Hormonal interactions in the effects of halogenated aromatic hydrocarbons on the developing brain

Toxicology and Industrial Health

Volumn 14, Issue 2, 1998, Pages 185-208

  Maclusky, Neil J ^a   Brown, Theodore J ^a   Schantz, Susan ^b   Woun Seo, Byung ^b   Peterson, Richard E ^c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

arylhydrocarbons; brain; development; glucocorticoids; sexual differentiation; steroid receptors

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CORTICOSTEROID RECEPTOR; DIOXIN; ESTROGEN DERIVATIVE; ESTROGEN RECEPTOR; HALOGENATED HYDROCARBON; SEX HORMONE; THYROID HORMONE; THYROID HORMONE RECEPTOR;

BRAIN DEVELOPMENT; COGNITIVE DEFECT; CONFERENCE PAPER; ENDOCRINE SYSTEM; HORMONE ACTION; HUMAN; NEUROTOXICITY; NONHUMAN; PRENATAL EXPOSURE; SEX DIFFERENTIATION;

ANIMALIA;

EID: 0031973648     PISSN: 07482337     EISSN: None     Source Type: Journal    
DOI: 10.1177/074823379801400112     Document Type: Article

References (89)

1. Abbott, B.D. (1995). “Review of the interaction between TCDD and glucocorticoids in embryonic palate.” Toxicology 105:365-373.
2. Abbott, B.D., Perdew, G.H., Buckalew, A.R., and Birnbaum, L.S. (1994). “Interactive regulation of Ah and glucocorticoid receptors in the synergistic induction of cleft palate by 2,3,7,8-tetrachlorodibenzo-p-dioxin and hydrocortisone.” Toxicol. Appl. Pharmacol. 128:138-150.
3. Astroff, B. and Safe, S. (1988). “Comparative antiestrogenic activities of 2,3,7,8-tetrachlorodibenzo-p-dioxin and 6-methyl-1,3,8-trichlorodibenzofuran in the female rat.” Toxicol. Appl. Pharmacol. 95:435-443.
4. Astroff, B., Eldridge, B., and Safe, S. (1991). “Inhibition of the 17 beta-estradiol-induced and constitutive expression of the cellular protooncogene c-fos by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the female rat uterus.” Toxicol. Lett. 56:305-315.
5. Beatty, W.W. (1979). “Gonadal hormones and sex differences in non-reproductive behaviors in rodents: Organizational and activational influences.” Horm. Behav. 12:112-163.
6. Beatty, W.W. (1984). “Hormonal organization of sex differences in play fighting and spatial behavior.” Prog. Brain Res. 61:315-330.
7. Bjerke, D.L., Brown, T.J., Maclusky, N.J., Hochberg, R.B., and Peterson, R.E. (1994). “Partial demasculinization and feminization of sex behavior in male rats by in utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin is not associated with alterations in estrogen receptor binding or volumes of sexually differentiated brain nuclei.” Toxicol. Appl. Pharmacol. 127:258-267.
8. Burgess, L.H. and Handa R.J. (1990). “Ovariectomy (OVX) and estrogen (E) replacement in female rats: Effects on ACTH, corticosterone (CORT) mineralocorticoid receptor (MR) and MR mRNA.” Neurosci. Abstracts 16, 1070-Abstract # 439.1.
9. Burgess, L.H. and Handa, R.J. (1992). “Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats.” Endocrinology 131:1261-1269.
10. Burgess, L.H. and Handa, R.J. (1993). “Estrogen-induced alterations in the regulation of mineralocorticoid and glucocorticoid receptor mRNA expression in the female rat anterior pituitary gland and brain.” Mol. Cell Neurosci. 4:191-198.
11. Carey, M.P. and De Kloet, E.R. (1994). “Interaction of progesterone with the hippocampal mineralocorticoid receptor.” Ann. NY Acad. Sci. 746:434-437.
12. Chen, Y.C., Guo, Y.L., Hsu, C.C., and Rogan, W.J. (1992). “Cognitive development of Yu-Cheng (“oil disease”) children prenatally exposed to heat-degraded PCBs.” J. Amer. Med. Assoc. 268:3213-3218.
13. Darnerud, P.O., Morse, D., Klasson-Wehler, E., and Brouwer, A. (1996). “Binding of a 3,3’, 4,4′-tetrachlorobiphenyl (CB-77) metabolite to fetal transthyretin and effects on fetal thyroid hormone levels in mice.” Toxicology 106:105-114.
14. De Kloet, E.R., Oitzl, M.S., and Joels, M. (1993). “Functional implications of brain corticosteroid receptor diversity.” Cell. Mol. Neurobiol. 13:433-455.
15. Dellovade, T.L., Zhu, Y.S., Krey, L., and Pfaff, D.W. (1996). “Thyroid hormone and estrogen interact to regulate behavior.” Proc. Natl. Acad. Sci. USA 93:12581-12586.
16. Dohler, K.D., Coquelin, A., Davis, F., Hines, M., Shryne, J.E., and Gorski, R.A. (1984). “Pre- and postnatal influence of testosterone propionate and diethylstilbestrol on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats.” Brain Res. 302:291-295.
17. Dohler, K.D., Coquelin, A., Davis, F., Hines, M., Shryne, J.E., Sickmoller, P.M., Jarzab, B., and Gorski, R.A. (1986). “Pre- and postnatal influence of an estrogen antagonist and an androgen antagonist on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats.” Neuroendocrinology 42:443-448.
18. Fishman, J., Hellman, L., Zumoff, B., and Gallager, T.F. (1962). “Influence of thyroid hormone on estrogen metabolism in man.” J. Clin. Endocrinol. Metab. 22:389-392.
19. Gala, R.R. and Westphal, U. (1965). “Corticosteroid-binding globulin in the rat: Studies on the sex difference.” Endocrinology 77:841-851.
20. Guillette, L.J., JR. and Guillette, E.A. (1996). “Environmental contaminants and reproductive abnormalities in wildlife: Implications for public health?” Toxicol. Ind. Health 12:537-550.
21. Handa, R.J., Burgess, L.H., Kerr, J.E., and O'Keefe, J.A. (1994). “Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis.” Horm. Behav. 28:464-476.
22. Harris, M., Zacharewski, T., and Safe, S. (1990). “Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds on the occupied nuclear estrogen receptor in MCF-7 human breast cancer cells.” Cancer Res. 50:3579-3584.
23. Herman, J.P. (1993). “Regulation of adrenocorticosteroid receptor mRNA expression in the central nervous system.” Cell. Mol. Neurobiol. 13:349-372.
24. Hutchison, J.B., Beyer, C., Green, S., and Wozniak, A. (1994). “Brain formation of oestrogen in the mouse: Sex dimorphism in aromatase development.” J. Steroid Biochem. Mol. Biol. 49:407-415.
25. Hutchison, J.B., Beyer, C., Hutchison, R.E., and Wozniak, A. (1995). “Sexual dimorphism in the developmental regulation of brain aromatase.” J. Steroid Biochem. Mol. Biol. 53:307-313.
26. Jacobson, J.L., Jacobson, S.W., and Humphrey, H.E. (1990). “Effects of in utero exposure to polychlorinated biphenyls and related contaminants on cognitive functioning in young children. “ J. Pediatr. 116:38-45.
27. Kelce, W.R., Stone, C.R., Laws, S.C., Gray, L.E., Kemppainen, J.A., and Wilson, E.M. (1995). “Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist.” Nature 375:581-585.
28. Kikuyama, S. (1969). “Alteration by neonatal hypothyroidism of the critical period for the induction of persistent estrus in the rat.” Endocrinologia Japonica 16:269-273.
29. Koopman-Esseboom, C., Morse, D.C., Weisglas-Kuperus, N., Lutkeschipholt, I.J., Van Der Paauw, C.G., Tuinstra, L.G.M.T., Brouwer, A., and Sauer, P.J.J. (1994). “Effects of dioxins and polychlorinated biphenyls on thyroid hormone status of pregnant women and their infants.” Pediatr. Res. 36:468-473.
30. Kühnemann, S., Brown, T.J., Hochberg, R.B., and Maclusky, N.J. (1994). “Sex differences I in the development of estrogen receptors in the rat brain.” Horm. Behav. 28:483-491.
31. Kühnemann, S., Brown, T.J., Hochberg, R.B., and Maclusky, N.J. (1995). “Sexual differentiation of estrogen receptor concentrations in the rat brain: Effects of neonatal testosterone exposure.” Brain Res. 691(1-2):229-234.
32. Lauder, J.M. (1983). “Hormonal and humoral influences on brain development. “ Psychoneuroendocrinology 8:121-155.
33. Le Mevel, J.C., Abitibol, S., Beraud, G., and Maniey, J. (1978). “Dynamic changes in plasma adrenocorticotrophin after neurotropic stress in male and female rats.” J. Endocrinol. 76:359-360.
34. Levin, E.D., Schantz, S.L., and Bowman, R.E. (1988). “Delayed spatial alternation deficits resulting from perinatal PCB exposure in monkeys.” Arch. Toxicol. 62:267-273.
35. Lieberburg, I. and McEwen, B.S. (1975). “Estradiol-17β: A metabolite of testosterone recovered in cell nuclei from limbic areas of neonatal rat brains.” Brain Res. 85:165-170.
36. Lieberburg, I., Krey, L.C., and McEwen, B.S. (1979). “Sex differences in serum testosterone and in exchangeable brain cell nuclear estradiol during the neonatal period in rats. “ Brain Res. 178:207-212.
37. Luine, V. and Rodriguez, M. (1994). “Effects of estradiol on radial arm maze performance of young and aged rats.” Behav. Neural Biol. 62:230-236.
38. Luine, V.N., Spencer, R.L., and McEwen, B.S. (1993). “Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function.” Brain Res. 616:65-70.
39. Luine, V., Villegas, M., Martinez, C., and McEwen, B.S. (1994). “Repeated stress causes reversible impairments of spatial memory performance.” Brain Res. 639:167-170.
40. Luine, V., Martinez, C., Villegas, M., Magarinos, A.M., and McEwen, B.S. (1996). “Restraint stress reversibly enhances spatial memory performance.” Physiol. Behav. 59:27-32.
41. Mably, T.A., Bjerke, D.L., Moore, R.W., Gendron-Fitzpatrick, A., and Peterson, R.E. (1992a). “In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. 3. Effects on spermatogenesis and reproductive capability.” Toxicol. Appl. Pharmacol. 114:118-126.
42. Mably, T.A., MOORE, R.W., GOY, R.W., and PETERSON, R.E. (1992b). “ In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. 2. Effects on sexual behavior and the regulation of luteinizing hormone secretion in adulthood.” Toxicol. Appl. Pharmacol. 114:108-117.
43. Mably, T.A., Moore, R.W., and Peterson, R.E. (1992c). “In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. 1. Effects on androgenic status.” Toxicol. Appl. Pharmacol. 114:97-107.
44. Maclusky, N.J. and Naftolin, F. (1981). “Sexual differentiation of the central nervous system.” Science 211:1294-1303.
45. Maclusky, N.J., Yuan, H., Elliott, J., and Brown, T. (1996). “Sex differences in corticosteroid binding in the rat brain: An in vitro autoradiographic study.” Brain Res. 708:71-81.
46. McCormick, C.M., Smythe, J.W., Sharma, S., and Meaney, M.J. (1995). “Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats.” Brain Res. Dev. Brain Res. 84(1):55-61.
47. McEwen B.S., Lieberburg, I., Chaptal, C., Davis, P.G., Krey, L.C., Maclusky, N.J. and Roy, E.J. (1979). “Attenuating the defeminization of the neonatal rat brain: Mechanisms of action of cyproterone acetate, 1,4,6-androsta-triene-3,17-dione and a synthetic progestin, R5020.” Horm. Behav. 13:269-281.
48. McEwen, B.S., Albeck, D., Cameron, H., Chao, H.M., Gould, E., Hastings, N., Kuroday, Luine, V., Magarinos, A.M., and McKittrick, C.R. (1995). “Stress and the brain: A paradoxical role for adrenal steroids.” Vitam. Horm. 51:371-402.
49. Meaney, M.J., Mitchell, J.B., Aitken, D.H., Bhatnagar, S., Bodnoff, S.R., Iny, L.J.S., and Sarrieau, A. (1991). “The effects of neonatal handling on the development of the adrenocortical response to stress: Implications for neuropathology and cognitive deficits in later life.” Psychoneuroendocrinology 16:85-103.
50. Meaney, M.J., Diorio, J., Francis, D., Larocque, S., O'Donnell, D., Smythe, J.W., Sharma, S., and Tannenbaum, B. (1994). “Environmental regulation of the development of glucocorticoid receptor systems in the rat forebrain. The role of serotonin. “ Ann. NY Acad. Sci. 746:260-273.
51. Miranda, R.C., Sohrabji, F., and Toran-Allerand, D. (1994). “Interactions of estrogen with the neurotrophins and their receptors during neural development.” Horm. Behav. 28:367-375.
52. Morse, D.C., Wehler, E.K., Wesseling, W., Koeman, J.H., and Brouwer, A. (1996). “Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (Aroclor 1254).” Toxicol. Appl. Pharmacol. 136:269-279.
53. Nau, H. and Bass, R. (1981). “Transfer of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) to the mouse embryo and fetus.” Toxicology 20:299-308.
54. Nau, H., Bass, R., and Neubert, D. (1986). “Transfer of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) via placenta and milk, and postnatal toxicity in the mouse.” Arch. Toxicol. 59:36-40.
55. Ness, D.K., Schantz, S.L., Moshtaghian, J., and Hansen, L.G. (1993). “Effects of perinatal exposure to specific PCB congeners on thyroid hormone concentrations and thyroid histology in the rat. “ Toxicol. Lett. 68:311-323.
56. O'Donnell, D., Larocque, S., Seckl, J.R., and Meaney, M.J. (1994). “Postnatal handling alters glucocorticoid, but not mineralocorticoid messenger RNA expression in the hippocampus of adult rats.” Brain Res. Mol. Brain Res. 26:242-248.
57. Olton, D.S. and Feustle, W.A. (1981). “Hippocampal function required for non-spatial working memory.” Exp. Brain Res. 41:380-389.
58. Parsons, B., Rainbow, T.C., and McEwen, B.S. (1984). “Organizational effects of testosterone via aromatization on feminine reproductive behavior and neural progestin receptors in rat brain. “ Endocrinology 115:1412-1417.
59. Patnode, K.A. and Curtis, L.R. (1994). “2,2′,4,4′,5,5′- and 3,3′,4,4′,5,5′-hexachlorobiphenyl alteration of uterine progesterone and estrogen receptors coincides with embryotoxicity in mink (Mustela vision).” Toxicol. Appl. Pharmacol. 127:9-18.
60. Pfaff, D.W., Freidin, M.M., WU-PENG, X.S., YIN, J., and ZHU, Y.S. (1994). “Competition for DNA steroid response elements as a possible mechanism for neuroendocrine integration.” J. Steroid Biochem. Mol. Biol. 49:373-379.
61. Phelps, C.P. and Sawyer, C.H. (1976). “Postnatal thyroxine modifies effects of early androgen on lordosis.” Horm. Behav. 7:331-340.
62. Reul, J.M., Sutanto, W., Van Eekelen, J.A., Rothuizen, J., and De Kloet, E.R. (1990). “Central action of adrenal steroids during stress and adaptation.” Adv. Exp. Med. Biol. 274:243-256.
63. Rupprecht, R., Reul, J.M., Van Steensel, B., Spengler. D., Soder, M., Berning, B.H., Holsboer, F., and Damm, K. (1993). “Pharmacological and functional characterization of human mineralocorticoid and glucocorticoid receptor ligands.” Eur. J. Pharmacol. 247:145-154.
64. Safe, S., Astroff, B., Harris, M., Zacharewski, T., Dickerson, R., Romkes, M., and Biegel, L. (1991). “2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds as antioestrogens: Characterization and mechanism of action. “ Pharmacol. Toxicol. 69:400-409.
65. Schantz, S.L. and Bowman, R.E. (1989). “Learning in monkeys exposed perinatally to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD).” Neurotoxicol. Teratol. 11:13-19.
66. Schantz, S.L., Levin, E.D., Bowman, R.E., Heironimus, M.P., and Laughlin, N.K. (1989). “Effects of perinatal PCB exposure on discrimination-reversal learning in monkeys.” Neurotoxicol. Teratol. 11:243-250.
67. Schantz, S.L., Levin, E.D., and Bowman, R.E. (1991). “Long-term neurobehavioral effects of perinatal polychlorinated biphenyl (PCB) exposure in monkeys.” Environ. Toxicol. Chem. 10:747-756.
68. 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. 26:117-126.
69. Schantz, S.L., Seo, B.W., Moshtaghian, J., Peterson, R.E., and Moore, R.W. (1996). “Effects of gestational and lactational exposure to TCDD or coplanar PCBs on spatial learning.” Neurotoxicol. Teratol. 18:305-313.
70. Seegal, R.F., Bush, B., and Brosch, K.O. (1985). “Polychlorinated biphenyls induce regional changes in brain norepinephrine concentrations in adult rats.” Neurotoxicology 6:13-23.
71. Seegal, R.F., Brosch, K.O., and Bush, B. (1986a). “Polychlorinated biphenyls produce regional alterations of dopamine metabolism in rat brain.” Toxicol. Lett. 30:197-202.
72. Seegal, R.F., Brosch, K.O., and Bush, B. (1986b). “Regional alterations in serotonin metabolism induced by oral exposure of rats to polychlorinated biphenyls.” Neurotoxicology 7:155-165.
73. Seegal, R.F., Bush, B., and Brosch, K.O. (1991). “Comparison of effects of Aroclors 1016 and 1260 on non-human primate catecholamine function.” Toxicology 66:145-163.
74. Seo, B.W., Li, M.H., Hansen, L.G., Moore, R.W., Peterson, R.E., and Schantz, S.L. (1995). “Effects of gestational and lactational exposure to coplanar polychlorinated biphenyl (PCB) congeners or 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on thyroid hormone concentrations in weanling rats.” Toxicol. Lett. 78:253-262.
75. Shanks, N., Larocque, S., and Meaney, M.J. (1995). “Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: Early illness and later responsivity to stress.” J. Neurosci. 15:376-384.
76. Smythe, J.W., McCormick, C.M., Rochford, J., and Meaney, M.J. (1994a). “The interaction between prenatal stress and neonatal handling on nociceptive response latencies in male and female rats. “ Physiol. Behav. 55:971-974.
77. Smythe, J.W., Rowe, W.B., and Meaney, M.J. (1994b). “Neonatal handling alters serotonin (5-HT) turnover and 5-HT2 receptor binding in selected brain regions: Relationship to the handling effect on glucocorticoid receptor expression.” Brain Res. Dev. Brain Res. 55:183-189.
78. Spencer, R.L., Miller, A.H., Stein, M., and McEwen, B.S. (1991). “Corticosterone regulation of type I and type II adrenal steroid receptors in brain, pituitary, and immune tissue.” Brain Res. 549:236-246.
79. Spencer, R.L., Miller, A.H., Moday, H., Stein, M., and McEwen, B.S. (1993). “Diurnal differences in basal and acute stress levels of type I and type II adrenal steroid receptor activation in neural and immune tissues.” Endocrinology 133:1941-1950.
80. Toran-Allerand, C.D. (1985). “On the genesis of sexual differentiation of the central nervous system: Morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein.” Prog. Brain Res. 61:63-97.
81. Turner, B.B. (1992). “Sex differences in the binding of type I and type II corticosteroid receptors in rat hippocampus.” Brain Res. 581:229-236.
82. Vaher, P., Luine, V., Gould, E., and McEwen, B.S. (1994a). “Adrenalectomy impairs spatial memory in rats. “ Ann. NY Acad. Sci. 746:405-407.
83. Vaher, P.R., Luine, V.N., Gould, E., and McEwen, B.S. (1994b). “Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology.” Brain Res. 656:71-78.
84. Wang, X., Porter, W., Krishnan, V., Narasimhan, T.R., and Safe, S. (1993). “Mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-mediated decrease of the nuclear estrogen receptor in MCF-7 human breast cancer cells.” Mol. Cell Endocrinol. 96:159-166.
85. Ward, I.L. and Weisz, J. (1980). “Maternal stress alters plasma testosterone in fetal males.” Science 207:328-329.
86. Weisz, J. and Ward, I.L. (1980). “Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses and neonatal offspring.” Endocrinology 106:306-316.
87. Westlind-Danielsson, A., Gould, E., and McEwen, B.S. (1991). “Thyroid hormone causes sexually distinct neurochemical and morphological alterations in rat septal-diagonal band neurons.” J. Neurochem. 56:119-128.
88. Yau, J.L., Olsson, T., Morris, R.G., Meaney, M.J., and Seckl, J.R. (1995). “Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: Relationship with spatial learning in young and aged rats.” Neuroscience 66:571-581.
89. Zhu, Y.S., Yen, P.M., Chin, W.W., and Pfaff, D.W. (1996). “Estrogen and thyroid hormone interaction on regulation of gene expression.” Proc. Natl. Acad. Sci. USA 93:12587-12592.