Skip to main content
NCBI home page
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 2002 Jun;110(Suppl 3):355–361. doi: 10.1289/ehp.02110s3355

Thyroid hormone, brain development, and the environment.

Thomas R Zoeller 1, Amy L S Dowling 1, Carolyn T A Herzig 1, Eric A Iannacone 1, Kelly J Gauger 1, Ruby Bansal 1
PMCID: PMC1241183  PMID: 12060829

Abstract

Thyroid hormone is essential for normal brain development. Therefore, it is a genuine concern that thyroid function can be altered by a very large number of chemicals routinely found in the environment and in samples of human and wildlife tissues. These chemicals range from natural to manufactured compounds. They can produce thyroid dysfunction when they are absent from the diet, as in the case of iodine, or when they are present in the diet, as in the case of thionamides. Recent clinical evidence strongly suggests that brain development is much more sensitive to thyroid hormone excess or deficit than previously believed. In addition, recent experimental research provides new insight into the developmental processes affected by thyroid hormone. Based on the authors' research focusing on the ability of polychlorinated biphenyls to alter the expression of thyroid hormone-responsive genes in the developing brain, this review provides background information supporting a new way of approaching risk analysis of thyroid disruptors.

Full Text

The Full Text of this article is available as a PDF (147.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alm J., Hagenfeldt L., Larsson A., Lundberg K. Incidence of congenital hypothyroidism: retrospective study of neonatal laboratory screening versus clinical symptoms as indicators leading to diagnosis. Br Med J (Clin Res Ed) 1984 Nov 3;289(6453):1171–1175. doi: 10.1136/bmj.289.6453.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Artavanis-Tsakonas S., Rand M. D., Lake R. J. Notch signaling: cell fate control and signal integration in development. Science. 1999 Apr 30;284(5415):770–776. doi: 10.1126/science.284.5415.770. [DOI] [PubMed] [Google Scholar]
  3. Bakker O., van Beeren H. C., Wiersinga W. M. Desethylamiodarone is a noncompetitive inhibitor of the binding of thyroid hormone to the thyroid hormone beta 1-receptor protein. Endocrinology. 1994 Apr;134(4):1665–1670. doi: 10.1210/endo.134.4.8137729. [DOI] [PubMed] [Google Scholar]
  4. Barres B. A., Lazar M. A., Raff M. C. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development. 1994 May;120(5):1097–1108. doi: 10.1242/dev.120.5.1097. [DOI] [PubMed] [Google Scholar]
  5. Bastomsky C. H., Murthy P. V., Banovac K. Alterations in thyroxine metabolism produced by cutaneous application of microscope immersion oil: effects due to polychlorinated biphenyls. Endocrinology. 1976 May;98(5):1309–1314. doi: 10.1210/endo-98-5-1309. [DOI] [PubMed] [Google Scholar]
  6. Baxter J. D., Dillmann W. H., West B. L., Huber R., Furlow J. D., Fletterick R. J., Webb P., Apriletti J. W., Scanlan T. S. Selective modulation of thyroid hormone receptor action. J Steroid Biochem Mol Biol. 2001 Jan-Mar;76(1-5):31–42. doi: 10.1016/s0960-0760(01)00052-8. [DOI] [PubMed] [Google Scholar]
  7. Bernal J., Nunez J. Thyroid hormones and brain development. Eur J Endocrinol. 1995 Oct;133(4):390–398. doi: 10.1530/eje.0.1330390. [DOI] [PubMed] [Google Scholar]
  8. Bernal J., Pekonen F. Ontogenesis of the nuclear 3,5,3'-triiodothyronine receptor in the human fetal brain. Endocrinology. 1984 Feb;114(2):677–679. doi: 10.1210/endo-114-2-677. [DOI] [PubMed] [Google Scholar]
  9. Boyages S. C., Halpern J. P. Endemic cretinism: toward a unifying hypothesis. Thyroid. 1993 Spring;3(1):59–69. doi: 10.1089/thy.1993.3.59. [DOI] [PubMed] [Google Scholar]
  10. Brouwer A., Morse D. C., Lans M. C., Schuur A. G., Murk A. J., Klasson-Wehler E., Bergman A., Visser T. J. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol Ind Health. 1998 Jan-Apr;14(1-2):59–84. doi: 10.1177/074823379801400107. [DOI] [PubMed] [Google Scholar]
  11. Brown D. D., Wang Z., Furlow J. D., Kanamori A., Schwartzman R. A., Remo B. F., Pinder A. The thyroid hormone-induced tail resorption program during Xenopus laevis metamorphosis. Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):1924–1929. doi: 10.1073/pnas.93.5.1924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brown D. D., Wang Z., Kanamori A., Eliceiri B., Furlow J. D., Schwartzman R. Amphibian metamorphosis: a complex program of gene expression changes controlled by the thyroid hormone. Recent Prog Horm Res. 1995;50:309–315. doi: 10.1016/b978-0-12-571150-0.50018-4. [DOI] [PubMed] [Google Scholar]
  13. Brucker-Davis F. Effects of environmental synthetic chemicals on thyroid function. Thyroid. 1998 Sep;8(9):827–856. doi: 10.1089/thy.1998.8.827. [DOI] [PubMed] [Google Scholar]
  14. Byrne J. J., Carbone J. P., Hanson E. A. Hypothyroidism and abnormalities in the kinetics of thyroid hormone metabolism in rats treated chronically with polychlorinated biphenyl and polybrominated biphenyl. Endocrinology. 1987 Aug;121(2):520–527. doi: 10.1210/endo-121-2-520. [DOI] [PubMed] [Google Scholar]
  15. Calvo R., Obregón M. J., Ruiz de Oña C., Escobar del Rey F., Morreale de Escobar G. Congenital hypothyroidism, as studied in rats. Crucial role of maternal thyroxine but not of 3,5,3'-triiodothyronine in the protection of the fetal brain. J Clin Invest. 1990 Sep;86(3):889–899. doi: 10.1172/JCI114790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cao X. Y., Jiang X. M., Dou Z. H., Rakeman M. A., Zhang M. L., O'Donnell K., Ma T., Amette K., DeLong N., DeLong G. R. Timing of vulnerability of the brain to iodine deficiency in endemic cretinism. N Engl J Med. 1994 Dec 29;331(26):1739–1744. doi: 10.1056/NEJM199412293312603. [DOI] [PubMed] [Google Scholar]
  17. Chan S., Kilby M. D. Thyroid hormone and central nervous system development. J Endocrinol. 2000 Apr;165(1):1–8. doi: 10.1677/joe.0.1650001. [DOI] [PubMed] [Google Scholar]
  18. Chauhan K. R., Kodavanti P. R., McKinney J. D. Assessing the role of ortho-substitution on polychlorinated biphenyl binding to transthyretin, a thyroxine transport protein. Toxicol Appl Pharmacol. 2000 Jan 1;162(1):10–21. doi: 10.1006/taap.1999.8826. [DOI] [PubMed] [Google Scholar]
  19. Cheek A. O., Kow K., Chen J., McLachlan J. A. Potential mechanisms of thyroid disruption in humans: interaction of organochlorine compounds with thyroid receptor, transthyretin, and thyroid-binding globulin. Environ Health Perspect. 1999 Apr;107(4):273–278. doi: 10.1289/ehp.99107273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Collins W. T., Jr, Capen C. C. 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. 1980 Apr;99(1):125–142. [PMC free article] [PubMed] [Google Scholar]
  21. Collins W. T., Jr, Capen C. C., Kasza L., Carter C., Dailey R. E. Effect of polychlorinated biphenyl (PCB) on the thyroid gland of rats. Ultrastructural and biochemical investigations. Am J Pathol. 1977 Oct;89(1):119–136. [PMC free article] [PubMed] [Google Scholar]
  22. Contempré B., Jauniaux E., Calvo R., Jurkovic D., Campbell S., de Escobar G. M. Detection of thyroid hormones in human embryonic cavities during the first trimester of pregnancy. J Clin Endocrinol Metab. 1993 Dec;77(6):1719–1722. doi: 10.1210/jcem.77.6.8263162. [DOI] [PubMed] [Google Scholar]
  23. Darnerud P. O., Morse D., Klasson-Wehler E., Brouwer A. Binding of a 3,3', 4,4'-tetrachlorobiphenyl (CB-77) metabolite to fetal transthyretin and effects on fetal thyroid hormone levels in mice. Toxicology. 1996 Jan 8;106(1-3):105–114. doi: 10.1016/0300-483x(95)03169-g. [DOI] [PubMed] [Google Scholar]
  24. Delange F. Neonatal screening for congenital hypothyroidism: results and perspectives. Horm Res. 1997;48(2):51–61. doi: 10.1159/000185485. [DOI] [PubMed] [Google Scholar]
  25. Dowling A. L., Iannacone E. A., Zoeller R. T. Maternal hypothyroidism selectively affects the expression of neuroendocrine-specific protein A messenger ribonucleic acid in the proliferative zone of the fetal rat brain cortex. Endocrinology. 2001 Jan;142(1):390–399. doi: 10.1210/endo.142.1.7871. [DOI] [PubMed] [Google Scholar]
  26. Dowling A. L., Martz G. U., Leonard J. L., Zoeller R. T. Acute changes in maternal thyroid hormone induce rapid and transient changes in gene expression in fetal rat brain. J Neurosci. 2000 Mar 15;20(6):2255–2265. doi: 10.1523/JNEUROSCI.20-06-02255.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Dowling A. L., Zoeller R. T. Thyroid hormone of maternal origin regulates the expression of RC3/neurogranin mRNA in the fetal rat brain. Brain Res Mol Brain Res. 2000 Oct 20;82(1-2):126–132. doi: 10.1016/s0169-328x(00)00190-x. [DOI] [PubMed] [Google Scholar]
  28. Dussault J. H., Ruel J. Thyroid hormones and brain development. Annu Rev Physiol. 1987;49:321–334. doi: 10.1146/annurev.ph.49.030187.001541. [DOI] [PubMed] [Google Scholar]
  29. Erickson C. K. Ethanol clearance in nine inbred rat strains. Alcohol Clin Exp Res. 1984 Sep-Oct;8(5):491–494. doi: 10.1111/j.1530-0277.1984.tb05710.x. [DOI] [PubMed] [Google Scholar]
  30. Farsetti A., Mitsuhashi T., Desvergne B., Robbins J., Nikodem V. M. Molecular basis of thyroid hormone regulation of myelin basic protein gene expression in rodent brain. J Biol Chem. 1991 Dec 5;266(34):23226–23232. [PubMed] [Google Scholar]
  31. Ferreiro B., Bernal J., Goodyer C. G., Branchard C. L. Estimation of nuclear thyroid hormone receptor saturation in human fetal brain and lung during early gestation. J Clin Endocrinol Metab. 1988 Oct;67(4):853–856. doi: 10.1210/jcem-67-4-853. [DOI] [PubMed] [Google Scholar]
  32. Fisher D. A., Dussault J. H., Foley T. P., Jr, Klein A. H., LaFranchi S., Larsen P. R., Mitchell M. L., Murphey W. H., Walfish P. G. Screening for congenital hypothyroidism: results of screening one million North American infants. J Pediatr. 1979 May;94(5):700–705. doi: 10.1016/s0022-3476(79)80133-x. [DOI] [PubMed] [Google Scholar]
  33. Fisher D. A., Dussault J. H., Sack J., Chopra I. J. Ontogenesis of hypothalamic--pituitary--thyroid function and metabolism in man, sheep, and rat. Recent Prog Horm Res. 1976;33:59–116. doi: 10.1016/b978-0-12-571133-3.50010-6. [DOI] [PubMed] [Google Scholar]
  34. Fortini M. E. Notch and presenilin: a proteolytic mechanism emerges. Curr Opin Cell Biol. 2001 Oct;13(5):627–634. doi: 10.1016/s0955-0674(00)00261-1. [DOI] [PubMed] [Google Scholar]
  35. Gaiano N., Nye J. S., Fishell G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron. 2000 May;26(2):395–404. doi: 10.1016/s0896-6273(00)81172-1. [DOI] [PubMed] [Google Scholar]
  36. Glinoer D., Delange F. The potential repercussions of maternal, fetal, and neonatal hypothyroxinemia on the progeny. Thyroid. 2000 Oct;10(10):871–887. doi: 10.1089/thy.2000.10.871. [DOI] [PubMed] [Google Scholar]
  37. Glinoer D. The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev. 1997 Jun;18(3):404–433. doi: 10.1210/edrv.18.3.0300. [DOI] [PubMed] [Google Scholar]
  38. Goldey E. S., Crofton K. M. Thyroxine replacement attenuates hypothyroxinemia, hearing loss, and motor deficits following developmental exposure to Aroclor 1254 in rats. Toxicol Sci. 1998 Sep;45(1):94–105. doi: 10.1006/toxs.1998.2495. [DOI] [PubMed] [Google Scholar]
  39. Goldey E. S., Kehn L. S., Lau C., Rehnberg G. L., Crofton K. M. Developmental exposure to polychlorinated biphenyls (Aroclor 1254) reduces circulating thyroid hormone concentrations and causes hearing deficits in rats. Toxicol Appl Pharmacol. 1995 Nov;135(1):77–88. doi: 10.1006/taap.1995.1210. [DOI] [PubMed] [Google Scholar]
  40. Goldey E. S., Kehn L. S., Rehnberg G. L., Crofton K. M. Effects of developmental hypothyroidism on auditory and motor function in the rat. Toxicol Appl Pharmacol. 1995 Nov;135(1):67–76. doi: 10.1006/taap.1995.1209. [DOI] [PubMed] [Google Scholar]
  41. Guadaño-Ferraz A., Escámez M. J., Morte B., Vargiu P., Bernal J. Transcriptional induction of RC3/neurogranin by thyroid hormone: differential neuronal sensitivity is not correlated with thyroid hormone receptor distribution in the brain. Brain Res Mol Brain Res. 1997 Oct 3;49(1-2):37–44. doi: 10.1016/s0169-328x(97)00119-8. [DOI] [PubMed] [Google Scholar]
  42. Gupta R. K., Bhatia V., Poptani H., Gujral R. B. Brain metabolite changes on in vivo proton magnetic resonance spectroscopy in children with congenital hypothyroidism. J Pediatr. 1995 Mar;126(3):389–392. doi: 10.1016/s0022-3476(95)70454-x. [DOI] [PubMed] [Google Scholar]
  43. Haddow J. E., Palomaki G. E., Allan W. C., Williams J. R., Knight G. J., Gagnon J., O'Heir C. E., Mitchell M. L., Hermos R. J., Waisbren S. E. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med. 1999 Aug 19;341(8):549–555. doi: 10.1056/NEJM199908193410801. [DOI] [PubMed] [Google Scholar]
  44. Hagmar L., Björk J., Sjödin A., Bergman A., Erfurth E. M. Plasma levels of persistent organohalogens and hormone levels in adult male humans. Arch Environ Health. 2001 Mar-Apr;56(2):138–143. doi: 10.1080/00039890109604065. [DOI] [PubMed] [Google Scholar]
  45. Hagmar L., Rylander L., Dyremark E., Klasson-Wehler E., Erfurth E. M. Plasma concentrations of persistent organochlorines in relation to thyrotropin and thyroid hormone levels in women. Int Arch Occup Environ Health. 2001 Apr;74(3):184–188. doi: 10.1007/s004200000213. [DOI] [PubMed] [Google Scholar]
  46. Hanukoglu A., Perlman K., Shamis I., Brnjac L., Rovet J., Daneman D. Relationship of etiology to treatment in congenital hypothyroidism. J Clin Endocrinol Metab. 2001 Jan;86(1):186–191. doi: 10.1210/jcem.86.1.7124. [DOI] [PubMed] [Google Scholar]
  47. Hood A., Klaassen C. D. Differential effects of microsomal enzyme inducers on in vitro thyroxine (T(4)) and triiodothyronine (T(3)) glucuronidation. Toxicol Sci. 2000 May;55(1):78–84. doi: 10.1093/toxsci/55.1.78. [DOI] [PubMed] [Google Scholar]
  48. Iniguez M. A., De Lecea L., Guadano-Ferraz A., Morte B., Gerendasy D., Sutcliffe J. G., Bernal J. Cell-specific effects of thyroid hormone on RC3/neurogranin expression in rat brain. Endocrinology. 1996 Mar;137(3):1032–1041. doi: 10.1210/endo.137.3.8603571. [DOI] [PubMed] [Google Scholar]
  49. Iskaros J., Pickard M., Evans I., Sinha A., Hardiman P., Ekins R. Thyroid hormone receptor gene expression in first trimester human fetal brain. J Clin Endocrinol Metab. 2000 Jul;85(7):2620–2623. doi: 10.1210/jcem.85.7.6766. [DOI] [PubMed] [Google Scholar]
  50. Iñiguez M. A., Rodriguez-Peña A., Ibarrola N., Aguilera M., Muñoz A., Bernal J. Thyroid hormone regulation of RC3, a brain-specific gene encoding a protein kinase-C substrate. Endocrinology. 1993 Aug;133(2):467–473. doi: 10.1210/endo.133.2.8344193. [DOI] [PubMed] [Google Scholar]
  51. Jacobsen B. B., Brandt N. J. Congenital hypothyroidism in Denmark. Arch Dis Child. 1981 Feb;56(2):134–136. doi: 10.1136/adc.56.2.134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Jacobson J. L., Jacobson S. W., Humphrey H. E. Effects of exposure to PCBs and related compounds on growth and activity in children. Neurotoxicol Teratol. 1990 Jul-Aug;12(4):319–326. doi: 10.1016/0892-0362(90)90050-m. [DOI] [PubMed] [Google Scholar]
  53. Jarriault S., Le Bail O., Hirsinger E., Pourquié O., Logeat F., Strong C. F., Brou C., Seidah N. G., Isra l A. Delta-1 activation of notch-1 signaling results in HES-1 transactivation. Mol Cell Biol. 1998 Dec;18(12):7423–7431. doi: 10.1128/mcb.18.12.7423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Kasza L., Collins W. T., Capen C. C., Garthoff L. H., Friedman L. Comparative toxicity of polychlorinated biphenyl and polybrominated biphenylin the rat thyroid gland: light and electron microscopic alterations after subacute dietary exposure. J Environ Pathol Toxicol. 1978 May-Jun;1(5):587–599. [PubMed] [Google Scholar]
  55. Klein R. Z., Haddow J. E., Faix J. D., Brown R. S., Hermos R. J., Pulkkinen A., Mitchell M. L. Prevalence of thyroid deficiency in pregnant women. Clin Endocrinol (Oxf) 1991 Jul;35(1):41–46. doi: 10.1111/j.1365-2265.1991.tb03494.x. [DOI] [PubMed] [Google Scholar]
  56. Klein R. Z., Mitchell M. L. Maternal hypothyroidism and child development. A review. Horm Res. 1999;52(2):55–59. doi: 10.1159/000023435. [DOI] [PubMed] [Google Scholar]
  57. Klett M. Epidemiology of congenital hypothyroidism. Exp Clin Endocrinol Diabetes. 1997;105 (Suppl 4):19–23. doi: 10.1055/s-0029-1211926. [DOI] [PubMed] [Google Scholar]
  58. Koibuchi N., Chin W. W. Thyroid hormone action and brain development. Trends Endocrinol Metab. 2000 May-Jun;11(4):123–128. doi: 10.1016/s1043-2760(00)00238-1. [DOI] [PubMed] [Google Scholar]
  59. Kolaja K. L., Klaassen C. D. Dose-response examination of UDP-glucuronosyltransferase inducers and their ability to increase both TGF-beta expression and thyroid follicular cell apoptosis. Toxicol Sci. 1998 Nov;46(1):31–37. doi: 10.1006/toxs.1998.2510. [DOI] [PubMed] [Google Scholar]
  60. Kooistra L., Laane C., Vulsma T., Schellekens J. M., van der Meere J. J., Kalverboer A. F. Motor and cognitive development in children with congenital hypothyroidism: a long-term evaluation of the effects of neonatal treatment. J Pediatr. 1994 Jun;124(6):903–909. doi: 10.1016/s0022-3476(05)83178-6. [DOI] [PubMed] [Google Scholar]
  61. Koopman-Esseboom C., Morse D. C., Weisglas-Kuperus N., Lutkeschipholt I. J., Van der Paauw C. G., Tuinstra L. G., Brouwer A., Sauer P. J. Effects of dioxins and polychlorinated biphenyls on thyroid hormone status of pregnant women and their infants. Pediatr Res. 1994 Oct;36(4):468–473. doi: 10.1203/00006450-199410000-00009. [DOI] [PubMed] [Google Scholar]
  62. Krude H., Biebermann H., Krohn H. P., Dralle H., Grüters A. Congenital hyperthyroidism. Exp Clin Endocrinol Diabetes. 1997;105 (Suppl 4):6–11. doi: 10.1055/s-0029-1211924. [DOI] [PubMed] [Google Scholar]
  63. Lans M. C., Spiertz C., Brouwer A., Koeman J. H. Different competition of thyroxine binding to transthyretin and thyroxine-binding globulin by hydroxy-PCBs, PCDDs and PCDFs. Eur J Pharmacol. 1994 Apr 4;270(2-3):129–136. doi: 10.1016/0926-6917(94)90054-x. [DOI] [PubMed] [Google Scholar]
  64. Lazar M. A. Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev. 1993 Apr;14(2):184–193. doi: 10.1210/edrv-14-2-184. [DOI] [PubMed] [Google Scholar]
  65. Leneman M., Buchanan L., Rovet J. Where and what visuospatial processing in adolescents with congenital hypothyroidism. J Int Neuropsychol Soc. 2001 Jul;7(5):556–562. doi: 10.1017/s1355617701755038. [DOI] [PubMed] [Google Scholar]
  66. Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
  67. Lowell S. Stem cells: You make me feel so glial. Curr Biol. 2000 Aug 24;10(16):R595–R597. doi: 10.1016/s0960-9822(00)00636-9. [DOI] [PubMed] [Google Scholar]
  68. Man E. B., Brown J. F., Serunian S. A. Maternal hypothyroxinemia: psychoneurological deficits of progeny. Ann Clin Lab Sci. 1991 Jul-Aug;21(4):227–239. [PubMed] [Google Scholar]
  69. Man E. B., Holden R. H., Jones W. S. Thyroid function in human pregnancy. VII. Development and retardation of 4-year-old progeny of euthyroid and of hypothyroxinemic women. Am J Obstet Gynecol. 1971 Jan 1;109(1):12–19. [PubMed] [Google Scholar]
  70. Man E. B., Jones W. S., Holden R. H., Mellits E. D. Thyroid function in human pregnancy. 8. Retardation of progeny aged 7 years; relationships to maternal age and maternal thyroid function. Am J Obstet Gynecol. 1971 Dec 1;111(7):905–916. [PubMed] [Google Scholar]
  71. Man E. B., Jones W. S. Thyroid function in human pregnancy. V. Incidence of maternal serum low butanol-extractable iodines and of normal gestational TBG and TBPA capacities; retardation of 8-month-old infants. Am J Obstet Gynecol. 1969 Jul 15;104(6):898–908. [PubMed] [Google Scholar]
  72. Man E. B., Reid W. A., Hellegers A. E., Jones W. S. Thyroid function in human pregnancy. II. Serum butanol-extractable iodine values of pregnant women 14 through 44 years. Am J Obstet Gynecol. 1969 Feb 1;103(3):328–337. [PubMed] [Google Scholar]
  73. Man E. B., Serunian S. A. Thyroid function in human pregnancy. IX. Development or retardation of 7-year-old progeny of hypothyroxinemic women. Am J Obstet Gynecol. 1976 Aug 1;125(7):949–949. [PubMed] [Google Scholar]
  74. Mangelsdorf D. J., Evans R. M. The RXR heterodimers and orphan receptors. Cell. 1995 Dec 15;83(6):841–850. doi: 10.1016/0092-8674(95)90200-7. [DOI] [PubMed] [Google Scholar]
  75. Marta C. B., Adamo A. M., Soto E. F., Pasquini J. M. Sustained neonatal hyperthyroidism in the rat affects myelination in the central nervous system. J Neurosci Res. 1998 Jul 15;53(2):251–259. doi: 10.1002/(SICI)1097-4547(19980715)53:2<251::AID-JNR14>3.0.CO;2-9. [DOI] [PubMed] [Google Scholar]
  76. McKinney J. D. Multifunctional receptor model for dioxin and related compound toxic action: possible thyroid hormone-responsive effector-linked site. Environ Health Perspect. 1989 Jul;82:323–336. doi: 10.1289/ehp.8982323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. McKinney J. D., Waller C. L. Molecular determinants of hormone mimicry: halogenated aromatic hydrocarbon environmental agents. J Toxicol Environ Health B Crit Rev. 1998 Jan-Mar;1(1):27–58. doi: 10.1080/10937409809524542. [DOI] [PubMed] [Google Scholar]
  78. McKinney J., Fannin R., Jordan S., Chae K., Rickenbacher U., Pedersen L. Polychlorinated biphenyls and related compound interactions with specific binding sites for thyroxine in rat liver nuclear extracts. J Med Chem. 1987 Jan;30(1):79–86. doi: 10.1021/jm00384a014. [DOI] [PubMed] [Google Scholar]
  79. McLachlan J. A. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev. 2001 Jun;22(3):319–341. doi: 10.1210/edrv.22.3.0432. [DOI] [PubMed] [Google Scholar]
  80. Miculan J., Turner S., Paes B. A. Congenital hypothyroidism: diagnosis and management. Neonatal Netw. 1993 Sep;12(6):25–38. [PubMed] [Google Scholar]
  81. Mirabella G., Feig D., Astzalos E., Perlman K., Rovet J. F. The effect of abnormal intrauterine thyroid hormone economies on infant cognitive abilities. J Pediatr Endocrinol Metab. 2000 Feb;13(2):191–194. doi: 10.1515/jpem.2000.13.2.191. [DOI] [PubMed] [Google Scholar]
  82. Morreale de Escobar G., Obregón M. J., Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J Clin Endocrinol Metab. 2000 Nov;85(11):3975–3987. doi: 10.1210/jcem.85.11.6961. [DOI] [PubMed] [Google Scholar]
  83. Morrison S. J., Perez S. E., Qiao Z., Verdi J. M., Hicks C., Weinmaster G., Anderson D. J. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell. 2000 May 26;101(5):499–510. doi: 10.1016/s0092-8674(00)80860-0. [DOI] [PubMed] [Google Scholar]
  84. Ness D. K., Schantz S. L., Moshtaghian J., Hansen L. G. Effects of perinatal exposure to specific PCB congeners on thyroid hormone concentrations and thyroid histology in the rat. Toxicol Lett. 1993 Jun;68(3):311–323. doi: 10.1016/0378-4274(93)90023-q. [DOI] [PubMed] [Google Scholar]
  85. Oppenheimer J. H., Schwartz H. L. Molecular basis of thyroid hormone-dependent brain development. Endocr Rev. 1997 Aug;18(4):462–475. doi: 10.1210/edrv.18.4.0309. [DOI] [PubMed] [Google Scholar]
  86. Oppenheimer J. H., Schwartz H. L., Strait K. A. Thyroid hormone action 1994: the plot thickens. Eur J Endocrinol. 1994 Jan;130(1):15–24. doi: 10.1530/eje.0.1300015. [DOI] [PubMed] [Google Scholar]
  87. Osius N., Karmaus W., Kruse H., Witten J. Exposure to polychlorinated biphenyls and levels of thyroid hormones in children. Environ Health Perspect. 1999 Oct;107(10):843–849. doi: 10.1289/ehp.99107843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Persky V., Turyk M., Anderson H. A., Hanrahan L. P., Falk C., Steenport D. N., Chatterton R., Jr, Freels S., Great Lakes Consortium The effects of PCB exposure and fish consumption on endogenous hormones. Environ Health Perspect. 2001 Dec;109(12):1275–1283. doi: 10.1289/ehp.011091275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Pop V. J., Kuijpens J. L., van Baar A. L., Verkerk G., van Son M. M., de Vijlder J. J., Vulsma T., Wiersinga W. M., Drexhage H. A., Vader H. L. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol (Oxf) 1999 Feb;50(2):149–155. doi: 10.1046/j.1365-2265.1999.00639.x. [DOI] [PubMed] [Google Scholar]
  90. Pop V. J., de Vries E., van Baar A. L., Waelkens J. J., de Rooy H. A., Horsten M., Donkers M. M., Komproe I. H., van Son M. M., Vader H. L. Maternal thyroid peroxidase antibodies during pregnancy: a marker of impaired child development? J Clin Endocrinol Metab. 1995 Dec;80(12):3561–3566. doi: 10.1210/jcem.80.12.8530599. [DOI] [PubMed] [Google Scholar]
  91. Porterfield S. P., Hendrich C. E. The role of thyroid hormones in prenatal and neonatal neurological development--current perspectives. Endocr Rev. 1993 Feb;14(1):94–106. doi: 10.1210/edrv-14-1-94. [DOI] [PubMed] [Google Scholar]
  92. Porterfield S. P., Hendry L. B. Impact of PCBs on thyroid hormone directed brain development. Toxicol Ind Health. 1998 Jan-Apr;14(1-2):103–120. doi: 10.1177/074823379801400109. [DOI] [PubMed] [Google Scholar]
  93. Rodriguez-Peña A., Ibarrola N., Iñiguez M. A., Muñoz A., Bernal J. Neonatal hypothyroidism affects the timely expression of myelin-associated glycoprotein in the rat brain. J Clin Invest. 1993 Mar;91(3):812–818. doi: 10.1172/JCI116301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Safe S. H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol. 1994;24(2):87–149. doi: 10.3109/10408449409049308. [DOI] [PubMed] [Google Scholar]
  95. Sala M., Sunyer J., Herrero C., To-Figueras J., Grimalt J. Association between serum concentrations of hexachlorobenzene and polychlorobiphenyls with thyroid hormone and liver enzymes in a sample of the general population. Occup Environ Med. 2001 Mar;58(3):172–177. doi: 10.1136/oem.58.3.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Schantz S. L. Developmental neurotoxicity of PCBs in humans: what do we know and where do we go from here? Neurotoxicol Teratol. 1996 May-Jun;18(3):217–276. doi: 10.1016/s0892-0362(96)90001-x. [DOI] [PubMed] [Google Scholar]
  97. Shain W., Bush B., Seegal R. Neurotoxicity of polychlorinated biphenyls: structure-activity relationship of individual congeners. Toxicol Appl Pharmacol. 1991 Oct;111(1):33–42. doi: 10.1016/0041-008x(91)90131-w. [DOI] [PubMed] [Google Scholar]
  98. Stewart P., Darvill T., Lonky E., Reihman J., Pagano J., Bush B. Assessment of prenatal exposure to PCBs from maternal consumption of Great Lakes fish: an analysis of PCB pattern and concentration. Environ Res. 1999 Feb;80(2 Pt 2):S87–S96. doi: 10.1006/enrs.1998.3905. [DOI] [PubMed] [Google Scholar]
  99. Stewart P., Reihman J., Lonky E., Darvill T., Pagano J. Prenatal PCB exposure and neonatal behavioral assessment scale (NBAS) performance. Neurotoxicol Teratol. 2000 Jan-Feb;22(1):21–29. doi: 10.1016/s0892-0362(99)00056-2. [DOI] [PubMed] [Google Scholar]
  100. Takahashi T., Nowakowski R. S., Caviness V. S., Jr BUdR as an S-phase marker for quantitative studies of cytokinetic behaviour in the murine cerebral ventricular zone. J Neurocytol. 1992 Mar;21(3):185–197. doi: 10.1007/BF01194977. [DOI] [PubMed] [Google Scholar]
  101. Takahashi T., Nowakowski R. S., Caviness V. S., Jr Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci. 1993 Feb;13(2):820–833. doi: 10.1523/JNEUROSCI.13-02-00820.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Takahashi T., Nowakowski R. S., Caviness V. S., Jr The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci. 1996 Oct 1;16(19):6183–6196. doi: 10.1523/JNEUROSCI.16-19-06183.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Thompson C. C., Potter G. B. Thyroid hormone action in neural development. Cereb Cortex. 2000 Oct;10(10):939–945. doi: 10.1093/cercor/10.10.939. [DOI] [PubMed] [Google Scholar]
  104. Tilson H. A., Kodavanti P. R., Mundy W. R., Bushnell P. J. Neurotoxicity of environmental chemicals and their mechanism of action. Toxicol Lett. 1998 Dec 28;102-103:631–635. doi: 10.1016/s0378-4274(98)00271-9. [DOI] [PubMed] [Google Scholar]
  105. Tilson H. A., Kodavanti P. R. Neurochemical effects of polychlorinated biphenyls: an overview and identification of research needs. Neurotoxicology. 1997;18(3):727–743. [PubMed] [Google Scholar]
  106. Timiras P. S., Nzekwe E. U. Thyroid hormones and nervous system development. Biol Neonate. 1989;55(6):376–385. doi: 10.1159/000242941. [DOI] [PubMed] [Google Scholar]
  107. Van Vliet G. Neonatal hypothyroidism: treatment and outcome. Thyroid. 1999 Jan;9(1):79–84. doi: 10.1089/thy.1999.9.79. [DOI] [PubMed] [Google Scholar]
  108. Vanderschueren-Lodeweyckx M., Debruyne F., Dooms L., Eggermont E., Eeckels R. Sensorineural hearing loss in sporadic congenital hypothyroidism. Arch Dis Child. 1983 Jun;58(6):419–422. doi: 10.1136/adc.58.6.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Visser T. J., Kaptein E., van Toor H., van Raaij J. A., van den Berg K. J., Joe C. T., van Engelen J. G., Brouwer A. Glucuronidation of thyroid hormone in rat liver: effects of in vivo treatment with microsomal enzyme inducers and in vitro assay conditions. Endocrinology. 1993 Nov;133(5):2177–2186. doi: 10.1210/endo.133.5.8404669. [DOI] [PubMed] [Google Scholar]
  110. Wagner R. L., Huber B. R., Shiau A. K., Kelly A., Cunha Lima S. T., Scanlan T. S., Apriletti J. W., Baxter J. D., West B. L., Fletterick R. J. Hormone selectivity in thyroid hormone receptors. Mol Endocrinol. 2001 Mar;15(3):398–410. doi: 10.1210/mend.15.3.0608. [DOI] [PubMed] [Google Scholar]
  111. Wang S., Barres B. A. Up a notch: instructing gliogenesis. Neuron. 2000 Aug;27(2):197–200. doi: 10.1016/s0896-6273(00)00028-3. [DOI] [PubMed] [Google Scholar]
  112. Zhang S. S., Carrillo A. J., Darling D. S. Expression of multiple thyroid hormone receptor mRNAs in human oocytes, cumulus cells, and granulosa cells. Mol Hum Reprod. 1997 Jul;3(7):555–562. doi: 10.1093/molehr/3.7.555. [DOI] [PubMed] [Google Scholar]
  113. Zoeller R. T., Dowling A. L., Vas A. A. Developmental exposure to polychlorinated biphenyls exerts thyroid hormone-like effects on the expression of RC3/neurogranin and myelin basic protein messenger ribonucleic acids in the developing rat brain. Endocrinology. 2000 Jan;141(1):181–189. doi: 10.1210/endo.141.1.7273. [DOI] [PubMed] [Google Scholar]
  114. van Beeren H. C., Bakker O., Wiersinga W. M. Desethylamiodarone is a competitive inhibitor of the binding of thyroid hormone to the thyroid hormone alpha 1-receptor protein. Mol Cell Endocrinol. 1995 Jul;112(1):15–19. doi: 10.1016/0303-7207(95)03578-u. [DOI] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Sciences

RESOURCES