of Experimental Biology & Medicine 224(2):61-68. [PubMed Link]

Ho SM, Tang WY, 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(11):5624-5632. [PubMed Link]

Honma S, Suzuki A, Buchanan DL, Katsu Y, Watanabe H, Iguchi T. 2002. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 16(2):117-122. [PubMed Link]

Howdeshell KL, vom Saal FS. 2000. Developmental exposure to bisphenol A: Interaction with endogenous estradiol during pregnancy in mice. Am Zool 40(3):429-437.

Ishido M, Morita M, Oka S, Masuo Y. 2005. Alteration of gene expression of G protein-coupled receptors in endocrine disruptors-caused hyperactive rats. Regul Pept 126(1-2):145-153. [PubMed Link]

Kawai K, Murakami S, Senba E, Yamanaka T, Fujiwara Y, Arimura C, Nozaki T, Takii M, Kubo C. 2007. Changes in estrogen receptors alpha and beta expression in the brain of mice exposed prenatally to bisphenol A. Regulatory Toxicology & Pharmacology 47(2):166-170. [PubMed Link]

Kawai K, Nozaki T, Nishikata H, Takii M, Kubo C. 2003. Aggressive behavior and serum testosterone concentration during the maturation process of male mice: The effects of fetal exposure to bisphenol A. Environ Health Perspect 111(2):175-178. [PubMed Link]

Kubo K, Arai O, Omura M, Watanabe R, Ogata R, Aou S. 2003. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res 45(3):345-356. [PubMed Link]

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 & Development 5(1):67-75.

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. [PubMed Link]

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(6):1344-1351. [PubMed Link]

Masuo Y, Morita M, Oka S, Ishido M. 2004. Motor hyperactivity caused by a deficit in dopaminergic neurons and the effects of endocrine disruptors: A study inspired by the physiological roles of PACAP in the brain. Regul Pept 123(1-3):225-234. [PubMed Link]

Miyagawa K, Narita M, Narita M, Akama H, Suzuki T. 2007. Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A. Neurosci Lett 418(3):236-241. [PubMed Link]

Miyawaki J, Sakayama K, Kato H, Yamamoto H, Masuno H. 2007. Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. Journal of Atherosclerosis and Thrombosis 14(5):245-252. [PubMed Link]

Moral R, Wang R, Russo IH, Lamartiniere CA, Pereira J, Russo J. 2008 Jan. Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J Endocrinol 196(1):101-12. [PubMed Link]

Munoz-de-Toro M, Markey C, Wadia PR, Luque EH, Rubin BS, Sonnenschein C, Soto AM. 2005. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 146(9):4138-4147. [PubMed Link]

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(3):383-390. [PubMed Link]

Nagel SC, vom Saal FS, Thayer KA, Dhar MG, Boechler M, Welshons WV. 1997. Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol. Environ Health Perspect 105(1):70-76. [PubMed Link]

Nakamura K, Itoh K, Sugimoto T, Fushiki S. 2007. Prenatal exposure to bisphenol A affects adult murine neocortical structure. Neurosci Lett 420(2):100-105. [PubMed Link]

Nakamura K, Itoh K, Yaoi T, Fujiwara Y, Sugimoto T, Fushiki S. 2006. Murine neocortical histogenesis is perturbed by prenatal exposure to low doses of bisphenol A. J Neurosci Res 84(6):1197-1205. [PubMed Link]

Negishi T, Kawasaki K, Suzaki S, Maeda H, Ishii Y, Kyuwa S, Kuroda Y, Yoshikawa Y. 2004. Behavioral alterations in response to fear-provoking stimuli and tranylcypromine induced by perinatal exposure to bisphenol A and nonylphenol in male rats. Environ Health Perspect 112:1159-1164. [PubMed Link]

Newbold RR, Jefferson WN, Padilla-Banks E. 2007. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol 24(2):253-258. [PubMed Link]

Newbold RR, Jefferson WN, Padilla-Banks E. 2009. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect 117(6):879-885.

Nikaido Y, Yoshizawa K, Danbara N, Tsujita-Kyutoku M, Yuri T, Uehara N, Tsubura A. 2004. Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring. Reprod Toxicol 18(6):803-811. [PubMed Link]

Nishizawa H, Manabe N, Morita M, Sugimoto M, Imanishi S, Miyamoto H. 2003. Effects of in utero exposure to bisphenol A on expression of RARalpha and RXRalpha mRNAs in murine embryos. Journal of Reproduction & Development 49(6):539-545. [PubMed Link]

Nishizawa H, Morita M, Sugimoto M, Imanishi S, Manabe N. 2005. Effects of in utero exposure to bisphenol A on mRNA expression of arylhydrocarbon and retinoid receptors in murine embryos. Journal of Reproduction & Development 51(3):315-324. [PubMed Link]

Okada A, Kai O. 2008 Mar. Effects of estradiol-17beta and bisphenol A administered chronically to mice throughout pregnancy and lactation on the male pups' reproductive system. Asian Journal of Androl 10(2):271-6. [PubMed Link]

Palanza P, Gioiosa L, vom Saal FS, Parmigiani S. 2008 Oct. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ Res 108(2):150-7. [PubMed Link]

Palanza PL, Howdeshell KL, Parmigiani S, vom Saal FS. 2002. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ Health Perspect 110 (suppl 3):415-422. [PubMed Link]

Ramos JG, Varayoud J, Kass L, Rodriguez H, Costabel L, Munoz-De-Toro M, Luque EH. 2003. Bisphenol A induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 144(7):3206-3215. [PubMed Link]

Ramos JG, Varayoud J, Sonnenschein C, Soto AM, Munoz de Toro M, Luque EH. 2001. Prenatal exposure to low doses of bisphenol A alters the periductal stroma and glandular cell function in the rat ventral prostate. Biol Reprod 65(4):1271-1277. [PubMed Link]

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(8):3681-3691. [PubMed Link]

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(7):675-680. [PubMed Link]

Ryan BC, Vandenbergh JG. 2006. Developmental exposure to environmental estrogens alters anxiety and spatial memory in female mice. Hormones & Behavior 50(1):85-93. [PubMed Link]

Sato K, Matsuki N, Ohno Y, Nakazawa K. 2002. Effects of 17beta-estradiol and xenoestrogens on the neuronal survival in an organotypic hippocampal culture. Neuroendocrinology 76(4):223-234. [PubMed Link]

Schonfelder G, Friedrich K, Paul M, Chahoud I. 2004. Developmental effects of prenatal exposure to bisphenol A on the uterus of rat offspring. Neoplasia 6(5):584-594. [PubMed Link]

Smith CC, Taylor HS. 2007. Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development. FASEB J 21(1):239-246. [PubMed Link]

Susiarjo M, Hassold TJ, Freeman E, Hunt PA. 2007. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genetics 3(1):63-70. [PubMed Link]

Takai Y, Tsutsumi O, Ikezuki Y, Hiroi H, Osuga Y, Momoeda M, Yano T, Taketani Y. 2000. Estrogen receptor-mediated effects of a xenoestrogen, bisphenol A, on preimplantation mouse embryos. Biochemical & Biophysical Research Communications 270(3):918-921. [PubMed Link]

Takai Y, Tsutsumi O, Ikezuki Y, Kamei Y, Osuga Y, Yano T, Taketan Y. 2001. Preimplantation exposure to bisphenol A advances postnatal development. Reprod Toxicol 15(1):71-74. [PubMed Link]

Talsness C, Fialkowski O, Gericke C, Merker H-J, Chahoud I. 2000. The effects of low and high doses of bisphenol A on the reproductive system of female and male rat offspring. Congenital Anomalies 40:S94-S107.

Tanabe N, Kimoto T, Kawato S. 2006. Rapid Ca2+ signaling induced by bisphenol A in cultured rat hippocampal neurons. Neuroendocrinology Letters 27(1-2):97-104. [PubMed Link]

Thuillier R, Wang Y, Culty M. 2003. Prenatal exposure to estrogenic compounds alters the expression pattern of platelet-derived growth factor receptors alpha and beta in neonatal rat testis: Identification of gonocytes as targets of estrogen exposure. Biol Reprod 68(3):867-880. [PubMed Link]

Timms BG, Howdeshell KL, Barton L, Bradley S, Richter CA, vom Saal FS. 2005. Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. Proceedings of the National Academy of Sciences USA 102(19):7014-7019 and cover illustration.

Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, Rubin BS, Soto AM. 2008 Nov-Dec. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol 26(3-4):210-9. [PubMed Link]

Vandenberg LN, Maffini MV, Wadia PR, Sonnenschein C, Rubin BS, Soto AM. 2007. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 148(1):116-127. [PubMed Link]

vom Saal FS, Cooke PS, Buchanan DL, Palanza P, Thayer KA, Nagel SC, Parmigiani S, Welshons WV. 1998. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicology & Industrial Health 14(1-2):239-260. [PubMed Link]

Xu X, Liu Y, Sadamatsu M, Tsutsumi S, Akaike M, Ushijima H, Kato N. 2007. Perinatal bisphenol A affects the behavior and SRC-1 expression of male pups but does not influence on the thyroid hormone receptors and its responsive gene. Neurosci Res 58(2):149-155. [PubMed Link]

Yaoi T, Itoh K, Nakamura K, Ogi H, Fujiwara Y, Fushiki S. 2008. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochemical & Biophysical Research Communications 376(3):563-567. [PubMed Link]

Yokosuka M, Ohtani-Kaneko R, Yamashita K, Muraoka D, Kuroda Y, Watanabe C. 2008. Estrogen and environmental estrogenic chemicals exert developmental effects on rat hypothalamic neurons and glias. Toxicology in Vitro 22(1):1-9. [PubMed Link]

Yoshino S, Yamaki K, Li X, Sai T, Yanagisawa R, Takano H, Taneda S, Hayashi H, Mori Y. 2004. Prenatal exposure to bisphenol A up-regulates immune responses, including T helper 1 and T helper 2 responses, in mice. Immunology 112:489-495. [PubMed Link]

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(2):607-612. [PubMed Link]

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Phthalates

Andrade AJ, Grande SW, Talsness CE, Gericke C, Grote K, Golombiewski A, Sterner-Kock A, Chahoud I. 2006. A dose response study following in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP): Reproductive effects on adult male offspring rats. Toxicology 228(1):85-97. [PubMed Link]

Andrade AJM, Grande SW, Talsness CE, Grote K, Chahoud I. 2006. A dose-response study following in utero and lactational exposure to di-(2-ethylhexyl)-phthalate (DEHP): Non-monotonic dose-response and low dose effects on rat brain aromatase activity. Toxicology 227(3):185-192. [PubMed Link]

Andrade AJM, Grande SW, Talsness CE, Grote K, Golombiewski A, Sterner-Kock A, Chahoud I. 2006. A dose-response study following in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP): Effects on androgenic status, developmental landmarks and testicular histology in male offspring rats. Toxicology 225(1):64-74. [PubMed Link]

Ashby J, Tinwell H, Lefevre PA, Odum J, Paton D, Millward SW, Tittensor S, Brooks AN. 1997. Normal sexual development of rats exposed to butyl benzyl phthalate from conception to weaning. Regulatory Toxicology & Pharmacology 26(1 Part 1):102-118. [PubMed Link]

Grande SW, Andrade AJM, Talsness CE, Grote K, Chahoud I. 2006. A dose-response study following in utero and lactational exposure to di(2-ethylhexyl)phthalate: Effects on female rat reproductive development. Toxicol Sci 91(1):247-254. [PubMed Link]

Ishido M, Masuo Y, Sayato-Suzuki J, Oka S, Niki E, Morita M. 2004 Oct. Dicyclohexylphthalate causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity. J Neurochem 91(1):69-76.

Lehmann KP, Phillips S, Sar M, Foster PMD, Gaido KW. 2004. Dose-dependent alterations in gene expression and testosterone synthesis in the fetal testes of male rats exposed to di (n-butyl) phthalate. Toxicol Sci 81(1):60-68. [PubMed Link]

Sabbieti MG, Agas D, Santoni G, Materazzi S, Menghi G, Marchetti L. 2009. Involvement of p53 in phthalate effects on mouse and rat osteoblasts. J Cell Biochem 107(2):316-327.

Sharpe RM, Fisher JS, Millar MM, Jobling S, Sumpter JP. 1995. Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ Health Perspect 103(12):1136-1143. [PubMed Link]

Yanagisawa R, Takano H, Inoue K, Koike E, Sadakane K, Ichinose T. 2008. Effects of maternal exposure to di-(2-ethylhexyl) phthalate during fetal and/or neonatal periods on atopic dermatitis in male offspring. Environ Health Perspect 116(9):1136-1141.

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Dioxin

Abbott BD, Birnbaum LS. 1990. Rat embryonic palatal shelves respond to TCDD in organ-culture. Toxicol Appl Pharmacol 103(3):441-451. [PubMed Link]

Abbott BD, Held GA, Wood CR, Buckalew AR, Brown JG, Schmid J. 1999. AhR, ARNT, and CYP1A1 mRNA quantitation in cultured human embryonic palates exposed to TCDD and comparison with mouse palate in vivo and in culture. Toxicol Sci 47(1):62-75.

Abbott BD, Lin TM, Rasmussen NT, Albrecht RM, Schmid JE, Peterson RE. 2003. Lack of expression of EGF and TGF-alpha in the fetal mouse alters formation of prostatic epithelial buds and influences the response to TCDD. Toxicol Sci 76(2):427-436. [PubMed Link]

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