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. 2002 Jun;110(Suppl 3):337–348. doi: 10.1289/ehp.02110s3337

A model of the development of the brain as a construct of the thyroid system.

Kembra L Howdeshell 1
PMCID: PMC1241181  PMID: 12060827

Abstract

Thyroid hormone is essential for normal brain development. However, little is known about the molecular and cellular mechanisms that mediate thyroid hormone action on the developing brain or the developmental events selectively affected. Consequently, although a large number of environmental chemicals interfere with the thyroid system, there are few neurodevelopmental end points to recruit for toxicological studies. Therefore, my goal here is to review what is known about the relative timing of normal brain construction and thyroid system development, with special focus on the period of in utero development in humans and the comparable developmental period in laboratory rats. These data are presented as a timeline to aid in the identification of thyroid-sensitive end points in brain development and to highlight important data gaps. I discuss the known influence of certain synthetic chemicals on the thyroid system and include a brief review of the effects of developmental exposure to chemicals on thyroid system function. The relationship between the thyroid hormone and retinoic acid systems, as well as the thyroid hormone sensitivity of the developing cochlea, is also discussed.

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Selected References

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  1. ALEXANDER N. M. Antithyroid action of 3-amino-1,2,4-triazole. J Biol Chem. 1959 Jan;234(1):148–150. [PubMed] [Google Scholar]
  2. ARNOTT D. G., DONIACH I. The effect of compounds allied to resorcinol upon the uptake of radioactive iodine (131I) by the thyroid of the rat. Biochem J. 1952 Feb;50(4):473–479. doi: 10.1042/bj0500473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allen-Rowlands C. F., Castracane V. D., Hamilton M. G., Seifter J. Effect of polybrominated biphenyls (PBB) on the pituitary--thyroid axis of the rat. Proc Soc Exp Biol Med. 1981 Apr;166(4):506–514. doi: 10.3181/00379727-166-41099. [DOI] [PubMed] [Google Scholar]
  4. Alliot F., Godin I., Pessac B. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res Dev Brain Res. 1999 Nov 18;117(2):145–152. doi: 10.1016/s0165-3806(99)00113-3. [DOI] [PubMed] [Google Scholar]
  5. Alvarez-Dolado M., Ruiz M., Del Río J. A., Alcántara S., Burgaya F., Sheldon M., Nakajima K., Bernal J., Howell B. W., Curran T. Thyroid hormone regulates reelin and dab1 expression during brain development. J Neurosci. 1999 Aug 15;19(16):6979–6993. doi: 10.1523/JNEUROSCI.19-16-06979.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Aubert M. L., Grumbach M. M., Kaplan S. L. The ontogenesis of human fetal hormones. IV. Somatostatin, luteinizing hormone releasing factor, and thyrotropin releasing factor in hypothalamus and cerebral cortex of human fetuses 10-22 weeks of age. J Clin Endocrinol Metab. 1977 Jun;44(6):1130–1141. doi: 10.1210/jcem-44-6-1130. [DOI] [PubMed] [Google Scholar]
  7. Balázs R., Kovács S., Teichgräber P., Cocks W. A., Eayrs J. T. Biochemical effects of thyroid deficiency on the developing brain. J Neurochem. 1968 Nov;15(11):1335–1349. doi: 10.1111/j.1471-4159.1968.tb05913.x. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Barter R. A., Klaassen C. D. Reduction of thyroid hormone levels and alteration of thyroid function by four representative UDP-glucuronosyltransferase inducers in rats. Toxicol Appl Pharmacol. 1994 Sep;128(1):9–17. doi: 10.1006/taap.1994.1174. [DOI] [PubMed] [Google Scholar]
  10. Barter R. A., Klaassen C. D. UDP-glucuronosyltransferase inducers reduce thyroid hormone levels in rats by an extrathyroidal mechanism. Toxicol Appl Pharmacol. 1992 Mar;113(1):36–42. doi: 10.1016/0041-008x(92)90006-e. [DOI] [PubMed] [Google Scholar]
  11. Bastomsky C. H. Effects of a polychlorinated biphenyl mixture (aroclor 1254) and DDT on biliary thyroxine excretion in rats. Endocrinology. 1974 Oct;95(4):1150–1155. doi: 10.1210/endo-95-4-1150. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Bastomsky C. H., Papapetrou P. D. The effect of methylcholanthrene on biliary thyroxine excretion in normal and Gunn rats. J Endocrinol. 1973 Feb;56(2):267–273. doi: 10.1677/joe.0.0560267. [DOI] [PubMed] [Google Scholar]
  14. Bayer S. A., Altman J., Russo R. J., Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology. 1993 Spring;14(1):83–144. [PubMed] [Google Scholar]
  15. Bellman S. C., Davies A., Fuggle P. W., Grant D. B., Smith I. Mild impairment of neuro-otological function in early treated congenital hypothyroidism. Arch Dis Child. 1996 Mar;74(3):215–218. doi: 10.1136/adc.74.3.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Bhattacharya T., Bhattacharya S., Ray A. K., Dey S. Influence of industrial pollutants on thyroid function in Channa punctatus (Bloch). Indian J Exp Biol. 1989 Jan;27(1):65–68. [PubMed] [Google Scholar]
  19. Blange I., Drvota V., Yen P. M., Sylven C. Species differences in cardiac thyroid hormone receptor isoforms protein abundance. Biol Pharm Bull. 1997 Nov;20(11):1123–1126. doi: 10.1248/bpb.20.1123. [DOI] [PubMed] [Google Scholar]
  20. Bradley D. J., Towle H. C., Young W. S., 3rd Alpha and beta thyroid hormone receptor (TR) gene expression during auditory neurogenesis: evidence for TR isoform-specific transcriptional regulation in vivo. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):439–443. doi: 10.1073/pnas.91.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Bradley D. J., Towle H. C., Young W. S., 3rd Spatial and temporal expression of alpha- and beta-thyroid hormone receptor mRNAs, including the beta 2-subtype, in the developing mammalian nervous system. J Neurosci. 1992 Jun;12(6):2288–2302. doi: 10.1523/JNEUROSCI.12-06-02288.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Breen J. J., Hickok N. J., Gurr J. A. The rat TSHbeta gene contains distinct response elements for regulation by retinoids and thyroid hormone. Mol Cell Endocrinol. 1997 Aug 8;131(2):137–146. doi: 10.1016/s0303-7207(97)00099-3. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Brouwer A., van den Berg K. J. Binding of a metabolite of 3,4,3',4'-tetrachlorobiphenyl to transthyretin reduces serum vitamin A transport by inhibiting the formation of the protein complex carrying both retinol and thyroxin. Toxicol Appl Pharmacol. 1986 Sep 30;85(3):301–312. doi: 10.1016/0041-008x(86)90337-6. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Brucker-Davis F., Skarulis M. C., Pikus A., Ishizawar D., Mastroianni M. A., Koby M., Weintraub B. D. Prevalence and mechanisms of hearing loss in patients with resistance to thyroid hormone. J Clin Endocrinol Metab. 1996 Aug;81(8):2768–2772. doi: 10.1210/jcem.81.8.8768826. [DOI] [PubMed] [Google Scholar]
  27. Burgunder J. M., Taylor T. Ontogeny of thyrotropin-releasing hormone gene expression in the rat diencephalon. Neuroendocrinology. 1989 Jun;49(6):631–640. doi: 10.1159/000125180. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Chao W. Y., Hsu C. C., Guo Y. L. Middle-ear disease in children exposed prenatally to polychlorinated biphenyls and polychlorinated dibenzofurans. Arch Environ Health. 1997 Jul-Aug;52(4):257–262. doi: 10.1080/00039899709602195. [DOI] [PubMed] [Google Scholar]
  30. Chaurasia S. S., Gupta P., Kar A., Maiti P. K. Lead induced thyroid dysfunction and lipid peroxidation in the fish Clarias batrachus with special reference to hepatic type I-5'-monodeiodinase activity. Bull Environ Contam Toxicol. 1996 Apr;56(4):649–654. doi: 10.1007/s001289900095. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Clancy B., Darlington R. B., Finlay B. L. Translating developmental time across mammalian species. Neuroscience. 2001;105(1):7–17. doi: 10.1016/s0306-4522(01)00171-3. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Crofton K. M., Ding D., Padich R., Taylor M., Henderson D. Hearing loss following exposure during development to polychlorinated biphenyls: a cochlear site of action. Hear Res. 2000 Jun;144(1-2):196–204. doi: 10.1016/s0378-5955(00)00062-9. [DOI] [PubMed] [Google Scholar]
  35. DANOWSKI T. S., SARVER M. E., MOSES C., BONESSI J. V. O-P'DDD THERAPY IN CUSHING'S SYNDROME AND IN OBESITY WITH CUSHINGOID CHANGES. Am J Med. 1964 Aug;37:235–250. doi: 10.1016/0002-9343(64)90008-7. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. De Sandro V., Chevrier M., Boddaert A., Melcion C., Cordier A., Richert L. Comparison of the effects of propylthiouracil, amiodarone, diphenylhydantoin, phenobarbital, and 3-methylcholanthrene on hepatic and renal T4 metabolism and thyroid gland function in rats. Toxicol Appl Pharmacol. 1991 Nov;111(2):263–278. doi: 10.1016/0041-008x(91)90030-i. [DOI] [PubMed] [Google Scholar]
  38. Debruyne F., Vanderschueren-Lodeweyckx M., Bastijns P. Hearing in congenital hypothyroidism. Audiology. 1983;22(4):404–409. doi: 10.3109/00206098309072800. [DOI] [PubMed] [Google Scholar]
  39. Dussault J. H., Labrie F. Development of the hypothalamic-pituitary-thyroid axis in the neonatal rat. Endocrinology. 1975 Nov;97(5):1321–1324. doi: 10.1210/endo-97-5-1321. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. EAYRS J. T. The cerebral cortex of normal and hypothyroid rats. Acta Anat (Basel) 1955;25(2-4):160–183. doi: 10.1159/000141068. [DOI] [PubMed] [Google Scholar]
  42. Ealey P. A., Henderson B., Loveridge N. A quantitative study of peroxidase activity in unfixed tissue sections of the guinea-pig thyroid gland. Histochem J. 1984 Feb;16(2):111–122. doi: 10.1007/BF01003543. [DOI] [PubMed] [Google Scholar]
  43. Eskandari S., Loo D. D., Dai G., Levy O., Wright E. M., Carrasco N. Thyroid Na+/I- symporter. Mechanism, stoichiometry, and specificity. J Biol Chem. 1997 Oct 24;272(43):27230–27238. doi: 10.1074/jbc.272.43.27230. [DOI] [PubMed] [Google Scholar]
  44. FLORSHEIM W. H., VELCOFF S. M. Some effects of 2,4-dichlorophenoxyacetic acid on thyroid function in the rat: effects on iodine accumulation. Endocrinology. 1962 Jul;71:1–6. doi: 10.1210/endo-71-1-1. [DOI] [PubMed] [Google Scholar]
  45. Falcone M., Miyamoto T., Fierro-Renoy F., Macchia E., DeGroot L. J. Evaluation of the ontogeny of thyroid hormone receptor isotypes in rat brain and liver using an immunohistochemical technique. Eur J Endocrinol. 1994 Jan;130(1):97–106. doi: 10.1530/eje.0.1300097. [DOI] [PubMed] [Google Scholar]
  46. Farwell A. P., Dubord-Tomasetti S. A. Thyroid hormone regulates the expression of laminin in the developing rat cerebellum. Endocrinology. 1999 Sep;140(9):4221–4227. doi: 10.1210/endo.140.9.7007. [DOI] [PubMed] [Google Scholar]
  47. Farwell A. P., Dubord-Tomasetti S. A. Thyroid hormone regulates the extracellular organization of laminin on astrocytes. Endocrinology. 1999 Nov;140(11):5014–5021. doi: 10.1210/endo.140.11.7114. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. Ferreiro B., Pastor R., Bernal J. T3 receptor occupancy and T3 levels in plasma and cytosol during rat brain development. Acta Endocrinol (Copenh) 1990 Jul;123(1):95–99. doi: 10.1530/acta.0.1230095. [DOI] [PubMed] [Google Scholar]
  50. 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]
  51. Fisher D. A. Fetal thyroid function: diagnosis and management of fetal thyroid disorders. Clin Obstet Gynecol. 1997 Mar;40(1):16–31. doi: 10.1097/00003081-199703000-00005. [DOI] [PubMed] [Google Scholar]
  52. Fisher D. A., Klein A. H. Thyroid development and disorders of thyroid function in the newborn. N Engl J Med. 1981 Mar 19;304(12):702–712. doi: 10.1056/NEJM198103193041205. [DOI] [PubMed] [Google Scholar]
  53. Forrest D. Deafness and goiter: molecular genetic considerations. J Clin Endocrinol Metab. 1996 Aug;81(8):2764–2767. doi: 10.1210/jcem.81.8.8768825. [DOI] [PubMed] [Google Scholar]
  54. Forrest D., Erway L. C., Ng L., Altschuler R., Curran T. Thyroid hormone receptor beta is essential for development of auditory function. Nat Genet. 1996 Jul;13(3):354–357. doi: 10.1038/ng0796-354. [DOI] [PubMed] [Google Scholar]
  55. Forrest D., Vennström B. Functions of thyroid hormone receptors in mice. Thyroid. 2000 Jan;10(1):41–52. doi: 10.1089/thy.2000.10.41. [DOI] [PubMed] [Google Scholar]
  56. Freeman S., Cherny L., Sohmer H. Thyroxine affects physiological and morphological development of the ear. Hear Res. 1996 Aug;97(1-2):19–29. [PubMed] [Google Scholar]
  57. Freudenthal R. I., Kerchner G., Persing R., Baron R. L. Dietary subacute toxicity of ethylene thiourea in the laboratory rat. J Environ Pathol Toxicol. 1978 Sep-Oct;1(1):147–161. [PubMed] [Google Scholar]
  58. GOLDBERG R. C., WOLFF J., GREEP R. O. The mechanism of depression of plasma protein bound iodine by 2,4 dinitrophenol. Endocrinology. 1955 May;56(5):560–566. doi: 10.1210/endo-56-5-560. [DOI] [PubMed] [Google Scholar]
  59. Ghinea E., Dumitriu L., Stefanovici G., Pop A., Oprescu M., Ciocîrdia C. Action of some pesticides on T4 to T3 conversion in cultured kidney and liver cells in the presence or absence of cysteine. Endocrinologie. 1986 Jul-Sep;24(3):157–166. [PubMed] [Google Scholar]
  60. Ghosh N., Bhattacharya S. Thyrotoxicity of the chlorides of cadmium and mercury in rabbit. Biomed Environ Sci. 1992 Sep;5(3):236–240. [PubMed] [Google Scholar]
  61. 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]
  62. 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]
  63. 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]
  64. 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]
  65. Goldman M., Blackburn P. The effect of mercuric chloride on thyroid function in the rat. Toxicol Appl Pharmacol. 1979 Mar 30;48(1 Pt 1):49–55. doi: 10.1016/s0041-008x(79)80007-1. [DOI] [PubMed] [Google Scholar]
  66. Goldman M., Dillon R. D. Interaction of selenium and lead on several aspects of thyroid function in Pekin ducklings. Res Commun Chem Pathol Pharmacol. 1982 Sep;37(3):487–490. [PubMed] [Google Scholar]
  67. Goldstein J. A., Taurog A. Enhanced biliary excretion of thyroxine glucuronide in rats pretreated with benzpyrene. Biochem Pharmacol. 1968 Jun;17(6):1049–1065. doi: 10.1016/0006-2952(68)90363-8. [DOI] [PubMed] [Google Scholar]
  68. Gould E, Tanapat P, Hastings NB, Shors TJ. Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci. 1999 May;3(5):186–192. doi: 10.1016/s1364-6613(99)01310-8. [DOI] [PubMed] [Google Scholar]
  69. Gravel C., Hawkes R. Maturation of the corpus callosum of the rat: I. Influence of thyroid hormones on the topography of callosal projections. J Comp Neurol. 1990 Jan 1;291(1):128–146. doi: 10.1002/cne.902910109. [DOI] [PubMed] [Google Scholar]
  70. Gressens P., Gofflot F., Van Maele-Fabry G., Misson J. P., Gadisseux J. F., Evrard P., Picard J. J. Early neurogenesis and teratogenesis in whole mouse embryo cultures. Histochemical, immunocytological and ultrastructural study of the premigratory neuronal-glial units in normal mouse embryo and in mouse embryos influenced by cocaine and retinoic acid. J Neuropathol Exp Neurol. 1992 Mar;51(2):206–219. doi: 10.1097/00005072-199203000-00010. [DOI] [PubMed] [Google Scholar]
  71. 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]
  72. Hallgren S., Sinjari T., Håkansson H., Darnerud P. O. Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroid hormone and vitamin A levels in rats and mice. Arch Toxicol. 2001 Jun;75(4):200–208. doi: 10.1007/s002040000208. [DOI] [PubMed] [Google Scholar]
  73. Herr D. W., Goldey E. S., Crofton K. M. Developmental exposure to Aroclor 1254 produces low-frequency alterations in adult rat brainstem auditory evoked responses. Fundam Appl Toxicol. 1996 Sep;33(1):120–128. doi: 10.1006/faat.1996.0149. [DOI] [PubMed] [Google Scholar]
  74. Herschkowitz N., Kagan J., Zilles K. Neurobiological bases of behavioral development in the first year. Neuropediatrics. 1997 Dec;28(6):296–306. doi: 10.1055/s-2007-973720. [DOI] [PubMed] [Google Scholar]
  75. Hurley P. M. Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents. Environ Health Perspect. 1998 Aug;106(8):437–445. doi: 10.1289/ehp.98106437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Hébert R., Langlois J. M., Dussault J. H. Permanent defects in rat peripheral auditory function following perinatal hypothyroidism: determination of a critical period. Brain Res. 1985 Dec;355(2):161–170. doi: 10.1016/0165-3806(85)90037-9. [DOI] [PubMed] [Google Scholar]
  77. Ibarrola N., Rodríguez-Peña A. Hypothyroidism coordinately and transiently affects myelin protein gene expression in most rat brain regions during postnatal development. Brain Res. 1997 Mar 28;752(1-2):285–293. doi: 10.1016/s0006-8993(96)01480-1. [DOI] [PubMed] [Google Scholar]
  78. 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]
  79. Kackar R., Srivastava M. K., Raizada R. B. Studies on rat thyroid after oral administration of mancozeb: morphological and biochemical evaluations. J Appl Toxicol. 1997 Nov-Dec;17(6):369–375. doi: 10.1002/(sici)1099-1263(199711/12)17:6<369::aid-jat449>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  80. Karabélyos C., Szeberényi S., Csaba G. Effect of allylestrenol exposure during pregnancy on the activity of microsomal enzyme system (PSMO) of rat in the F1 and F2 generations. Acta Physiol Hung. 1994;82(1):15–22. [PubMed] [Google Scholar]
  81. Kawada J., Nishida M., Yoshimura Y., Mitani K. Effects of organic and inorganic mercurials on thyroidal functions. J Pharmacobiodyn. 1980 Mar;3(3):149–159. doi: 10.1248/bpb1978.3.149. [DOI] [PubMed] [Google Scholar]
  82. Kilby M. D., Gittoes N., McCabe C., Verhaeg J., Franklyn J. A. Expression of thyroid receptor isoforms in the human fetal central nervous system and the effects of intrauterine growth restriction. Clin Endocrinol (Oxf) 2000 Oct;53(4):469–477. doi: 10.1046/j.1365-2265.2000.01074.x. [DOI] [PubMed] [Google Scholar]
  83. Klein R. Z., Sargent J. D., Larsen P. R., Waisbren S. E., Haddow J. E., Mitchell M. L. Relation of severity of maternal hypothyroidism to cognitive development of offspring. J Med Screen. 2001;8(1):18–20. doi: 10.1136/jms.8.1.18. [DOI] [PubMed] [Google Scholar]
  84. Knipper M., Bandtlow C., Gestwa L., Köpschall I., Rohbock K., Wiechers B., Zenner H. P., Zimmermann U. Thyroid hormone affects Schwann cell and oligodendrocyte gene expression at the glial transition zone of the VIIIth nerve prior to cochlea function. Development. 1998 Sep;125(18):3709–3718. doi: 10.1242/dev.125.18.3709. [DOI] [PubMed] [Google Scholar]
  85. Knipper M., Zinn C., Maier H., Praetorius M., Rohbock K., Köpschall I., Zimmermann U. Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J Neurophysiol. 2000 May;83(5):3101–3112. doi: 10.1152/jn.2000.83.5.3101. [DOI] [PubMed] [Google Scholar]
  86. Koibuchi N., Chin W. W. ROR alpha gene expression in the perinatal rat cerebellum: ontogeny and thyroid hormone regulation. Endocrinology. 1998 May;139(5):2335–2341. doi: 10.1210/endo.139.5.6013. [DOI] [PubMed] [Google Scholar]
  87. 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]
  88. Kornack D. R., Rakic P. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4752–4757. doi: 10.1073/pnas.081074998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Kuzan F. B., Prahlad K. V. The effects of 1, 2, 3, 4, 10, 10-hexachloro-1, 4, 4a, 5, 8, 8a-hexahydroxy endo, exo-5, 8-dimethionaphthalene (aldrin) and sodium ethylenebisdithiocarbomate (nabam) on the chick. Poult Sci. 1975 Jul;54(4):1054–1064. doi: 10.3382/ps.0541054. [DOI] [PubMed] [Google Scholar]
  90. Köhrle J. Thyroid hormone metabolism and action in the brain and pituitary. Acta Med Austriaca. 2000;27(1):1–7. doi: 10.1046/j.1563-2571.2000.200101.x. [DOI] [PubMed] [Google Scholar]
  91. Lauder J. M., Bloom F. E. Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. II. Synaptogenesis. J Comp Neurol. 1975 Oct 1;163(3):251–264. doi: 10.1002/cne.901630302. [DOI] [PubMed] [Google Scholar]
  92. 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]
  93. Lecavalier P., Chu I., Yagminas A., Villeneuve D. C., Poon R., Feeley M., Håkansson H., Ahlborg U. G., Valli V. E., Bergman A. Subchronic toxicity of 2,2',3,3',4,4'-hexachlorobiphenyl in rats. J Toxicol Environ Health. 1997 Jun 27;51(3):265–277. doi: 10.1080/00984109708984026. [DOI] [PubMed] [Google Scholar]
  94. 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]
  95. Leonard J. L., Farwell A. P., Yen P. M., Chin W. W., Stula M. Differential expression of thyroid hormone receptor isoforms in neurons and astroglial cells. Endocrinology. 1994 Aug;135(2):548–555. doi: 10.1210/endo.135.2.8033801. [DOI] [PubMed] [Google Scholar]
  96. Li D., Henley C. M., O'Malley B. W., Jr Distortion product otoacoustic emissions and outer hair cell defects in the hyt/hyt mutant mouse. Hear Res. 1999 Dec;138(1-2):65–72. doi: 10.1016/s0378-5955(99)00150-1. [DOI] [PubMed] [Google Scholar]
  97. Lima F. R., Gervais A., Colin C., Izembart M., Neto V. M., Mallat M. Regulation of microglial development: a novel role for thyroid hormone. J Neurosci. 2001 Mar 15;21(6):2028–2038. doi: 10.1523/JNEUROSCI.21-06-02028.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Lybeck H., Leppäluoto J., Aito H. The influence of an anticholinesterase, methylparathion, on the radioiodine uptake of the rat thyroid in vivo and in vitro. Ann Med Exp Biol Fenn. 1967;45(1):76–79. [PubMed] [Google Scholar]
  99. Maiti P. K., Kar A. Dimethoate inhibits extrathyroidal 5'-monodeiodination of thyroxine to 3,3',5-triiodothyronine in mice: the possible involvement of the lipid peroxidative process. Toxicol Lett. 1997 Mar 14;91(1):1–6. doi: 10.1016/s0378-4274(96)03865-9. [DOI] [PubMed] [Google Scholar]
  100. Maiti P. K., Kar A. Dual role of testosterone in fenvalerate-treated mice with respect to thyroid function and lipid peroxidation. J Appl Toxicol. 1997 Mar-Apr;17(2):127–131. doi: 10.1002/(sici)1099-1263(199703)17:2<127::aid-jat418>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  101. Maiti P. K., Kar A., Gupta P., Chaurasia S. S. Loss of membrane integrity and inhibition of type-I iodothyronine 5'-monodeiodinase activity by fenvalerate in female mouse. Biochem Biophys Res Commun. 1995 Sep 25;214(3):905–909. doi: 10.1006/bbrc.1995.2372. [DOI] [PubMed] [Google Scholar]
  102. 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]
  103. Marinovich M., Guizzetti M., Ghilardi F., Viviani B., Corsini E., Galli C. L. Thyroid peroxidase as toxicity target for dithiocarbamates. Arch Toxicol. 1997;71(8):508–512. doi: 10.1007/s002040050420. [DOI] [PubMed] [Google Scholar]
  104. Marshall J. S., Tompkins L. S. Effect of o,p'-DDD and similar compounds on thyroxine binding globulin. J Clin Endocrinol Metab. 1968 Mar;28(3):386–392. doi: 10.1210/jcem-28-3-386. [DOI] [PubMed] [Google Scholar]
  105. Martínez-Galán J. R., Pedraza P., Santacana M., Escobar del Ray F., Morreale de Escobar G., Ruiz-Marcos A. Early effects of iodine deficiency on radial glial cells of the hippocampus of the rat fetus. A model of neurological cretinism. J Clin Invest. 1997 Jun 1;99(11):2701–2709. doi: 10.1172/JCI119459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Mayberry W. E. Antithyroid effects of 3-amino-1,2,4-triazole. Proc Soc Exp Biol Med. 1968 Nov;129(2):551–556. doi: 10.3181/00379727-129-33367. [DOI] [PubMed] [Google Scholar]
  107. McCall M. A., Gregg R. G., Behringer R. R., Brenner M., Delaney C. L., Galbreath E. J., Zhang C. L., Pearce R. A., Chiu S. Y., Messing A. Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiology. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6361–6366. doi: 10.1073/pnas.93.13.6361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. McClain R. M., Levin A. A., Posch R., Downing J. C. The effect of phenobarbital on the metabolism and excretion of thyroxine in rats. Toxicol Appl Pharmacol. 1989 Jun 15;99(2):216–228. doi: 10.1016/0041-008x(89)90004-5. [DOI] [PubMed] [Google Scholar]
  109. 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]
  110. Mission J. P., Takahashi T., Caviness V. S., Jr Ontogeny of radial and other astroglial cells in murine cerebral cortex. Glia. 1991;4(2):138–148. doi: 10.1002/glia.440040205. [DOI] [PubMed] [Google Scholar]
  111. Morreale de Escobar G., Pastor R., Obregon M. J., Escobar del Rey F. Effects of maternal hypothyroidism on the weight and thyroid hormone content of rat embryonic tissues, before and after onset of fetal thyroid function. Endocrinology. 1985 Nov;117(5):1890–1900. doi: 10.1210/endo-117-5-1890. [DOI] [PubMed] [Google Scholar]
  112. Morse D. C., Wehler E. K., Wesseling W., Koeman J. H., Brouwer A. Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (Aroclor 1254). Toxicol Appl Pharmacol. 1996 Feb;136(2):269–279. doi: 10.1006/taap.1996.0034. [DOI] [PubMed] [Google Scholar]
  113. Muller Y., Rocchi E., Lazaro J. B., Clos J. Thyroid hormone promotes BCL-2 expression and prevents apoptosis of early differentiating cerebellar granule neurons. Int J Dev Neurosci. 1995 Dec;13(8):871–885. doi: 10.1016/0736-5748(95)00057-7. [DOI] [PubMed] [Google Scholar]
  114. Neveu I., Arenas E. Neurotrophins promote the survival and development of neurons in the cerebellum of hypothyroid rats in vivo. J Cell Biol. 1996 May;133(3):631–646. doi: 10.1083/jcb.133.3.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Ng L., Hurley J. B., Dierks B., Srinivas M., Saltó C., Vennström B., Reh T. A., Forrest D. A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet. 2001 Jan;27(1):94–98. doi: 10.1038/83829. [DOI] [PubMed] [Google Scholar]
  116. Nicholson J. L., Altman J. The effects of early hypo- and hyperthyroidism on the development of rat cerebellar cortex. I. Cell proliferation and differentiation. Brain Res. 1972 Sep 15;44(1):13–23. doi: 10.1016/0006-8993(72)90362-9. [DOI] [PubMed] [Google Scholar]
  117. Nicholson J. L., Altman J. The effects of early hypo- and hyperthyroidism on the development of the rat cerebellar cortex. II. Synaptogenesis in the molecular layer. Brain Res. 1972 Sep 15;44(1):25–36. doi: 10.1016/0006-8993(72)90363-0. [DOI] [PubMed] [Google Scholar]
  118. Obregon M. J., Mallol J., Pastor R., Morreale de Escobar G., Escobar del Rey F. L-thyroxine and 3,5,3'-triiodo-L-thyronine in rat embryos before onset of fetal thyroid function. Endocrinology. 1984 Jan;114(1):305–307. doi: 10.1210/endo-114-1-305. [DOI] [PubMed] [Google Scholar]
  119. Oliver C., Eskay R. L., Porter J. C. Developmental changes in brain TRH and in plasma and pituitary TSH and prolactin levels in the rat. Biol Neonate. 1980;37(3-4):145–152. doi: 10.1159/000241266. [DOI] [PubMed] [Google Scholar]
  120. 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]
  121. Oppenheimer J. H., Schwartz H. L. Stereospecific transport of triiodothyronine from plasma to cytosol and from cytosol to nucleus in rat liver, kidney, brain, and heart. J Clin Invest. 1985 Jan;75(1):147–154. doi: 10.1172/JCI111667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Perez-Castillo A., Bernal J., Ferreiro B., Pans T. The early ontogenesis of thyroid hormone receptor in the rat fetus. Endocrinology. 1985 Dec;117(6):2457–2461. doi: 10.1210/endo-117-6-2457. [DOI] [PubMed] [Google Scholar]
  123. 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]
  124. 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]
  125. Porterfield S. P. Vulnerability of the developing brain to thyroid abnormalities: environmental insults to the thyroid system. Environ Health Perspect. 1994 Jun;102 (Suppl 2):125–130. doi: 10.1289/ehp.94102125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Rakic P. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 1971 Oct 29;33(2):471–476. doi: 10.1016/0006-8993(71)90119-3. [DOI] [PubMed] [Google Scholar]
  127. Ram R. N., Joy K. P., Sathyanesan A. G. Cythion-induced histophysiological changes in thyroid and thyrotrophs of the teleost fish, Channa punctatus (Bloch). Ecotoxicol Environ Saf. 1989 Jun;17(3):272–278. doi: 10.1016/0147-6513(89)90047-x. [DOI] [PubMed] [Google Scholar]
  128. Rami A., Rabié A. Delayed synaptogenesis in the dentate gyrus of the thyroid-deficient developing rat. Dev Neurosci. 1990;12(6):398–405. doi: 10.1159/000111867. [DOI] [PubMed] [Google Scholar]
  129. Rice D., Barone S., Jr Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000 Jun;108 (Suppl 3):511–533. doi: 10.1289/ehp.00108s3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Ringer R. K., Polin D. The biological effects of polybrominated biphenyls in avian species. Fed Proc. 1977 May;36(6):1894–1898. [PubMed] [Google Scholar]
  131. Rodríguez-García M., Jolín T., Santos A., Pérez-Castillo A. Effect of perinatal hypothyroidism on the developmental regulation of rat pituitary growth hormone and thyrotropin genes. Endocrinology. 1995 Oct;136(10):4339–4350. doi: 10.1210/endo.136.10.7664653. [DOI] [PubMed] [Google Scholar]
  132. Rodríguez-Peña A. Oligodendrocyte development and thyroid hormone. J Neurobiol. 1999 Sep 15;40(4):497–512. doi: 10.1002/(sici)1097-4695(19990915)40:4<497::aid-neu7>3.0.co;2-#. [DOI] [PubMed] [Google Scholar]
  133. Roti E. Regulation of thyroid-stimulating hormone (TSH) secretion in the fetus and neonate. J Endocrinol Invest. 1988 Feb;11(2):145–158. doi: 10.1007/BF03350124. [DOI] [PubMed] [Google Scholar]
  134. Rozman K., Gorski J. R., Rozman P., Parkinson A. Reduced serum thyroid hormone levels in hexachlorobenzene-induced porphyria. Toxicol Lett. 1986 Jan;30(1):71–78. doi: 10.1016/0378-4274(86)90181-5. [DOI] [PubMed] [Google Scholar]
  135. Ruiz-Marcos A., Sanchez-Toscano F., Escobar del Rey F., Morreale de Escobar G. Severe hypothyroidism and the maturation of the rat cerebral cortex. Brain Res. 1979 Feb 23;162(2):315–329. doi: 10.1016/0006-8993(79)90292-0. [DOI] [PubMed] [Google Scholar]
  136. Rüsch A., Erway L. C., Oliver D., Vennström B., Forrest D. Thyroid hormone receptor beta-dependent expression of a potassium conductance in inner hair cells at the onset of hearing. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15758–15762. doi: 10.1073/pnas.95.26.15758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Schuur A. G., Boekhorst F. M., Brouwer A., Visser T. J. Extrathyroidal effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on thyroid hormone turnover in male Sprague-Dawley rats. Endocrinology. 1997 Sep;138(9):3727–3734. doi: 10.1210/endo.138.9.5386. [DOI] [PubMed] [Google Scholar]
  138. Schwab J. M., Schluesener H. J., Seid K., Meyermann R. IL-16 is differentially expressed in the developing human fetal brain by microglial cells in zones of neuropoesis. Int J Dev Neurosci. 2001 Feb;19(1):93–100. doi: 10.1016/s0736-5748(00)00063-0. [DOI] [PubMed] [Google Scholar]
  139. Seo B. W., Li M. H., Hansen L. G., Moore R. W., Peterson R. E., Schantz S. L. 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. 1995 Aug;78(3):253–262. doi: 10.1016/0378-4274(95)03329-j. [DOI] [PubMed] [Google Scholar]
  140. Shambaugh G. E., 3rd, Kubek M., Wilber J. F. Characterization of rat placental TRH-like material and the ontogeny of placental and fetal brain TRH. Placenta. 1983 Oct-Dec;4(4):329–337. doi: 10.1016/s0143-4004(83)80036-8. [DOI] [PubMed] [Google Scholar]
  141. Shepard T. H. Onset of function in the human fetal thyroid: biochemical and radioautographic studies from organ culture. J Clin Endocrinol Metab. 1967 Jul;27(7):945–958. doi: 10.1210/jcem-27-7-945. [DOI] [PubMed] [Google Scholar]
  142. Sidman R. L., Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973 Nov 9;62(1):1–35. doi: 10.1016/0006-8993(73)90617-3. [DOI] [PubMed] [Google Scholar]
  143. Singh H., Singh T. P. Thyroid activity and TSH potency of the pituitary gland and blood serum in response to cythion and hexadrin treatment in the freshwater catfish, Hetteropneustes fossilis (Bloch). Environ Res. 1980 Jun;22(1):184–189. doi: 10.1016/0013-9351(80)90130-9. [DOI] [PubMed] [Google Scholar]
  144. Sinha N., Lal B., Singh T. P. Effect of endosulfan on thyroid physiology in the freshwater catfish, Clarias batrachus. Toxicology. 1991 Apr 8;67(2):187–197. doi: 10.1016/0300-483x(91)90142-n. [DOI] [PubMed] [Google Scholar]
  145. Smith A. G., Dinsdale D., Cabral J. R., Wright A. L. Goitre and wasting induced in hamsters by hexachlorobenzene. Arch Toxicol. 1987 Jul;60(5):343–349. doi: 10.1007/BF00295753. [DOI] [PubMed] [Google Scholar]
  146. Soriguer F., Millón M. C., Muñoz R., Mancha I., López Siguero J. P., Martinez Aedo M. J., Gómez-Huelga R., Garriga M. J., Rojo-Martinez G., Esteva I. The auditory threshold in a school-age population is related to iodine intake and thyroid function. Thyroid. 2000 Nov;10(11):991–999. doi: 10.1089/thy.2000.10.991. [DOI] [PubMed] [Google Scholar]
  147. Spear P. A., Higueret P., Garcin H. Increased thyroxine turnover after 3,3',4,4',5,5'-hexabromobiphenyl injection and lack of effect on peripheral triiodothyronine production. Can J Physiol Pharmacol. 1990 Aug;68(8):1079–1084. doi: 10.1139/y90-162. [DOI] [PubMed] [Google Scholar]
  148. Steinhoff D., Weber H., Mohr U., Boehme K. Evaluation of amitrole (aminotriazole) for potential carcinogenicity in orally dosed rats, mice, and golden hamsters. Toxicol Appl Pharmacol. 1983 Jun 30;69(2):161–169. doi: 10.1016/0041-008x(83)90296-x. [DOI] [PubMed] [Google Scholar]
  149. Strait K. A., Schwartz H. L., Seybold V. S., Ling N. C., Oppenheimer J. H. Immunofluorescence localization of thyroid hormone receptor protein beta 1 and variant alpha 2 in selected tissues: cerebellar Purkinje cells as a model for beta 1 receptor-mediated developmental effects of thyroid hormone in brain. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3887–3891. doi: 10.1073/pnas.88.9.3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Strbak V., Greer M. A. Acute effects of hypothalamic ablation on plasma thyrotropin and prolactin concentrations in the suckling rat: evidence that early postnatal pituitary-thyroid regulation is independent of hypothalamic control. Endocrinology. 1979 Aug;105(2):488–489. doi: 10.1210/endo-105-2-488. [DOI] [PubMed] [Google Scholar]
  151. Strum J. M., Karnovsky M. J. Aminotriazole goiter. Fine structure and localization of thyroid peroxidase activity. Lab Invest. 1971 Jan;24(1):1–12. [PubMed] [Google Scholar]
  152. Sun Z. Q., Ojamaa K., Nakamura T. Y., Artman M., Klein I., Coetzee W. A. Thyroid hormone increases pacemaker activity in rat neonatal atrial myocytes. J Mol Cell Cardiol. 2001 Apr;33(4):811–824. doi: 10.1006/jmcc.2001.1353. [DOI] [PubMed] [Google Scholar]
  153. Sutor B., Luhmann H. J. Development of excitatory and inhibitory postsynaptic potentials in the rat neocortex. Perspect Dev Neurobiol. 1995;2(4):409–419. [PubMed] [Google Scholar]
  154. Swann J. W., Smith K. L., Brady R. J. Neural networks and synaptic transmission in immature hippocampus. Adv Exp Med Biol. 1990;268:161–171. doi: 10.1007/978-1-4684-5769-8_19. [DOI] [PubMed] [Google Scholar]
  155. Thliveris J. A., Currie R. W. Observations on the hypothalamo-hypophyseal portal vasculature in the developing human fetus. Am J Anat. 1980 Apr;157(4):441–444. doi: 10.1002/aja.1001570411. [DOI] [PubMed] [Google Scholar]
  156. 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]
  157. Thompson C. C. Thyroid hormone-responsive genes in developing cerebellum include a novel synaptotagmin and a hairless homolog. J Neurosci. 1996 Dec 15;16(24):7832–7840. doi: 10.1523/JNEUROSCI.16-24-07832.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  158. Thorpe-Beeston J. G., Nicolaides K. H., McGregor A. M. Fetal thyroid function. Thyroid. 1992 Fall;2(3):207–217. doi: 10.1089/thy.1992.2.207. [DOI] [PubMed] [Google Scholar]
  159. Uziel A. Periods of sensitivity to thyroid hormone during the development of the organ of Corti. Acta Otolaryngol Suppl. 1986;429:23–27. doi: 10.3109/00016488609122726. [DOI] [PubMed] [Google Scholar]
  160. VAN WYK J. J., ARNOLD M. B., WYNN J., PEPPER F. The effects of a soybean product on thyroid function in humans. Pediatrics. 1959 Nov;24:752–760. [PubMed] [Google Scholar]
  161. Van Birgelen A. P., 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., Brouwer A. Subchronic effects of 2,3,7,8-TCDD or PCBs on thyroid hormone metabolism: use in risk assessment. Eur J Pharmacol. 1995 May 26;293(1):77–85. doi: 10.1016/0926-6917(95)90021-7. [DOI] [PubMed] [Google Scholar]
  162. Van den Berg K. J., van Raaij J. A., Bragt P. C., Notten W. R. Interactions of halogenated industrial chemicals with transthyretin and effects on thyroid hormone levels in vivo. Arch Toxicol. 1991;65(1):15–19. doi: 10.1007/BF01973497. [DOI] [PubMed] [Google Scholar]
  163. Verity A. N., Campagnoni A. T. Regional expression of myelin protein genes in the developing mouse brain: in situ hybridization studies. J Neurosci Res. 1988 Oct-Dec;21(2-4):238–248. doi: 10.1002/jnr.490210216. [DOI] [PubMed] [Google Scholar]
  164. Versloot P. M., Schröder-van der Elst J. P., van der Heide D., Boogerd L. Effects of marginal iodine deficiency on thyroid hormone production, distribution and transport in nonpregnant and near-term pregnant rats. Eur J Endocrinol. 1998 Jun;138(6):713–718. doi: 10.1530/eje.0.1380713. [DOI] [PubMed] [Google Scholar]
  165. 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]
  166. Vulsma T., Gons M. H., de Vijlder J. J. Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. N Engl J Med. 1989 Jul 6;321(1):13–16. doi: 10.1056/NEJM198907063210103. [DOI] [PubMed] [Google Scholar]
  167. Winters A. J., Eskay R. L., Porter J. C. Concentration and distribution of TRH and LRH in the human fetal brain. J Clin Endocrinol Metab. 1974 Nov;39(5):960–963. doi: 10.1210/jcem-39-5-960. [DOI] [PubMed] [Google Scholar]
  168. Wolff J. Perchlorate and the thyroid gland. Pharmacol Rev. 1998 Mar;50(1):89–105. [PubMed] [Google Scholar]
  169. Woods R. J., Sinha A. K., Ekins R. P. Uptake and metabolism of thyroid hormones by the rat foetus in early pregnancy. Clin Sci (Lond) 1984 Sep;67(3):359–363. doi: 10.1042/cs0670359. [DOI] [PubMed] [Google Scholar]
  170. Xiao Q., Nikodem V. M. Apoptosis in the developing cerebellum of the thyroid hormone deficient rat. Front Biosci. 1998 Sep 15;3:A52–A57. doi: 10.2741/a252. [DOI] [PubMed] [Google Scholar]
  171. Yadav A. K., Singh T. P. Pesticide-induced impairment of thyroid physiology in the freshwater catfish, Heteropneustes fossilis. Environ Pollut. 1987;43(1):29–38. doi: 10.1016/0269-7491(87)90165-5. [DOI] [PubMed] [Google Scholar]
  172. Yoshida K., Sugihira N., Suzuki M., Sakurada T., Saito S., Yoshinaga K., Saito H. Effect of cadmium on T4 outer ring monodeiodination by rat liver. Environ Res. 1987 Apr;42(2):400–405. doi: 10.1016/s0013-9351(87)80206-2. [DOI] [PubMed] [Google Scholar]
  173. 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]
  174. Zoeller R. T., Crofton K. M. Thyroid hormone action in fetal brain development and potential for disruption by environmental chemicals. Neurotoxicology. 2000 Dec;21(6):935–945. [PubMed] [Google Scholar]
  175. den Besten C., Vet J. J., Besselink H. T., Kiel G. S., van Berkel B. J., Beems R., van Bladeren P. J. The liver, kidney, and thyroid toxicity of chlorinated benzenes. Toxicol Appl Pharmacol. 1991 Oct;111(1):69–81. doi: 10.1016/0041-008x(91)90135-2. [DOI] [PubMed] [Google Scholar]
  176. van Raaij J. A., Frijters C. M., van den Berg K. J. Hexachlorobenzene-induced hypothyroidism. Involvement of different mechanisms by parent compound and metabolite. Biochem Pharmacol. 1993 Oct 19;46(8):1385–1391. doi: 10.1016/0006-2952(93)90103-4. [DOI] [PubMed] [Google Scholar]
  177. van Raaij J. A., Kaptein E., Visser T. J., van den Berg K. J. Increased glucuronidation of thyroid hormone in hexachlorobenzene-treated rats. Biochem Pharmacol. 1993 Feb 9;45(3):627–631. doi: 10.1016/0006-2952(93)90136-k. [DOI] [PubMed] [Google Scholar]
  178. van den Berg K. J. Interaction of chlorinated phenols with thyroxine binding sites of human transthyretin, albumin and thyroid binding globulin. Chem Biol Interact. 1990;76(1):63–75. doi: 10.1016/0009-2797(90)90034-k. [DOI] [PubMed] [Google Scholar]

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