Perspectives in the Study of Thyroid Hormone Action on Brain Development and Function

Thyroid

Volumn 13, Issue 11, 2003, Pages 1005-1012

  Bernal, Juan ^a,b   Guadaño Ferraz, Ana ^a   Morte, Beatriz ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LIOTHYRONINE; THYROID HORMONE; THYROID HORMONE RECEPTOR;

BEHAVIOR; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN LEVEL; BRAIN MATURATION; BRAIN REGION; CELL DIFFERENTIATION; CORRELATION ANALYSIS; DATA ANALYSIS; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; HORMONE ACTION; HORMONE DETERMINATION; HUMAN; HYPOTHYROIDISM; MOLECULAR MECHANICS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

EID: 0345283182     PISSN: 10507256     EISSN: None     Source Type: Journal    
DOI: 10.1089/105072503770867174     Document Type: Review

References (73)

1. Lumsden A, Kintner C, 2003 Neural induction and pattern formation. In: Squire LR, Bloom FE, McConnel SK, Roberts IL, Spitzer NC, Zigmond MJ (eds) Fundamental Neuroscience. Academic Press, San Diego, pp. 363-390.
2. Legrand J 1984 Effects of thyroid hormones on Central Nervous System. In: Yanai J (ed) Neurobehavioral Teratology. Elsevier Science Publishers, Amsterdam, pp. 331-363.
3. Morreale de Escobar G, Obregón MJ, Escobar de Rey F 2000 Is neuropsychological development related to maternal hypothyroidism, or to maternal hypothyroxinemia? J Clin Endocrinol Metab 85:3975-3987.
4. Bernal J 2002 Action of thyroid hormone in brain. J Endocrinol Invest 25:268-288.
5. Berbel P, Auso E, Garcia-Velasco JV, Molina ML, Camacho M 2001 Role of thyroid hormones in the maturation and organization of rat barrel cortex. Neuroscience 107:383-394.
6. Muñoz A, Bernal J 1997 Biological activities of thyroid hormone receptors. Eur J Endocrinol 137:433-445.
7. Gharami K, Das S 2000 Thyroid hormone-induced morphological differentiation and maturation of astrocytes are mediated through the beta-adrenergic receptor. J Neurochem 75:1962-1969.
8. Lima FR, Gervais A, Colin C, Izembart M, Neto VM, Mallat M 2001. Regulation of microglial development: A novel role for thyroid hormone. J Neurosci 21:2028-2038.
9. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR 2002 Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38-89.
10. Kaplan MM, Yaskoski KA 1981 Maturational patterns of iodothyronine phenolic and tyrosyl ring deiodinase activities in rat cerebrum, cerebellum, and hypothalamus. J Clin Invest 67:1208-1214.
11. Galton VA, Martínez E, Hernández A, St. Germain EA, Bates JM, St. Germain DL 1999 Pregnant rat uterus expresses high levels of the type 3 iodothyronine deiodinase. J Clin Invest 103:979-987.
12. Hernandez A, Schneider MJ, Galton VA, St. Germain DL 2003 Physiological consequences of deficiencies of the type 2 (D2) and type 3 (D3) deiodinases [Abstracts S14-1]. 85th Annual Meeting of the Endocrine Society. Philadelphia, PA, 2003, p. 22.
13. Marsh-Armstrong N, Huang H, Remo BF, Liu TT, Brown DD 1999 Asymmetric growth and development of the xenopus laevis retina during metamorphosis is controlled by type III deiodinase. Neuron 24:871-878.
14. Tu HM, Legradi G, Bartha T, Salvatore D, Lechan RM, Larsen PR 1999 Regional expression of the type 3 iodothyronine deiodinase messenger ribonucleic acid in the rat central nervous system and its regulation by thyroid hormone. Endocrinology 140:784-790.
15. Escámez MJ, Guadaño-Ferraz A, Cuadrado A, Bernal J 1999 Type 3 iodothyronine deiodinase is selectively expressed in areas related to sexual differentiation in the newborn rat brain. Endocrinology 140:5443-5446.
16. Tu HM, Kim SW, Salvatore D, Bartha T, Legradi G, Larsen PR, Lechan RM 1997 Regional distribution of type 2 thyroxine deiodinase messenger ribonucleic acid in rat hypothalamus and pituitary and its regulation by thyroid hormone. Endocrinology 138:3359-3368.
17. Guadaño-Ferraz A, Obregón MJ, St-Germain D, Bernal J 1997 The type 2 iodothyronine deiodinase is expressed primarily in glial cells in the neonatal rat brain. Proc Natl Acad Sci USA 94:10391-10396.
18. Fekete C, Harney JW, Dora JM, Gereben B, Bianco A, Sarkar S, Rand W, Emerson C, Lechan RM 2003 Type 2 iodothyronine deiodinase (D2) in the mediobasal hypothalamus may contribute to development of the nonthyroidal illness syndrome induced by bacterial lipopolysaccharide (LPS). 85th Annual Meeting of the Endocrine Society, Philadelphia, PA.
19. Guadaño-Ferraz A, Escámez MJ, Rausell E, Bernal J 1999 Expression of type 2 iodothyronine deiodinase in hypothyroid rat brain indicates an important role of thyroid hormone in the development of specific primary sensory systems. J Neurosci 19:3430-3439.
20. Ibarrola N, Mayer-Proschel M, Rodriguez-Pena A, Noble M 1996 Evidence for the existence of at least two timing mechanisms that contribute to oligodendrocyte generation in vitro. Dev Biol 180:1-21.
21. Rodriguez-Pena A, Ibarrola N, Iniguez MA, Munoz A, Bernal J 1993 Neonatal hypothyroidism affects the timely expression of myelin-associated glycoprotein in the rat brain. J Clin Invest 91:812-818.
22. Guadaño-Ferraz A, Escobar dRF, Morreale dEG, Innocenti GM, Berbel P 1994 The development of the anterior commissure in normal and hypothyroid rats. Brain Res Dev Brain Res 81:293-308.
23. Ben-Hur T, Rogister B, Murray K, Rougon G, Dubois-Dalcq M 1998 Growth and fate of PSA-NCAM+ precursors of the postnatal brain. J Neurosci 18:5777-5788.
24. Billon N, Jolicoeur C, Tokumoto Y, Vennstrom B, Raff M 2002 Normal timing of oligodendrocyte development depends on thyroid hormone receptor alpha 1 (TRalpha1). Embo J 21:6452-6460.
25. Liu YY, Tachiki KH, Brent GA 2002 A targeted thyroid hormone receptor alpha gene dominant-negative mutation (P398H) selectively impairs gene expression in differentiated embryonic stem cells. Endocrinology 143:2664-2672.
26. Perez-Juste G, Aranda A 1999 The cyclin-dependent kinase inhibitor p27(Kip1) is involved in thyroid hormone-mediated neuronal differentiation. J Biol Chem 274:5026-5031.
27. Lindholm D, Castren E, Tsoulfas P, Kolbeck R, Penha Berzaghi M, Leingartner A, Heisenberg CP, Tesarollo L, Parada LF, Thoenen H 1993 Neurotrophin-3 induced by tri-iodothyronine in cerebellar granullar cells promotes Purkinje cell differentiation. J Cell Biol 122:443-450.
28. Ruiz-Marcos A, Cartagena P, García A, Escobar del Rey F, Morreale de Escobar G 1988 Rapid effects of adult-onset hypothyroidism on dendritic spines of pyramidal cells of the rat cerebral cortex. Exp Brain Res 73:583-588.
29. Gerendasy DD, Sutcliffe JG 1997 RC3/neurogranin, a post-synaptic calpacitin for setting the response threshold to calcium influxes. Mol Neurobiol 15:131-163.
30. Iñiguez MA, Rodriguez-Pena A, Ibarrola N, Morreale de Escobar G, Bernal J 1992 Adult rat brain is sensitive to thyroid hormone. Regulation of RC3/neurogranin mRNA. J Clin Invest 90:554-558.
31. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T 1995 A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719-723.
32. Alvarez-Dolado M, Ruiz M, del Rio JA, Alcantara S, Burgaya F, Sheldon M, Nakajima K, Bernal J, Howell BW, Curran T, Soriano E, Muñoz A 1999 Thyroid hormone regulates reelin and dab1 expression during brain development. J Neurosci 19:6979-6993.
33. GarciaFernandez LF, Rausell E, Urade Y, Hayaishi O, Bernal J, Munoz A 1997 Hypothyroidism alters the expression of prostaglandin D-2 synthase beta trace in specific areas of the developing rat brain. Eur J Neurosc 9:1566-1573.
34. Alvarez-Dolado M, Gonzalez-Sancho JM, Bernal J, Muñoz A 1998 Developmental expression of tenascin-C is altered by hypothyroidism in the rat brain. Neurosci 84:309-322.
35. Alvarez-Dolado M, Cuadrado A, Navarro-Yubero C, Sonderegger P, Furley AJ, Bernal J, Muñoz A 2000 Regulation of the L1 cell adhesion molecule by thyroid hormone in the developing brain. Mol Cell Neurobiol 16:499-514.
36. Farwell AP, Lynch RM, Okulicz WC, Comi AM, Leonard JL 1990 The actin cytoskeleton mediates the hormonally regulated translocation of type II iodothyronine 5′-deiodinase in astrocytes. J Biol Chem 265:18546-18553.
37. Siegrist-Kaiser CA, Juge-Aubry C, Tranter MP, Ekenbarger DM, Leonard JL 1990 Thyroxine-dependent modulation of actin polymerization in cultured astrocytes. A novel, extranuclear action of thyroid hormone. J Biol Chem 265:5296-5302.
38. Farwell AP, Tranter MP, Leonard JL 1995 Thyroxine-dependent regulation of integrin-laminin interactions in astrocytes. Endocrinology 136:3909-3915.
39. Davis PJ, Shih A, Lin HY, Martino LJ, Davis FB 2000 Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J Biol Chem 275:38032-38039.
40. Gothe S, Wang Z, Ng L, Kindblom JM, Barros AC, Ohlsson C, Vennstrom B, Forrest D 1999 Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev 13:1329-1341.
41. Davis PJ, Davis FB 2002 Nongenomic actions of thyroid hormone on the heart. Thyroid 12:459-466.
42. Bernal J 2002 Thyroid hormones and brain development. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, Brain and Behavior. Academic Press, San Diego, CA, pp. 543-587.
43. Enriquez JA, Fernandez-Silva P, Garrido-Perez N, Lopez-Perez MJ, Perez-Martos A, Montoya J 1999 Direct regulation of mitochondrial RNA synthesis by thyroid hormone. Mol Cell Biol 19:657-670.
44. Casas F, Daury L, Grandemange S, Busson M, Seyer P, Hatier R, Carazo A, Cabello G, Wrutniak-Cabello C 2003 Endocrine regulation of mitochondrial activity: Involvement of truncated RXRalpha and c-Erb Aalpha 1 proteins. FASEB J 17:426-436.
45. Wrutniak-Cabello C, Casas F, Cabello G 2001 Thyroid hormone action in mitochondria. J Mol Endocrinol 26:67-77.
46. Morte B, Iniguez MA, Lorenzo PI, Bernal J 1997 Thyroid hormone-regulated expression of RC3/neurogranin in the immortalized hypothalamic cell line GT1-7. J Neurochem 69:902-909.
47. Martinez de Arrieta C, Morte B, Coloma A, Bernal J 1999 The human RC3 gene homolog, NRGN contains a thyroid hormone-responsive element located in the first intron. Endocrinology 140:335-343.
48. Siddiq A, Miyazaki T, Takagishi Y, Kanou Y, Hayasaka S, Inouye M, Seo H, Murata Y 2001 Expression of ZAKI-4 messenger ribonucleic acid in the brain during rat development and the effect of hypothyroidism. Endocrinology 142:1752-1759.
49. Cao X, Jong-Kook L, Moeller L, Kambe F, Hayashi Y, Refetoff S, Seo H 2003 Thyroid hormone receptor-mediated regulation of ZAKI-4α expression involves the activation of PI3K and mammalian target of rapamycin (mTOR). 85th Annual Meeting of the Endocrine Society, Philadelphia, PA.
50. Dowling AL, Zoeller RT 2000 Thyroid hormone of maternal origin regulates the expression of RC3/neurogranin mRNA in the fetal rat brain. Brain Res Mol Brain Res 82:126-132.
51. Dowling AL, Martz GU, Leonard JL, Zoeller RT 2000 Acute changes in maternal thyroid hormone induce rapid and transient changes in gene expression in fetal rat brain. J Neurosci 20:2255-2265.
52. Lavado-Autric R, Auso E, Garcia-Velasco JV, Arufe Mdel C, Escobar del Rey F, Berbel P, Morreale de Escobar G 2003 Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 111:1073-1082.
53. Harvey CB, Williams GR 2002 Mechanism of thyroid hormone action. Thyroid 12:441-446.
54. Farsetti A, Desvergne B, Hallenbeck P, Robbins J, Nikodem V 1992 Characterization of myelin basic protein thyroid hormone response element and its function in the context of native and heterologous promoter. J Biol Chem 267:15784-15788.
55. Zou L, Hagen SC, Strait KA, Oppenheimer JH 1994 Identification of thyroid hormone response elements in rodent Pcp-2, a developmentally regulated gene of cerebellar Purkinje cells. J Biol Chem 269:13346-13352.
56. Luo Y, Denker BM 1999 Interaction of heterotrimeric G protein Galphao with Purkinje cell protein-2. Evidence for a novel nucleotide exchange factor. J Biol Chem 274:10685-10688.
57. White DM, Takeda T, DeGroot LJ, Stefansson K, Arnason BG 1997 Beta-trace gene expression is regulated by a core promoter and a distal thyroid hormone response element. J Biol Chem 272:14387-14393.
58. García-Fernández LF, Urade Y, Hayaishi O, Bernal J, Muñoz A 1998 Identification of a thyroid hormone response element in the promoter region of the rat lipocalin-type prostaglandin D synthase (beta-trace) gene. Mol Brain Res 55:321-330.
59. Thompson CC 1996 Thyroid hormone-responsive genes in developing cerebellum include a novel synaptotagmin and a hairless homolog. J Neurosci 16:7832-7840.
60. Iglesias T, Caubin J, Stunnenberg HG, Zaballos A, Bernal J, Miñoz A 1996 Thyroid hormone-dependent transcriptional repression of neural cell adhesion molecule during brain maturation EMBO J 15:4307-4316.
61. Ghorbel MT, Seugnet I, Hadj-Sahraoui N, Topilko P, Levi G, Demeneix B 1999 Thyroid hormone effects on Krox-24 transcription in the post-natal mouse brain are developmentally regulated but are not correlated with mitosis. Oncogene 18:917-924.
62. Cuadrado A, Garcia-Fernandez LF, Imai T, Okano H, Munoz A 2002 Regulation of tau RNA maturation by thyroid hormone is mediated by the neural RNA-binding protein musashi-1. Mol Cel Neurosci 20:198-210.
63. Schwartz HL, Strait KA, Ling NC, Oppenheimer JH 1992 Quantitation of rat tissue thyroid hormone binding receptor isoforms by immunoprecipitation of nuclear triiodothyronine binding capacity. J Biol Chem 267:11794-11799.
64. Morte B, Manzano J, Scanlan T, Vennstrom B, Bernal J 2002 Deletion of the thyroid hormone receptor alpha 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc Natl Acad Sci USA 99:3985-3989.
65. Guadaño-Ferraz A, Benavides-Piccione R, Venero C, Lancha C, Vennström B, Sandi C, DeFelipe J, Bernal J 2003 Lack of thyroid hormone receptor α1 is associated with selective alterations in behavior and hippocampal circuits. Mol Psychiatry 8:30-38.
66. Ribeiro MO, Carvalho SD, Schultz JJ, Chiellini G, Scanlan TS, Bianco AC, Brent GA 2001 Thyroid hormone-sympathetic interaction and adaptive thermogenesis are thyroid hormone receptor isoform-specific. J Clin Invest 108:97-105.
67. Ercan-Fang S, Schwartz HL, Oppenheimer JH 1996 Isoform specific 3,5,3′-triiodothyronine receptor binding capacity and messenger ribonucleic acid content in rat adenohypophysis: Effect of thyroidal state and comparison with extrapituitary tissues. Endocrinology 137:3228-3233.
68. Flamant F, Poguet AL, Plateroti M, Chassande O, Gauthier K, Streichenberger N, Mansouri A, Samarut J 2002 Congenital hypothyroid Pax8(-/-) mutant mice can be rescued by inactivating the TRalpha gene. Mol Endocrinol 16:24-32.
69. Hashimoto K, Curty FH, Borges PP, Lee CE, Abel ED, Elmquist JK, Cohen RN, Wondisford FE 2001 An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc Natl Acad Sci USA 98:3998-4003.
70. Forrest D 2002 Twists in the tail-change-of-function mutations in thyroid hormone receptors. Endocrinology 143:2466-2468.
71. Forrest D, Hanebuth E, Smeyne RJ, Everds N, Stewart CL, Wehner JM, Curran T 1996 Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: Evidence for tissue-specific modulation of receptor function. EMBO J 15:3006-3015.
72. Dellovade TL, Chan J, Vennstrom B, Forrest D, Pfaff DW 2000 The two thyroid hormone receptor genes have opposite effects on estrogen-stimulated sex behaviors. Nat Neurosci 3:472-475.
73. Vasudevan N, Ogawa S, Pfaff D 2002 Estrogen and thyroid hormone receptor interactions: Physiological flexibility by molecular specificity. Physiol Rev 82:923-944.