[en] Sex steroids and thyroid hormones play a key role in the development of the central nervous system. The critical role of these hormonal systems may explain the sensitivity of the hypothalamus, the cerebral cortex, and the hippocampus to endocrine-disrupting chemicals (EDC). This review examines the evidence for endocrine disruption of glial-neuronal functions in the hypothalamus, hippocampus, and cerebral cortex. Focus was placed on two well-studied EDC, the insecticide dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCB). DDT is involved in neuroendocrine disruption of the reproductive axis, whereas polychlorinated biphenyls (PCB) interact with both the thyroid hormone- and sex steroid-dependent systems and disturb the neuroendocrine control of reproduction and development of hippocampus and cortex. These results highlight the impact of EDC on the developing nervous system and the need for more research in this area.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Environmental sciences & ecology
Author, co-author :
Parent, Anne-Simone ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Agrawal, A. K., Tilson, H. A., and Bondy, S. C. 1981. 3,4,3',4'-Tetrachlorobiphenyl given to mice prenatally produces long-term decreases in striatal dopamine and receptor binding sites in the caudate nucleus. Toxicol. Lett. 7: 417-24. (Pubitemid 11114698)
Alvarez-Dolado, M., Gonzalez-Sancho, J. M., Bernal, J., and Munoz, A. 1998. Developmental expression of the tenascin-C is altered by hypothyroidism in the rat brain. Neuroscience 84: 309-22. (Pubitemid 28081546)
Arulmozhiraja, S., and Morita M. 2004. Structure-activity relationships for the toxicity of polychlorinated dibenzofu-rans: Approach through density functional theory-based descriptors Chem. Res. Toxicol. 17:348-56. (Pubitemid 38375061)
Auso, E., Lavado-Autric, R., Cuevas, E., Del Rey, F. E., Morreale De Escobar, G., and Berbel, P. 2004. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogene-sis alters neuronal migration. Endocrinology 145: 4034-36.
Baas, D., Bourbeau, D., Sarlieve, L. L., Ittel, M. E., Dussault, J. H., and Puymirat, J. 1997. Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia 19: 324-32. (Pubitemid 27165239)
Bakker, J., and Brock, O. 2010. Early oestro-gens in shaping reproductive networks: Evidence for a potential organisational role of oestradiol in female brain development. J. Neuroendocrinol. 22: 728-35.
Bansal, R., and Zoeller, R. T. 2008. Polychlorinated biphenyls (Aroclor 1254) do not uniformly produce agonist actions on thyroid hormone responses in the developing rat brain. Endocrinology 149: 4001-8.
Bastomsky, C. H. 1974. Effects of polychlo-rinated biphenyls: lessons from the Inuit cohort study. Environ. Health Perspect. 111: 1253-58.
Bay, K., Asklund, C., Skakkebaek, N. E., and Andersson, A. M. 2006. Testicular dysgenesis syndrome: possible role of endocrine disrup-tors. Best Pract. Res. Clin. Endocrinol. Metab. 20: 77-90. (Pubitemid 43323765)
Brevik, K., Sweetman, A., Pacyna, J. M., and Jones, K. C. 2002. Towards a global historical inventory for selected PCB congeners-A mass balance approach. 2. Emissions. Sci. Total Environ. 290: 199-224. (Pubitemid 34460498)
Bourguignon, J. P., Gérard, A., Alvarez Gonzalez, M. L., and Franchimont, P. 1992. The neuroendocrine mechanism of onset of puberty: Sequential reduction in activity of inhibitory and facilitatory N-methyl-D-aspartate receptors. J. Clin, Invest. 90: 1736-44.
Bourguignon, J. P., Rasier, G., Lebrethon, M. C., Gérard, A., Naveau, E., and Parent, A. S. 2010. Neuroendocrine disruption of puber-tal timing and interactions between home-ostasis of reproduction and energy balance. Mol Cell Endocrinol. 324:110-20.
Brouwer, A., Morse, D. C., Lans, M. C., Schuur, A. G., Murk, A. J., Klasson-Wheler, E., Bergman, A., and Visser, T. J. 1998. Interactions of persistent environtal organohalogens with the thyroid hormones system: Mechanisms and possible consequences for animal and human health. Toxicol. Ind. Health 14: 59-84. (Pubitemid 28044970)
Cheng, S. Y., Leonard, J. L., and Davis, P. J. 2010. Molecular aspects of thyroid hormone actions. Endocr. Rev. 31:139-70.
Chou, S. M., Miike, T., Payne, W. M., and Davis, G. J. 1979. Neuropathology of "spinning syndrome" induced by prenatal intoxication with a PCB in mice. Ann. NY Acad. Sci. 320: 373-95.
Cohn, B. A., Cirillo, P. M., Wolff, M. S., Schwingl, P. J., Cohen, R. D., Sholtz, R. I., Ferrara, A., Christianson, R. E., van den Berg, B. J., and Siiteri, P. K. 2003. DDT and DDE exposure in mothers and time to pregnancy in daughters. Lancet 361: 2205-6. (Pubitemid 36782556)
Collins, W. T., and Capen, C. C. 1980. Fine structural lesions and hormonal alterations in thyroid glands of perinatal rats exposed in utero and by the milk to polychlorinated biphenyls. Am. J. Pathol. 99: 125-42.
Crews, D., Gore, A. C., Hsu, T. S., Dangleben, N. L., Spinetta, M., Schallert, T., Anway, M. D., and Skinner, M. K. 2007. Transgenerational epigenetic imprints on mate preference. Proc. Nat.Acad. Sci. USA 104: 5942-46. (Pubitemid 47175638)
Cuevas, E., Auso, E., Telefont, M., Morreale de Escobar, G., Sotelo, C., and Berbel, P. 2005. Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminence-derived neurons. Eur. J. Neurosci. 22: 541-51. (Pubitemid 41192265)
Darbre, P. D. 2006. Environmental oestrogens, cosmetics and breast cancer. Best Pract. Res. Clin. Endocrinol. Metab. 20: 121-43. (Pubitemid 43328572)
DeLange, F. 2000. Endemic cretinism. In The thyroid, ed. L. E. Braverman and R. D. Utiger, 756-67. Philadelphia: Lippincott.
Desvergne, B., Feige, J. N., and Casals-Casas, C. 2009. PPAR-mediated activity of phthalates: A link to the obesity epidemic? Mol. Cell. Endocrinol. 304:43-48.
Dewailly, E., Mulvad, G., Pedersen, H. S., Ayotte, P., Demers, A., Weber, J. P., and Hansen, J. C. 1999. Concentration of organochlorines in human brain, liver, and adipose tissue autopsy samples from Greenland. Environ Health Perspect. 107:823-28. (Pubitemid 29525136)
Dickerson, S. M., Guevara, E., Woller, M. J., and Gore, A. C. 2009. Cell death mechanisms in GT1-7 GnRH cells exposed to polychlorinated biphenyl PCB74, PCB118 and PCB153. Toxicol. Appl. Pharmacol. 237: 237-45.
Dietrich, C., and Kaina, B. 2010. The aryl hydrocarbon receptor (AhR) in the regulation of cell-cell contact and tumor growth. Carcinogenesis 31: 1319-28.
Farwell, A. P., and Dubord-Tomasetti, S. A. 1999. Thyroid hormone regulates the extracellular organization of laminin on astro-cytes. Endocrinology 140: 5014-21.
Farwell, A. P., Dubord-Tomasetti, S. A., Pietzykowski, A. Z., Stachelek, S. J., and Leonard, J. L. 2005. Regulation of cerebellar neuronal migration and neurite outgrowth by thyroxine and 3,3',5'-triiodothyronine. Brain Res. Dev. Brain Res. 154: 121-35. (Pubitemid 40023136)
Fenton, S. E. 2006. Endocrine-disrupting compounds and mammary gland development: early exposure and later life consequences. Endocrinology 147: S18-24. (Pubitemid 43764586)
Forrest, D., and Vennstrom, B. 2000. Functions of thyroid hormone receptors in mice. Thyroid 10: 41-52. (Pubitemid 30090364)
Fritsche, E., Cline, J. E., Nguyen, N. H., Scanlan, T. S., and Abel, J. 2005. Polychlorinated biphenyls disturb differentiation of normal neural progenitor cells: Clue for involvement of thyroid hormone receptors. Environ. Health Perspect. 113: 871-76. (Pubitemid 40984187)
Funabashi, T., Sano, A., Mitsushima, D., and Kimura, F. 2003. Bisphenol A increases progesterone receptor immunoreactivity in the hypothalamus in a dose-dependent manner and affects sexual behaviour in adult ovariectomized rats. J. Neuroendocrinol 15: 134-40. (Pubitemid 36193026)
Garcia-Segura, L. M., and Melcangi, R. C. 2006. Steroids and glial cell function. Glia 54: 485-98. (Pubitemid 44449330)
Gauger, K. J., Kato, Y., Haraguchi, K., Lehmler, H. J., Robertson, L. W., Bansal, R., and Zoeller, T. 2004. Polychlorinated biphenyl (PCBs) exert thyroid hormone-like effects in the fetal rat brain but do not bind to thyroid hormone receptors. Environ. Health Perspect. 112: 516-23. (Pubitemid 38500038)
Gilbert, M. E., Mundy, W. R., and Crofton, K. M. 2000. Saptial learning and long-term potentiation in the dentate gyrus of the hippocampus in animals developmentally exposed to Aroclor 1254. Toxicol. Sci. 57: 102-11.
Gilbert, M. E. 2004. Alterations in synaptic transmission and plasticity in area CA1 of adult hippocampus following developmental hypothyroidism. Dev. Brain Res. 148: 11-18. (Pubitemid 38147800)
Gluckman, P. D., and Hanson, M. A. 2004. Living with the past: Evolution, development and patterns of disease. Science 305: 1733-36. (Pubitemid 39249632)
Glynn, A., Aune, M., Darnerud, P. O., Cnattingius, S., Bjerselius, R., Becker, W., and Lignell, S. 2007. Determinants of serum concentrations of organochlorine compounds in Swedish pregnant women: A cross-sectional study. Environ. Health 6: 2.
Gong, J., Dong, J., Wang, Y., Xu, H., Wei, W., Zhong, J., Liu, W., Xi, Q., and Chen, J. 2010. Developmental iodine deficiency and hypothyroidism impair neural development, up-regulate caveolin-1 and down-regulate synaptophysin in rat hippocampus. J. Neuroendocrinol. 22:129-39.
Gore, A. C., Wu, T. J., Oung, T., Lee, J. B., and Woller, M. J. 2002. A novel mechanism for endocrine-disrupting effects of polychlorinated biphenyls: Direct effects on gonadotropin-releasing hormone neurones. J. Neuroendocrinol. 14: 814-23. (Pubitemid 35203479)
Gore, A. C. 2008. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front. Neuroendocrinol. 29: 358-74.
Gorski, R. A. 1968. Influence of age on a paranatal administration of a low dose of androgen. Endocrionology 82: 1001-4.
Heindel, J. J. 2003 Endocrine disruptors and the obesity epidemic. Toxicol. Sci 76: 247-49. (Pubitemid 38035417)
Heindel, J. J., and vom Saal, F. S. 2009. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the oetiology of obesity. Mol. Cell. Endocrinol. 304: 90-96.
Hering, H., and Sheng, M. 2001. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2: 880-88. (Pubitemid 33674075)
Honma, T., Suda, M., Miyagawa, M., Wang, R. S., Kobayashi, K., and Sekiguchi, S. 2009. Alteration of brain neurotransmit-ters in female rat offspring induced by prenatal administration of 16 and 64 mg/kg of 2,2',4,4',5,5'-hexachlorobiphenyl (PCB153). Ind. Health 47: 11-21.
Horn, S., and Heuer, H. 2010. Thyroid hormone action during brain development: more questions than answers. Mol. Cell. Endocrinol. 315: 19-26.
Hojo, Y., Hattori, T. A., Enami, T., Furukawa, A., Suzuki, K., Ishii, H. T., Mukai, H., Morrison, J. H., Janssen, W. G., Kominami, S., Harada, N., Kimoto, T., and Kawato, S. 2004. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aro-matase localized in neurons. Proc. Natl. Acad. Sci. USA 101:865-70. (Pubitemid 38121049)
Hugo, E. R., Brandebourg, T. D., Woo, J. G., Loftus, J., Alexander, J. W., and Ben-Jonathan, N. 2008. Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ. Health Perspect. 116: 1642-47.
Isgor, C., and Sengelaub, D. R. 2003. Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats. J. Neurobiol. 55: 179-90. (Pubitemid 36423157)
Jones, D. C., and Miller, G. W. 2008. The effects of environmental neurotoxicants on the dopaminergic system: A possible role in drug addiction. Biochem. Pharmacol. 76: 569-81.
Kenet, T., Froemke, R. C., Schreiner, C. E., Pessah, I. N., and Merzenich, M. M. 2007. Perinatal exposure to a nanocpolanar poly-chlorinated biphenyl alters tonotopy, receptive fields, and plasticity in rat primary auditory cortex. Proc. Natl. Acad. Sci. USA 104: 7646-51. (Pubitemid 47185960)
Khan, I. A., and Thomas, P. 2001. Disruption of neuroendocrine control of luteiniz-ing hormone secretion by Aroclor 1254 involves inhibition of hypothalamic trypto-phan hydroxylase activity. Biol. Reprod. 64: 955-64. (Pubitemid 32174069)
Kodavanti, P. R., Shin, D. S., Tilson, H. A., and Harry, G. J. 1993. Comparative effects of two polychlorinated biphenyl congeners on calcium homeostasis in rat cerebellar granule cells. Toxicol. Appl. Pharmacol. 123: 97-106. (Pubitemid 23343177)
Kodavanti, P. R. 2006. Neurotoxicity of persistent organic pollutants: Possible mode(s) of action and further considerations. Dose-Response 3: 273-305.
Krstevska-Konstantinova, M., Charlier, C., Craen, M., Du Caju, M., Heinrichs, C., de Beaufort, C., Plomteux, G., and Bourguignon, J. P. 2001. Sexual precocity after immigration from developing countries to Belgium: Evidence of previous exposure to organochlorine pesticides. Hum. Reprod. 16: 1020-26. (Pubitemid 32451843)
Kuhl, A. J., Manning, S., and Brouwer, M. 2005. Brain aromatase in Japanese medaka: Molecular characterization and role in xenoestrogen-induced sex reversal. J. Steroid Biochem. Mol Biol. 96: 67-77. (Pubitemid 41080520)
Lans, M. C., Klasson-Wehler, E., Willemsen, M., Meussen, E., Safe, S., and Brouwer, A. 1993. Structure-dependent, competitive interaction of hydroxy-polychlorinated biphenyls,-dibenzo-p-dioxins, and-dibenzofurans with human transthyretin. Chem. Biol. Interact. 88: 7-21. (Pubitemid 23205415)
Lavado-Autric, R., Auso, E., Garcia-Velasco, J. V., Arufe Mdel, C., Escobar del Rey, F., Berbel, P., and Morreale de Escobar, G. 2003. Early maternal hypothyroxine-mia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J. Clin. Invest. 111: 1073-82. (Pubitemid 36397484)
Lebrethon, M. C., and Bourguignon, J. P. 2001. Central and peripheral isosexual precocious puberty. Curr. Opin. Endocrinol. Diabetes 8: 17-22.
Lein, P. J., Yang, D., Bachstetter, A. D., Tilson, H. A., Harry, G. J., Mervis, R. F., and Kodavanti, P. R. 2007. Ontogenetic alterations in molecular and structural correlates of dendritic growth after developmental exposure to polychlorinated biphenyls. Environ. Health Perspect. 115: 556-63. (Pubitemid 46591105)
Llop, S., Ballester, F., Vizcaino, E., Murcia, M., Lopez-Espinosa, M. J., Rebagliato, M., Vioque, J., Marco, A., and Grimalt, J. O. 2010. Concentrations and determinants of organochlorine levels among pregnant women in eastern Spain. Sci. Total Environ. 408: 5758-67.
Maffucci, J. A., and Gore, A. C. 2009. Hypothalamic neural systems controlling the female reproductive life cycle: Gonadotropin-releasing hormone, gluta-mate, and GABA. Int. Rev. Cell. Mol. Biol. 274: 69-127.
Makri, A., Goveia, M., Balbus, J., and Parkin, R. 2004. Children's susceptibility to chemicals: A review. J. Toxicol. Environ. Health B 7: 417-35.
Mariussen, E., Myhre, O., Reistad, T., and Fonnum, F. 2002. The polychlorinated biphenyl mixture aroclor 1254 induces death of rat cerebellar granule cells: The involvement of the N-methyl-D-aspartate receptor and reactive oxygen species. Toxicol. Appl. Pharmacol. 179: 137-44. (Pubitemid 34279406)
Martinez-Cerdeno, V., Noctor, S. C., and Kriegstein, A. R. 2006. Estradiol stimulates progenitor cell division in the ventricular and subventricular zones of the embryonic neocortex. Eur. J. Neurosci. 24: 3475-88. (Pubitemid 44952613)
Martínez de Arrieta, C., Morte, B., Coloma, A., and Bernal, J. 1999 The human RC3 gene homolog, NRGN contains a thyroid hormone-responsive element located in the first intron. Endocrinology 140: 335-43. (Pubitemid 29011177)
Matagne, V., Rasier, G., Lebrethon, M. C., Gérard, A., and Bourguignon, J. P. 2004 Estradiol stimulation of pulsatile GnRH secretion in vitro: Correlation with perinatal exposure to sex steroids and induction of sexual precocity in vivo. Endocrinology 145: 2775-83. (Pubitemid 38686227)
McEwen, B. S., and Alves, S. E. 1999. Estrogen actions in the central nervous system. Endocr. Rev. 20: 279-307. (Pubitemid 30649809)
McKinney, J. D., and Waller, C. L. 1994. Polychlorinated biphenyls as hormonally active structural analogues. Environ. Health Perspect. 102: 290-97. (Pubitemid 24132275)
McKinney, J. D., and Waller, C. L. 1998. Molecular determinants of hormone mimicry: Halogenated aromatic hydrocarbon environmental agents active. J. Toxicol. Environ. Health B 1: 27-58. (Pubitemid 128693555)
McLachlan, J. A., Simpson, E., and Martin, M. 2006. Endocrine disrupters and female reproductive health. Best Pract. Res. Clin. Endocrinol. Metab. 20: 63-75. (Pubitemid 43323764)
Micevych, P., Bondar, G., and Kuo, J. 2010. Estrogen actions on neuroendocrine glia. Neuroendocrinology 91:211-22.
Moult, P. R., and Harvey, J. 2008. Hormonal regulation of hippocampal dendritic morphology and synaptic plasticity. Cell Adhes. Migration 2: 269-75.
Mundy, W. R., Shafer, T. J., Tilson, H. A., and Kodavanti, P. R. 1999. Extracellular calcium is required for the polychlorinated biphenyl-induced increase of intracellular free calcium levels in cerebellar granule cell culture. Toxicology 136: 27-39. (Pubitemid 29361520)
Newbold, R. R., Padilla-Banks, E., Jefferson, W. N., and Heindel, J. J. 2008. Effects of endocrine disruptors on obesity. Int. J. Androl. 31: 201-8.
Nuñez, J. L., Bambrick, L. L., Krueger, B. K., and McCarthy, M. M. 2005. Prolongation and enhancement of gamma-aminobutyric acid receptor mediated excitation by chronic treatment with estradiol in developing rat hippocampal neurons. Eur. J. Neurosci. 21: 3251-61. (Pubitemid 40961420)
Nygard, M., Wahlstrom, G. M., Gustafsson, M. V., Tokumoto, Y. M., and Bondesson, M. 2003. Hormone-dependent repression of the E2F-1 gene by thyroid hormone receptors. Mol. Endocrinol. 17: 79-92. (Pubitemid 36132660)
Obata, T., and Kubota, S. 2000. Formation of hydroxyl radicals by environmental estrogenlike chemicals in rat striatum. Neurosci. Lett. 296: 41-44.
Ouyang, F., Perry, M. J., Venners, S. A., Chen, C., Wang, B., Yang, G., Fang, Z., Zang, T., Wang, L., Xu, X., and Wang, X. 2005. Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup. Environ. Med. 62: 878-84. (Pubitemid 41729778)
Patisaul, H. B., Dindo, M., Whitten, P. L., and Young, L. J. 2001. Soy isoflavone supplements antagonize reproductive behavior and estrogen receptor alpha-and beta-dependent gene expression in the brain. Endocrinology 142:2946-52. (Pubitemid 32577104)
Parent, A. S., Teilmann, G., Juul, A., Skakkebaek, N. E. Toppari, J., and Bourguignon, J. P. 2003. The timing of normal puberty and the age limits of sexual precocity: Variations around the world, secular trends, and changes after migration. Endocr. Rev. 24: 668-93. (Pubitemid 37330586)
Pellegrini, E., Mouriec, K., Anglade, I., Menuet, A., Le Page, Y., Gueguen, M. M., Marmignon, M. H., Brion, F., Pakdel, F., and Kah, O. 2007. Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish. J. Comp. Neurol. 501: 150-67. (Pubitemid 46155876)
Pruitt, D. L, Meserve, L. A., and Bingman, V. P. 1999. Reduced growth of intra-and infra-pyramidal mossy fibers is produced by continuous exposure to polychlorinated biphenyl. Toxicology 138:11-17. (Pubitemid 29476567)
Purnelle, G., Gérard, A., Czajkowski, V., and Bourguignon, J. P. 1997. Pulsatile secretion of Gonadotropin-releasing hormone (GnRH) by rat hypothalamic explants without cell bodies of GnRH neurons. Neuroendocrinology 66: 305-12. (Pubitemid 27460396)
Puzianowska-Kuznicka, M., Pietrzak, M., Turowska, O., and Nauman, A. 2006. Thyroid hormones and their receptors in the regulation of cell proliferation. Acta Biochim. Pol. 53: 641-50. (Pubitemid 46090114)
Rami, A., and Rabié, A. 1990. Delayed synap-togenesis in the dentate gyrus of the thyroid-deficient developing rat. Dev. Neurosci. 12:398-405.
Ramos, J. G., Varayoud, J., Monje, L., Moreno-Piovano, G., Munoz-de-Toro, M., and Luque, E. H. 2007. Diethylstilbestrol alters the population dynamic of neural precursor cells in the neonatal male rat dentate gyrus. Brain Res. Bull. 71: 619-27. (Pubitemid 46209528)
Rasier, G., Parent, A. S., Gérard, A., Lebrethon, M. C., and Bourguignon, J. P. 2007. Early maturation of Gonadotropin-releasing hormone secretion and sexual precocity after exposure of infantile female rats to estradiol or dichlorodiphenyltrichloroethane. Biol. Reprod. 77: 734-42. (Pubitemid 47494389)
Rasier, G., Parent, A. S., Gérard, A., Denooz, R., Lebrethon, M. C., Charlier, C., and Bourguignon, J. P. 2008. Mechanisms of interaction of endocrine disrupting chemicals with glutamate-evoked secretion of gonadotropin-releasing hormone. Toxicol. Sci.102: 33-41. (Pubitemid 351250467)
Roy, D., Palangat, M., Chen, C.-W., Thomas, R. D., Colerangle, J., Atkinson, A., and Yan, Z.-J. 1997. Biochemical and molecular changes at the cellular level in response to exposure to environmental estrogen-like chemicals. J. Toxicol. Environ. Health 50: 1-29.
Royland, J. E., Parker, J. S., and Gilbert, M. E. 2008a. A genomic analysis of sub-clinical hypothyroidism in hippocampus and neocortex of the developing rat brain. J. Neuroendocrinol. 20:1319-38.
Royland, J. E., Wu, J., Zawia, N. H., and Kodavanti, P. R. 2008b. Gene expression profiles in the cerebellum and hippocampus following exposure to a neurotoxi-cant, Aroclor 1254: Developmental effects. Toxicol. Appl. Pharmacol. 231: 165-78.
Rubin, B. S., Lenkowski, J. R., Schaeberle, C. M., Vandenberg, L. N., Ronsheim, P. M., and Soto, A. M. 2006. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 147: 3681-91. (Pubitemid 44079373)
Sanchez-Alonso, J. A., Lopez-Aparicio, P., Recio, M. N., and Perez-Albarsanz, M. A. 2003. Apoptosis-mediated neurotoxic potential of a planar (PCB 77) and a non-planar (PCB 153) polychlorinated biphenyl congeners in neuronal cell cultures. Toxicol. Lett. 144: 337-49. (Pubitemid 36966717)
Sar, M., and Stumpf, W. E. 1973. Autoradiographic localization of radioactivity in the rat brain after the injection of 1,2,3-H-testosterone. Endocrinology 92: 251-56.
Savabieasfahani, M., Kannan, K., Astapova, O., Evans, N. P., and Padmanabhan, V. 2006. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology 147: 5956-66. (Pubitemid 44833514)
Sawaki, M., Noda, S., Muroi, T., Mitoma, H., Takakura, S., Sakamoto, S., and Yamasaki, K. 2003. In utero through lactational exposure to ethinyl estradiol induces cleft phallus and delayed ovarian dysfunction in the offspring. Toxicol. Sci.75: 402-11. (Pubitemid 37220287)
Schantz, S. L., Moshtaghian, J., and Ness, D. K. 1995. Spatial learning deficits in adult rats exposed to ortho-substituted PCB congeners during gestation and lactation. Fundam. Appl. Toxicol. 26: 117-26.
Schantz, S. L., Widholm, J. J., and Rice, D. C. 2003. Effects of PCB exposure on neuropsy-chological function in children. Environ. Health Perspect. 111: 357-76. (Pubitemid 36395204)
Seegal, R. F., Brosch, K. O., and Okoniewski, R. J. 1997. Effets of in utero and lacta-tional exposure of the laboratory rat to 2,4,2',4'-and 3,4,3',4'-tetrachlorobiphenyl on dopamine function. Toxicol. Appl. Pharmacol. 146: 95-103. (Pubitemid 27406401)
Seegal, R. F. 2000. The neurotoxicological consequences of developmental exposure to PCBs. Toxicol. Sci. 57: 1-3.
Sharpe, R. M. 2006. Pathways of endocrine disruption during male sexual differentiation and masculinisation. Best Pract. Res. Clin. Endocrinol. Metab. 20: 91-110. (Pubitemid 43323766)
Skakkebaek, N. E., Rajpert-De Meyts, E., and Main, K. M. 2001. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum. Reprod. 16: 972-78. (Pubitemid 32451837)
Steinberg, R. M., Juenger, T. E., and Gore, A. C. 2007. The effects of prenatal PCBs on adult female paced mating reproductive behaviors in rats. Hormone Behav. 51: 364-72. (Pubitemid 46365688)
Steinberg, R. M., Walker, D. M., Juenger, T. E., Woller, M. J., and Gore, A. C. 2008. The effects of perinatal PCBs on adult female rat reproduction: Development, reproductive physiology, and second generational effects. Biol. Reprod. 78: 1091-101. (Pubitemid 351749295)
Tan, Y., Chen, C. H., Lawrence, D., and Carpenter, D. O. 2004. Ortho-substituted PCBs kill cells by altering membrane structure. Toxicol. Sci. 80: 54-59. (Pubitemid 38967396)
Teilmann, G., Boas, M., Petersen, J. H., Main, K. M., Gormsen, M., Damgaard, K., Brocks, V., Skakkebæk, N. E., and Jensen, K. T. 2007. Early pituitary-gonadal activation in 5-8 years old adopted girls before clinical signs of puberty: A study of 99 foreign adopted girls and 93 controls. J. Clin. Endocrinol. Metab. 92: 2538-44. (Pubitemid 47037355)
Thompson, C. C., and Potter, G. B. 2000. Thyroid hormone action in neural development. Cereb. Cortex. 10:939-45.
Tokumoto, Y. M., Tang, D. G., and Raff, M. C. 2001. Two molecularly distinct intracellular pathways to oligodendrocyte differentiation: Role of a p53 family protein. EMBO J. 20: 5261-68. (Pubitemid 32910920)
Uchida, K., Yonezawa, M., Nakamura, S., Kobayashi, T. and Machida, T. 2005. Impaired neurogenesis in the growth retarded mouse is reversed by T3 treatment. Neuroreport 16: 103-6. (Pubitemid 40250378)
Unsworth, W. P., Taylor, J. A., and Robinson, J. E. 2005. Prenatal programming of reproductive neuroendocrine function: the effect of prenatal androgens on the development of estrogen positive feedback and ovarian cycles in the ewe. Biol. Reprod. 72: 619-27. (Pubitemid 40279840)
Van Birgelen, A. P. J. M., Smit, E. A., Kampen, I. M., Groeneveld, C. N., Fase, K. M., Van der Kolk, J., Poiger, H., Van den Berg, M., Koeman, J. H., and Brouwer, A. 1995. Subchronic effects of 2,3,7,8-TCDD or PCBs on thyroid hormone metabolism: Use in risk assessment. Eur. J. Pharmacol. 293: 77-85.
Vasiliu, O., Muttineni, J., and Karmaus, W. 2004. In utero exposure to organochlorines and age at menarche. Hum. Reprod. 19: 1506-12. (Pubitemid 38997172)
Viglietti-Panzica, C., Montoncello, B., Mura, E., Pessatti, M., and Panzica, G. 2005 Organizational effects of diethylstilbe-strol on brain vasotocin and sexualbehavior in male quail. Brain Res. Bull. 65:225-33. (Pubitemid 40461967)
Weselak, M., Arbuckle, T. E., and Foster, W. 2007. Pesticide exposures and developmental outcomes: The epidemiological evidence. J. Toxicol. Environ. Health B 10: 41-80.
Williams, G. R. 2008. Neurodevelopmental and neurophysiological actions of thyroid hormone. J. Neuroendocrinol. 20: 784-94. (Pubitemid 351858730)
Wong, P. W, Joy, R. M., Albertson, T. E., Schantz, S. L., and Pessah I. N. 1997. Ortho-substituted 2,2',3,5',6-pentachlorobiphenyl (PCB 95) alters rat hippocampal ryan-odine receptors and neuroplasticity in vitro: Evidence for altered hippocampal function. Neurotoxicology 18: 443-56. (Pubitemid 27392653)
Yang, D., Kim, K. H., Phimister, A., Bachstetter, A. D., Ward, T. R., Stackman, R. W, Mervis, R. F., Wisniewski, A. B., Klein, S. L., Kodavanti, P. R., Anderson, K. A., Wayman, G., Pessah, I. N., and Lein, P. J. 2009. Developmental exposure to polychlorinated biphenyls interferes with experience-dependent dendritic plasticity and ryanodine receptor expression in weanling rats. Environ. Health Perspect. 117: 426-35.
Zhang, J. M., Konkle, A. T. M., Zup, S. L., and McCarthy, M. M 2008. Impact of sex and hormones on new cells in the developing rat hippocampus: A novel source of sex dimorphism. Eur. J. Neurosci. 27: 791-800. (Pubitemid 351365183)
Zhang, L., Blomgren, K., Kuhn, H. G., and Cooper-Kuhn, C. M. 2009. Effects of postnatal thyroid hormone deficiency on neuroge-nesis in the juvenile and adult rat. Neurobiol. Dis. 34: 366-74.
