Regulators of thyroid hormone availability and action in embryonic chicken brain development

General and Comparative Endocrinology

Volumn 190, Issue , 2012, Pages 96-104

  Van Herck, Stijn L J ^a   Geysens, Stijn ^a   Delbaere, Joke ^a   Darras, Veerle M ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Brain barriers; Brain development; Chicken; Deiodinases; Mammals; TH receptors; TH transporters; Thyroid hormones

Indexed keywords

AMINO ACID TRANSPORTER; CELL NUCLEUS RECEPTOR; LIOTHYRONINE; LIOTHYRONINE RECEPTOR; MONOCARBOXYLATE TRANSPORTER 8; ORGANIC ANION TRANSPORTER 1; PREALBUMIN; THYROID HORMONE; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA; THYROXINE; THYROXINE DEIODINASE;

BIRD; BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN BLOOD VESSEL; BRAIN DEVELOPMENT; CHICKEN; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME INACTIVATION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE MUTATION; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; REVIEW; SPECIES DIFFERENCE; THYROID FUNCTION; THYROID HORMONE RELEASE;

AHDS; ALLAN-HERNDON-DUDLEY SYNDROME; BBB; BCSFB; BLOOD-BRAIN-BARRIER; BLOOD-CEREBROSPINAL FLUID-BARRIER; BRAIN BARRIERS; BRAIN DEVELOPMENT; CEREBROSPINAL FLUID; CHICKEN; CSF; D2; D3; DEIODINASES; E#; EMBRYO OF # DAYS OLD; IN SITU HYBRIDISATION; INNER/OUTER RING DEIODINATION; IRD/ORD; ISH; L-TYPE AMINO ACID TRANSPORTER; LAT; MAMMALS; MCT; MONOCARBOXYLATE TRANSPORTER; OATP; ORGANIC ANION TRANSPORTING POLYPEPTIDE; REVERSE T(3); RT(3); TH; TH RECEPTORS; TH TRANSPORTERS; THYROID HORMONE; THYROID HORMONE RECEPTOR; THYROID HORMONES; TR; TRANSTHYRETIN; TTR; TYPE 2 DEIODINASE; TYPE 3 DEIODINASE;

ANIMALS; BRAIN; CHICK EMBRYO; CHICKENS; THYROID HORMONES;

EID: 84882865543     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.05.003     Document Type: Review

References (109)

1. Abbott N.J., Patabendige A.A., Dolman D.E., Yusof S.R., Begley D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37:13-25.
2. Abe T., Kakyo M., Sakagami H., Tokui T., Nishio T., Tanemoto M., Nomura H., Hebert S.C., Matsuno S., Kondo H., Yawo H. Molecular characterization and tissue distribution of a new organic anion transporter subtype (oatp3) that transports thyroid hormones and taurocholate and comparison with oatp2. J. Biol. Chem. 1998, 273:22395-22401.
3. Ahmed O.M., El-Gareib A.W., El-Bakry A.M., Abd El-Tawab S.M., Ahmed R.G. Thyroid hormones states and brain development interactions. Int. J. Dev. Neurosci. 2008, 26:147-209.
4. Alkemade A., Friesema E.C., Kalsbeek A., Swaab D.F., Visser T.J., Fliers E. Expression of thyroid hormone transporters in the human hypothalamus. J. Clin. Endocrinol. Metab. 2011, 96:E967-971.
5. Anderson G.W., Schoonover C.M., Jones S.A. Control of thyroid hormone action in the developing rat brain. Thyroid 2003, 13:1039-1056.
6. Argumedo G.S., Sanz C.R., Olguin H.J. Experimental models of developmental hypothyroidism. Horm. Metab. Res. 2012, 44:79-85.
7. Bates J.M., St Germain D.L., Galton V.A. Expression profiles of the three iodothyronine deiodinases, D1, D2, and D3, in the developing rat. Endocrinology 1999, 140:844-851.
8. Bernal J. Thyroid hormones and brain development. Vitam. Horm. 2005, 71:95-122.
9. Bernal J. Thyroid hormone receptors in brain development and function. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3:249-259.
10. Bernal J., Pekonen F. Ontogenesis of the nuclear 3,5,3'-triiodothyronine receptor in the human fetal brain. Endocrinology 1984, 114:677-679.
11. Bradley D.J., Young W.S., Weinberger C. Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary. Proc. Natl. Acad. Sci. USA 1989, 86:7250-7254.
12. Bradley D.J., Towle H.C., Young W.S. 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, 12:2288-2302.
13. Braun D., Kinne A., Brauer A.U., Sapin R., Klein M.O., Kohrle J., Wirth E.K., Schweizer U. Developmental and cell type-specific expression of thyroid hormone transporters in the mouse brain and in primary brain cells. Glia 2011, 59:463-471.
14. Brent G.A. Mechanisms of thyroid hormone action. J. Clin. Invest. 2012, 122:3035-3043.
15. Chan S., Kachilele S., McCabe C.J., Tannahill L.A., Boelaert K., Gittoes N.J., Visser T.J., Franklyn J.A., Kilby M.D. Early expression of thyroid hormone deiodinases and receptors in human fetal cerebral cortex. Brain Res. Dev. Brain Res. 2002, 138:109-116.
16. Chan S.Y., Martin-Santos A., Loubiere L.S., Gonzalez A.M., Stieger B., Logan A., McCabe C.J., Franklyn J.A., Kilby M.D. The expression of thyroid hormone transporters in the human fetal cerebral cortex during early development and in N-Tera-2 neurodifferentiation. J. Physiol. 2011, 589:2827-2845.
17. Chang L., Munro S.L., Richardson S.J., Schreiber G. Evolution of thyroid hormone binding by transthyretins in birds and mammals. Eur. J. Biochem. 1999, 259:534-542.
18. Chanoine J.P., Braverman L.E. The role of transthyretin in the transport of thyroid hormone to cerebrospinal fluid and brain. Acta Med. Austriaca 1992, 19(Suppl. 1):25-28.
19. Cheng S.Y., Leonard J.L., Davis P.J. Molecular aspects of thyroid hormone actions. Endocr. Rev. 2010, 31:139-170.
20. Christensen H.N., Hess B., Riggs T.R. Concentration of taurine, beta-alanine, and triiodothyronine by ascites carcinoma cells. Cancer Res. 1954, 14:124-127.
21. Christoffolete M.A., Arrojo e Drigo R., Gazoni F., Tente S.M., Goncalves V., Amorim B.S., Larsen P.R., Bianco A.C., Zavacki A.M. Mice with impaired extrathyroidal thyroxine to 3,5,3'-triiodothyronine conversion maintain normal serum 3,5,3'-triiodothyronine concentrations. Endocrinology 2007, 148:954-960.
22. Crantz F.R., Silva J.E., Larsen P.R. An analysis of the sources and quantity of 3,5,3'-triiodothyronine specifically bound to nuclear receptors in rat cerebral cortex and cerebellum. Endocrinology 1982, 110:367-375.
23. Darras V.M., Van Herck S.L. Iodothyronine deiodinase structure and function: from ascidians to humans. J. Endocrinol. 2012, 215:189-206.
24. Darras V.M., Van Herck S.L., Heijlen M., De Groef B. Thyroid hormone receptors in two model species for vertebrate embryonic development: chicken and zebrafish. J. Thyroid Res. 2011, 2011:402320.
25. De Felice M., Di Lauro R. Thyroid development and its disorders: genetics and molecular mechanisms. Endocr. Rev. 2004, 25:722-746.
26. Dumitrescu A.M., Liao X.H., Best T.B., Brockmann K., Refetoff S. A novel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene. Am. J. Hum. Genet. 2004, 74:168-175.
27. Dumitrescu A.M., Liao X.H., Weiss R.E., Millen K., Refetoff S. Tissue-specific thyroid hormone deprivation and excess in monocarboxylate transporter (mct) 8-deficient mice. Endocrinology 2006, 147:4036-4043.
28. Farwell A.P., Dubord-Tomasetti S.A., Pietrzykowski A.Z., Leonard J.L. Dynamic nongenomic actions of thyroid hormone in the developing rat brain. Endocrinology 2006, 147:2567-2574.
29. Flamant F., Samarut J. Involvement of thyroid hormone and its alpha receptor in avian neurulation. Dev. Biol. 1998, 197:1-11.
30. Foelix R.F., Oppenheim R. The development of synapses in the cerebellar cortex of the chick embryo. J. Neurocytol. 1974, 3:277-294.
31. Forrest D., Sjoberg M., Vennstrom B. Contrasting developmental and tissue-specific expression of alpha and beta thyroid hormone receptor genes. EMBO J. 1990, 9:1519-1528.
32. Forrest D., Hallbook F., Persson H., Vennstrom B. Distinct functions for thyroid hormone receptors alpha and beta in brain development indicated by differential expression of receptor genes. EMBO J. 1991, 10:269-275.
33. Friesema E.C., Docter R., Moerings E.P., Verrey F., Krenning E.P., Hennemann G., Visser T.J. Thyroid hormone transport by the heterodimeric human system l amino acid transporter. Endocrinology 2001, 142:4339-4348.
34. Friesema E.C., Ganguly S., Abdalla A., Manning Fox J.E., Halestrap A.P., Visser T.J. Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J. Biol. Chem. 2003, 278:40128-40135.
35. Friesema E.C., Grueters A., Biebermann H., Krude H., von Moers A., Reeser M., Barrett T.G., Mancilla E.E., Svensson J., Kester M.H., Kuiper G.G., Balkassmi S., Uitterlinden A.G., Koehrle J., Rodien P., Halestrap A.P., Visser T.J. Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet 2004, 364:1435-1437.
36. Friesema E.C., Visser T.J., Borgers A.J., Kalsbeek A., Swaab D.F., Fliers E., Alkemade A. Thyroid hormone transporters and deiodinases in the developing human hypothalamus. Eur. J. Endocrinol. 2012, 167:379-386.
37. Galileo D.S. Spatiotemporal gradient of oligodendrocyte differentiation in chick optic tectum requires brain integrity and cell-cell interactions. Glia 2003, 41:25-37.
38. Galton V.A., Wood E.T., St Germain E.A., St Germain C.A., Aldrich G., St Germain G.M., Clark A.S., St Germain D.L. Thyroid hormone homeostasis and action in the type 2 deiodinase-deficient rodent brain during development. Endocrinology 2007, 148:3080-3088.
39. Gereben B., Pachucki J., Kollar A., Liposits Z., Fekete C. Ontogenic redistribution of type 2 deiodinase messenger ribonucleic acid in the brain of chicken. Endocrinology 2004, 145:3619-3625.
40. Geysens S., Ferran J.L., Van Herck S.L., Tylzanowski P., Puelles L., Darras V.M. Dynamic mRNA distribution pattern of thyroid hormone transporters and deiodinases during early embryonic chicken brain development. Neuroscience 2012, 221:69-85.
41. Gilbert M.E., Rovet J., Chen Z., Koibuchi N. Developmental thyroid hormone disruption: prevalence, environmental contaminants and neurodevelopmental consequences. Neurotoxicology 2012, 33:842-852.
42. Grijota-Martinez C., Diez D., Morreale de Escobar G., Bernal J., Morte B. Lack of action of exogenously administered T3 on the fetal rat brain despite expression of the monocarboxylate transporter 8. Endocrinology 2011, 152:1713-1721.
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., Faix J.D., Klein R.Z. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N. Engl. J. Med. 1999, 341:549-555.
44. Haidar M.A., Sarkar P.K. Ontogeny, regional distribution and properties of thyroid-hormone receptors in the developing chick brain. Biochem. J. 1984, 220:547-552.
45. Hanau A. Cretinism and Myxoedema. Br. Med. J. 1890, 2:786-787.
46. Harvey C.B., Williams G.R. Mechanism of thyroid hormone action. Thyroid 2002, 12:441-446.
47. Hernandez A., Martinez M.E., Fiering S., Galton V.A., St Germain D. Type 3 deiodinase is critical for the maturation and function of the thyroid axis. J. Clin. Invest. 2006, 116:476-484.
48. Hernandez A., Quignodon L., Martinez M.E., Flamant F., St Germain D.L. Type 3 deiodinase deficiency causes spatial and temporal alterations in brain T3 signaling that are dissociated from serum thyroid hormone levels. Endocrinology 2010, 151:5550-5558.
49. Heuer H., Visser T.J. Minireview: pathophysiological importance of thyroid hormone transporters. Endocrinology 2009, 150:1078-1083.
50. Heuer H., Maier M.K., Iden S., Mittag J., Friesema E.C., Visser T.J., Bauer K. The monocarboxylate transporter 8 linked to human psychomotor retardation is highly expressed in thyroid hormone-sensitive neuron populations. Endocrinology 2005, 146:1701-1706.
51. Horn S., Heuer H. Thyroid hormone action during brain development: more questions than answers. Mol. Cell. Endocrinol. 2010, 315:19-26.
52. Howdeshell K.L. A model of the development of the brain as a construct of the thyroid system. Environ. Health Perspect. 2002, 110(Suppl. 3):337-348.
53. Huang T.S., Chopra I.J., Boado R., Soloman D.H., Chua Teco G.N. Thyroxine inner ring monodeiodinating activity in fetal tissues of the rat. Pediatr. Res. 1988, 23:196-199.
54. 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, 85:2620-2623.
55. Jones I., Srinivas M., Ng L., Forrest D. The thyroid hormone receptor beta gene: structure and functions in the brain and sensory systems. Thyroid 2003, 13:1057-1068.
56. 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, 53:469-477.
57. Komur M., Ozen S., Okuyaz C., Makharoblidze K., Erdogan S. Neurodevelopment evaluation in children with congenital hypothyroidism by Bayley-III. Brain Dev. 2013, 35:392-397.
58. Krenning E.P., Docter R., Bernard H.F., Visser T.J., Hennemann G. Active-transport of triiodothyronine (T3) into isolated rat-liver cells. FEBS Lett. 1978, 91:113-116.
59. LaFranchi S. Thyroid function in the preterm infant. Thyroid 1999, 9:71-78.
60. Lavado-Autric R., Auso E., Garcia-Velasco J.V., Arufe Mdel C., Escobar del Rey F., Berbel P., Morreale de Escobar G. Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J. Clin. Invest. 2003, 111:1073-1082.
61. Leonard J.L. Non-genomic actions of thyroid hormone in brain development. Steroids 2008, 73:1008-1012.
62. Liesi P. Extracellular matrix and neuronal movement. Experientia 1990, 46:900-907.
63. McNabb F.M.A., Wilson C.M. Thyroid hormone deposition in avian eggs and effects on embryonic development. Am. Zool. 1997, 37:553-560.
64. Mebis L., Debaveye Y., Ellger B., Derde S., Ververs E.J., Langouche L., Darras V.M., Fliers E., Visser T.J., Van den Berghe G. Changes in the central component of the hypothalamus-pituitary-thyroid axis in a rabbit model of prolonged critical illness. Crit. Care 2009, 13:R147.
65. Mendel C.M., Weisiger R.A., Jones A.L., Cavalieri R.R. Thyroid hormone-binding proteins in plasma facilitate uniform distribution of thyroxine within tissues: a perfused rat liver study. Endocrinology 1987, 120:1742-1749.
66. Mey J., Thanos S. Development of the visual system of the chick. I. Cell differentiation and histogenesis. Brain Res. Brain Res. Rev. 2000, 32:343-379.
67. Morreale de Escobar G., Obregon M.J., Escobar del Rey F. Role of thyroid hormone during early brain development. Eur. J. Endocrinol. 2004, 151(Suppl. 3):U25-37.
68. Morte B., Manzano J., Scanlan T., Vennstrom B., Bernal J. Deletion of the thyroid hormone receptor alpha 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc. Natl. Acad. Sci. USA 2002, 99:3985-3989.
69. Nakao N., Takagi T., Iigo M., Tsukamoto T., Yasuo S., Masuda T., Yanagisawa T., Ebihara S., Yoshimura T. Possible involvement of organic anion transporting polypeptide 1c1 in the photoperiodic response of gonads in birds. Endocrinology 2006, 147:1067-1073.
70. Ng L., Goodyear R.J., Woods C.A., Schneider M.J., Diamond E., Richardson G.P., Kelley M.W., Germain D.L., Galton V.A., Forrest D. Hearing loss and retarded cochlear development in mice lacking type 2 iodothyronine deiodinase. Proc. Natl. Acad. Sci. USA 2004, 101:3474-3479.
71. Ng L., Hernandez A., He W., Ren T., Srinivas M., Ma M., Galton V.A., St Germain D.L., Forrest D. A protective role for type 3 deiodinase, a thyroid hormone-inactivating enzyme, in cochlear development and auditory function. Endocrinology 2009, 150:1952-1960.
72. Norkute A., Kipp M., Dang J., von Keyserlingk D.G., Valanciute A., Beyer C. Early formation of a GFAP-positive cell population in the ventricular zone during chicken brain development. Cells, Tissues, Organs 2010, 191:57-65.
73. 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, 114:305-307.
74. Ohkawa M., Ohno Y., Masuko K., Takeuchi A., Suda K., Kubo A., Kawahara R., Okazaki S., Tanaka T., Saya H., Seki M., Enomoto T., Yagi H., Hashimoto Y., Masuko T. Oncogenicity of L-type amino-acid transporter 1 (LAT1) revealed by targeted gene disruption in chicken DT40 cells: LAT1 is a promising molecular target for human cancer therapy. Biochem. Biophys. Res. Commun. 2011, 406:649-655.
75. Palha J.A., Nissanov J., Fernandes R., Sousa J.C., Bertrand L., Dratman M.B., Morreale de Escobar G., Gottesman M., Saraiva M.J. Thyroid hormone distribution in the mouse brain: the role of transthyretin. Neuroscience 2002, 113:837-847.
76. Patel J., Landers K., Li H., Mortimer R.H., Richard K. Thyroid hormones and fetal neurological development. J. Endocrinol. 2011, 209:1-8.
77. 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, 50:149-155.
78. Prati M., Calvo R., Morreale G., Morreale de Escobar G. l-Thyroxine and 3,5,3'-triiodothyronine concentrations in the chicken egg and in the embryo before and after the onset of thyroid function. Endocrinology 1992, 130:2651-2659.
79. Railton T.C. Sporadic cretinism treated by administration of the thyroid gland. Br. Med. J. 1894, 1:1180-1181.
80. Rentoumis A., Chatterjee V.K., Madison L.D., Datta S., Gallagher G.D., Degroot L.J., Jameson J.L. Negative and positive transcriptional regulation by thyroid hormone receptor isoforms. Mol. Endocrinol. 1990, 4:1522-1531.
81. Reyns G.E., Venken K., Morreale de Escobar G., Kuhn E.R., Darras V.M. Dynamics and regulation of intracellular thyroid hormone concentrations in embryonic chicken liver, kidney, brain, and blood. Gen. Comp. Endocrinol. 2003, 134:80-87.
82. Roberts L.M., Woodford K., Zhou M., Black D.S., Haggerty J.E., Tate E.H., Grindstaff K.K., Mengesha W., Raman C., Zerangue N. Expression of the thyroid hormone transporters monocarboxylate transporter-8 (SLC16A2) and organic ion transporter-14 (SLCO1C1) at the blood-brain barrier. Endocrinology 2008, 149:6251-6261.
83. Romijn H.J., Hofman M.A., Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby?. Early Hum. Dev. 1991, 26:61-67.
84. Rudas P., Ronai Z., Bartha T. Thyroid hormone metabolism in the brain of domestic animals. Domest. Anim. Endocrinol. 2005, 29:88-96.
85. Ruiz de Ona C., Obregon M.J., Escobar del Rey F., Morreale de Escobar G. Developmental changes in rat brain 5'-deiodinase and thyroid hormones during the fetal period: the effects of fetal hypothyroidism and maternal thyroid hormones. Pediatr. Res. 1988, 24:588-594.
86. Samuels H.H., Tsai J.S., Casanova J., Stanley F. Thyroid hormone action: in vitro characterization of solubilized nuclear receptors from rat liver and cultured GH1 cells. J. Clin. Invest. 1974, 54:853-865.
87. Santos G.M., Fairall L., Schwabe J.W. Negative regulation by nuclear receptors: a plethora of mechanisms. Trends Endocrinol. Metab. 2011, 22:87-93.
88. Sap J., Munoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennstrom B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature 1986, 324:635-640.
89. Schneider M.J., Fiering S.N., Pallud S.E., Parlow A.F., St Germain D.L., Galton V.A. Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Mol. Endocrinol. 2001, 15:2137-2148.
90. Shepard T.H. Onset of function in the human fetal thyroid: biochemical and radioautographic studies from organ culture. J. Clin. Endocrinol. Metab. 1967, 27:945-958.
91. Siegrist-Kaiser C.A., Juge-Aubry C., Tranter M.P., Ekenbarger D.M., Leonard J.L. Thyroxine-dependent modulation of actin polymerization in cultured astrocytes. A novel, extranuclear action of thyroid hormone. J. Biol. Chem. 1990, 265:5296-5302.
92. Sjoberg M., Vennstrom B., Forrest D. Thyroid hormone receptors in chick retinal development: differential expression of mRNAs for alpha and N-terminal variant beta receptors. Development 1992, 114:39-47.
93. Skeaff S.A. Iodine deficiency in pregnancy: the effect on neurodevelopment in the child. Nutrients 2011, 3:265-273.
94. St Germain D.L., Galton V.A., Hernandez A. Minireview: defining the roles of the iodothyronine deiodinases: current concepts and challenges. Endocrinology 2009, 150:1097-1107.
95. Thommes R.C. Ontogenesis of thyroid function and regulation in the developing chick embryo. J. Exp. Zool. Suppl. 1987, 1:273-279.
96. Tohyama K., Kusuhara H., Sugiyama Y. Involvement of multispecific organic anion transporter, Oatp14 (Slc21a14), in the transport of thyroxine across the blood-brain barrier. Endocrinology 2004, 145:4384-4391.
97. Trajkovic M., Visser T.J., Mittag J., Horn S., Lukas J., Darras V.M., Raivich G., Bauer K., Heuer H. Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter 8. J. Clin. Invest. 2007, 117:627-635.
98. Van der Geyten S., Van den Eynde I., Segers I.B., Kuhn E.R., Darras V.M. Differential expression of iodothyronine deiodinases in chicken tissues during the last week of embryonic development. Gen. Comp. Endocrinol. 2002, 128:65-73.
99. Van Herck S.L., Geysens S., Delbaere J., Tylzanowski P., Darras V.M. Expression profile and thyroid hormone responsiveness of transporters and deiodinases in early embryonic chicken brain development. Mol. Cell. Endocrinol. 2012, 349:289-297.
100. Verhoelst C.H., Vandenborne K., Severi T., Bakker O., Zandieh Doulabi B., Leonard J.L., Kuhn E.R., van der Geyten S., Darras V.M. Specific detection of type III iodothyronine deiodinase protein in chicken cerebellar purkinje cells. Endocrinology 2002, 143:2700-2707.
101. Verhoelst C.H., Darras V.M., Doulabi B.Z., Reyns G., Kuhn E.R., Van der Geyten S. Type I iodothyronine deiodinase in euthyroid and hypothyroid chicken cerebellum. Mol. Cell. Endocrinol. 2004, 214:97-105.
102. Verhoelst C.H., Darras V.M., Roelens S.A., Artykbaeva G.M., Van der Geyten S. Type II iodothyronine deiodinase protein in chicken choroid plexus: additional perspectives on T3 supply in the avian brain. J. Endocrinol. 2004, 183:235-241.
103. Verhoelst C.H., Roelens S.A., Darras V.M. Role of spatiotemporal expression of iodothyronine deiodinase proteins in cerebellar cell organization. Brain Res. Bull. 2005, 67:196-202.
104. Visser W.E., Friesema E.C., Jansen J., Visser T.J. Thyroid hormone transport in and out of cells. Trends Endocrinol. Metab. 2008, 19:50-56.
105. Williams G.R. Cloning and characterization of two novel thyroid hormone receptor beta isoforms. Mol. Cell. Biol. 2000, 20:8329-8342.
106. Williams G.R. Neurodevelopmental and neurophysiological actions of thyroid hormone. J. Neuroendocrinol. 2008, 20:784-794.
107. Wirth E.K., Roth S., Blechschmidt C., Holter S.M., Becker L., Racz I., Zimmer A., Klopstock T., Gailus-Durner V., Fuchs H., Wurst W., Naumann T., Brauer A., de Angelis M.H., Kohrle J., Gruters A., Schweizer U. Neuronal 3',3,5-triiodothyronine (T3) uptake and behavioral phenotype of mice deficient in Mct8, the neuronal T3 transporter mutated in Allan-Herndon-Dudley syndrome. J. Neurosci. 2009, 29:9439-9449.
108. Zoeller R.T. Transplacental thyroxine and fetal brain development. J. Clin. Invest. 2003, 111:954-957.
109. Zoeller R.T., Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 2004, 16:809-818.