The thyroid hormone receptor α1 protein is expressed in embryonic postmitotic neurons and persists in most adult neurons

Molecular Endocrinology

Volumn 24, Issue 10, 2010, Pages 1904-1916

  Wallis, Karin ^a   Dudazy, Susi ^a   Van Hogerlinden, Max ^a   Nordström, Kristina ^a   Mittag, Jens ^a   Vennström, Björn ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; GREEN FLUORESCENT PROTEIN; THYROID HORMONE RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CELL MATURATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; FEMALE; FETUS DEVELOPMENT; GENE LOCUS; GLIA CELL; HYPOTHALAMUS; IN VIVO STUDY; MALE; MATURATION; MITOSIS; MOUSE; MOUSE STRAIN; NERVE CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; TANYCYTE; TELENCEPHALON;

ANIMALS; CELL LINE, TUMOR; CEREBELLUM; EMBRYO, MAMMALIAN; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; NEUROGLIA; NEURONS; RECOMBINANT FUSION PROTEINS; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONES;

EID: 77957348924     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0175     Document Type: Article

References (66)

1. Delange FM 1996 Endemic cretinism. In: Braverman LE, Utiger RD eds. Werner and Ingbar's the thyroid, 7th ed. Philadelphia: Lippincott-Raven Publishers; 756-767
2. DeLong GR 1996 The neuromuscular system and brain in hypothyroidism. In: Braverman LE, Utiger RD, eds. Werner and Ingbar's the thyroid, 7th ed. Philadelphia: Lippincott-Raven Publishers; 826-835
3. Morreale de Escobar G, Obregon MJ, Escobar del Rey F 2004 Role of thyroid hormone during early brain development. Eur J Endocrinol 151(Suppl 3):U25-U37 (Pubitemid 39627053)
4. Sap J, Muñoz A, Damm K, Goldberg Y, Ghysdael J, Leutz A, Beug H, Vennström B 1986 The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature 324:635-640 (Pubitemid 17206350)
5. Weinberger C, Thompson CC, Ong ES, Lebo R, Gruol DJ, Evans RM 1986 The c-erb-A gene encodes a thyroid hormone receptor. Nature 324:641-646 (Pubitemid 17206351)
6. Mitsuhashi T, Tennyson GE, Nikodem VM 1988 Alternative splicing generates messages encoding rat c-erbA proteins that do not bind thyroid hormone. Proc Natl Acad Sci USA 85:5804-5808
7. Saltó C, Kindblom JM, Johansson C, Wang Z, Gullberg H, Nordström K, Mansén A, Ohlsson C, Thorén P, Forrest D, Vennström B 2001 Ablation of TRα2 and a concomitant overexpression of α1 yields a mixed hypo- and hyperthyroid phenotype in mice. Mol Endocrinol 15:2115-2128
8. Sarliève LL, Rodriguez-Peña A, Langley K 2004 Expression of thyroid hormone receptor isoforms in the oligodendrocyte lineage. Neurochem Res 29:903-922
9. Hodin RA, Lazar MA, Chin WW 1990 Differential and tissue-specific regulation of the multiple rat c-erbA messenger RNA species by thyroid hormone. J Clin Invest 85:101-105
10. Strait KA, Schwartz HL, Perez-Castillo A, Oppenheimer JH 1990 Relationship of c-erbA mRNA content to tissue triiodothyronine nuclear binding capacity and function in developing and adult rats. J Biol Chem 265:10514-10521
11. Mellström B, Naranjo JR, Santos A, Gonzalez AM, Bernal J 1991 Independent expression of the α and β c-erbA genes in developing rat brain. Mol Endocrinol 5:1339-1350
12. Forrest D, Hallböök F, Persson H, Vennström B 1991 Distinct functions for thyroid hormone receptors α and β in brain development indicated by differential expression of receptor genes. EMBO J 10:269-275 (Pubitemid 21905476)
13. Bradley DJ, Towle HC, Young III WS 1992 Spatial and temporal expression of α- and β-thyroid hormone receptor mRNAs, including the α 2-subtype, in the developing mammalian nervous system. J Neurosci 12:2288-2302
14. Bury F, Carré JL, Vega S, Ghandour MS, Rodriguez-Peña A, Langley K, Sarliève LL 2002 Coexpression of thyroid hormone receptor isoforms in mouse oligodendrocytes. J Neurosci Res 67:106-113
15. Carlson DJ, Strait KA, Schwartz HL, Oppenheimer JH 1996 Thyroid hormone receptor isoform content in cultured type 1 and type 2 astrocytes. Endocrinology 137:911-917
16. Baas D, Bourbeau D, Carre JL, Sarlieve LL, Dussault JH, Puymirat J 1994 Expression of α and β thyroid receptors during oligodendrocyte differentiation. Neuroreport 5:1805-1808 (Pubitemid 24288358)
17. Muñoz A, Wrighton C, Seliger B, Bernal J, Beug H 1993 Thyroid hormone receptor/c-erbA: control of commitment and differentiation in the neuronal/chromaffin progenitor line PC12. J Cell Biol 121:423-438 (Pubitemid 23110885)
18. 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
19. Martinez-Galan JR, Escobar del Rey F, Morreale de Escobar G, Santacana M, Ruiz-Marcos A 2004 Hypothyroidism alters the development of radial glial cells in the term fetal and postnatal neocortex of the rat. Brain Res Dev Brain Res 153:109-114 (Pubitemid 39298882)
20. Lavado-Autric R, Ausó 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
21. Ausó E, Lavado-Autric R, Cuevas E, Del Rey FE, Morreale De Escobar G, Berbel P 2004 A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 145:4037-4047 (Pubitemid 39120549)
22. Berbel P, Marco P, Cerezo JR, DeFelipe J 1996 Distribution of parvalbumin immunoreactivity in the neocortex of hypothyroid adult rats. Neurosci Lett 204:65-68
23. 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 (Pubitemid 36188571)
24. Gilbert ME, Sui L, Walker MJ, Anderson W, Thomas S, Smoller SN, Schon JP, Phani S, Goodman JH 2007 Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology 148:92-102 (Pubitemid 46021441)
25. Cuevas E, Ausó E, Telefont M, Morreale de Escobar G, Sotelo C, Berbel P 2005 Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminence-derived neurons. Eur J Neurosci 22:541-551
26. Morte B, Manzano J, Scanlan TS, Vennström B, Bernal J 2004 Aberrant maturation of astrocytes in thyroid hormone receptor α 1 knockout mice reveals an interplay between thyroid hormone receptor isoforms. Endocrinology 145:1386-1391 (Pubitemid 38281023)
27. Heuer H, Mason CA 2003 Thyroid hormone induces cerebellar Purkinje cell dendritic development via the thyroid hormone receptor α1. J Neurosci 23:10604-10612 (Pubitemid 37485274)
28. Manzano J, Bernal J, Morte B 2007 Influence of thyroid hormones on maturation of rat cerebellar astrocytes. Int J Dev Neurosci 25:171-179 (Pubitemid 46636172)
29. Lemkine GF, Raj A, Alfama G, Turque N, Hassani Z, Alegria-Prévot O, Samarut J, Levi G, Demeneix BA 2005 Adult neural stem cell cycling in vivo requires thyroid hormone and its α receptor. FASEB J 19:863-865
30. Ambrogini P, Cuppini R, Ferri P, Mancini C, Ciaroni S, Voci A, Gerdoni E, Gallo G 2005 Thyroid hormones affect neurogenesis in the dentate gyrus of adult rat. Neuroendocrinology 81:244-253
31. Desouza LA, Ladiwala U, Daniel SM, Agashe S, Vaidya RA, Vaidya VA 2005 Thyroid hormone regulates hippocampal neurogenesis in the adult rat brain. Mol Cell Neurosci 29:414-426
32. Alkemade A, Visser TJ, Fliers E 2008 Thyroid hormone signaling in the hypothalamus. Curr Opin Endocrinol Diabetes Obes 15:453-458
33. Tinnikov A, Nordström K, Thorén P, Kindblom JM, Malin S, Rozell B, Adams M, Rajanayagam O, Pettersson S, Ohlsson C, Chatterjee K, Vennström B 2002 Retardation of post-natal development caused by a negatively acting thyroid hormone receptor α1. EMBO J 21:5079-5087
34. Sjögren M, Alkemade A, Mittag J, Nordström K, Katz A, Rozell B, Westerblad H, Arner A, Vennström B 2007 Hypermetabolism in mice caused by the central action of an unliganded thyroid hormone receptor α1. EMBO J 26:4535-4545
35. 3 treatment. Genes Dev 19:2152-2163
36. Wallis K, Sjögren M, van Hogerlinden M, Silberberg G, Fisahn A, Nordström K, Larsson L, Westerblad H, Morreale de Escobar G, Shupliakov O, Vennström B 2008 Locomotor deficiencies and aberrant development of subtype-specific GABAergic interneurons caused by an unliganded thyroid hormone receptor α1. J Neurosci 28:1904-1915
37. Morte B, Manzano J, Scanlan T, Vennström B, Bernal J 2002 Deletion of the thyroid hormone receptor α 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc Natl Acad Sci USA 99:3985-3989 (Pubitemid 34252217)
38. Kaneshige M, Suzuki H, Kaneshige K, Cheng J, Wimbrow H, Barlow C, Willingham MC, Cheng S 2001 A targeted dominant negative mutation of the thyroid hormone α 1 receptor causes increased mortality, infertility, and dwarfism in mice. Proc Natl Acad Sci USA 98:15095-15100 (Pubitemid 34013975)
39. Liu YY, Schultz JJ, Brent GA 2003 A thyroid hormone receptor α gene mutation (P398H) is associated with visceral adiposity and impaired catecholamine-stimulated lipolysis in mice. J Biol Chem 278:38913-38920
40. 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 TRα gene. Mol Endocrinol 16:24-32 (Pubitemid 34044495)
41. Berry MJ, Kates AL, Larsen PR 1990 Thyroid hormone regulates type I deiodinase messenger RNA in rat liver. Mol Endocrinol 4:743-748 (Pubitemid 20369385)
42. Izumo S, Mahdavi V 1988 Thyroid hormone receptor α isoforms generated by alternative splicing differentially activate myosin HC gene transcription. Nature 334:539-542
43. Edwards JG, Bahl JJ, Flink IL, Cheng SY, Morkin E 1994 Thyroid hormone influences β myosin heavy chain (β MHC) expression. Biochem Biophys Res Commun 199:1482-1488
44. 3 and evidence for an upstream enhancer. Am J Physiol 276:C883-C891
45. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, Martin JE 1997 Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 8:711-713 (Pubitemid 127739700)
46. Hadjab-Lallemend S, Wallis K, van Hogerlinden M, Dudazy S, Nordstrom K, Vennstrom B, Fisahn A 2010 A mutant thyroid hormone receptor α1 alters hippocampal circuitry and reduces seizure susceptibility in mice. Neuropharmacology 58:1130-1139
47. Guadaño-Ferraz A, Obregón MJ, St Germain DL, 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 (Pubitemid 27407052)
48. 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
49. Manzano J, Cuadrado M, Morte B, Bernal J 2007 Influence of thyroid hormone and thyroid hormone receptors in the generation of cerebellar γ-aminobutyric acid-ergic interneurons from precursor cells. Endocrinology 148:5746-5751
50. Bernal J 2007 Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab 3:249-259 (Pubitemid 46310532)
51. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, et al. 2007 Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176 (Pubitemid 46095716)
52. Thompson CC, Bottcher MC 1997 The product of a thyroid hormone-responsive gene interacts with thyroid hormone receptors. Proc Natl Acad Sci USA 94:8527-8532 (Pubitemid 27335072)
53. Dressel U, Thormeyer D, Altincicek B, Paululat A, Eggert M, Schneider S, Tenbaum SP, Renkawitz R, Baniahmad A 1999 Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol Cell Biol 19:3383-3394 (Pubitemid 29193798)
54. Potter GB, Zarach JM, Sisk JM, Thompson CC 2002 The thyroid hormone-regulated corepressor hairless associates with histone deacetylases in neonatal rat brain. Mol Endocrinol 16:2547-2560
55. Tenbaum SP, Juenemann S, Schlitt T, Bernal J, Renkawitz R, Muñoz A, Baniahmad A 2003 Alien/CSN2 gene expression is regulated by thyroid hormone in rat brain. Dev Biol 254:149-160
56. Nishihara E, Moriya T, Shinohara K 2007 Expression of steroid receptor coactivator-1 is elevated during neuronal differentiation of murine neural stem cells. Brain Res 1135:22-30 (Pubitemid 46176821)
57. Herwig A, Ross AW, Nilaweera KN, Morgan PJ, Barrett P 2008 Hypothalamic thyroid hormone in energy balance regulation. Obesity Facts 1:71-79
58. Lechan RM, Fekete C 2007 Infundibular tanycytes as modulators of neuroendocrine function: hypothetical role in the regulation of the thyroid and gonadal axis. Acta Biomed 78(Suppl 1):84-98
59. Billon N, Jolicoeur C, Tokumoto Y, Vennström B, Raff M 2002 Normal timing of oligodendrocyte development depends on thyroid hormone receptor α 1 (TRα1). EMBO J 21:6452-6460 (Pubitemid 35448423)
60. Wikström L, Johansson C, Saltó C, Barlow C, Campos Barros A, Baas F, Forrest D, Thorén P, Vennström B 1998 Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor α 1. EMBO J 17:455-461 (Pubitemid 28045486)
61. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H 1996 Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci USA 93:5860-5865 (Pubitemid 26190768)
62. Samuels HH, Stanley F, Casanova J 1979 Depletion of L-3,5,3′- triiodothyronine and L-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. Endocrinology 105:80-85
63. Vujovic M, Nordström K, Gauthier K, Flamant F, Visser TJ, Vennström B, Mittag J 2009 Interference of a mutant thyroid hormone receptor α1 with hepatic glucose metabolism. Endocrinology 150:2940-2947
64. Sap J, de Magistris L, Stunnenberg H, Vennström B 1990 A major thyroid hormone response element in the third intron of the rat growth hormone gene. EMBO J 9:887-896 (Pubitemid 20080625)
65. Bigler J, Eisenman RN 1988 c-erbA encodes multiple proteins in chicken erythroid cells. Mol Cell Biol 8:4155-4161
66. Kapoor R, van Hogerlinden M, Wallis K, Ghosh H, Nordström K, Vennström B, Vaidya VA 13 August 2010 Unliganded thyroid hormone receptor α1 impairs adult hippocampal neurogenesis. FASEB J 10.1096/fj.10-161802