Best Practice & Research Clinical Endocrinology & Metabolism
Volume 21, Issue 2 , Pages 265-276 , June 2007

The importance of thyroid hormone transporters for brain development and function

  • Heike Heuer (Junior Research Group Leader)

      Affiliations

    • Corresponding Author InformationTel.: +49 3641 65 6021; Fax: +49 3641 65 6040.

References 

  1. Legrand J. Effects of thyroid hormones on central nervous system development. In:  Yanai J editors. Neurobehavioral Teratology. Amsterdam: Elsevier; 1984;p. 331–363
  2. Oppenheimer JH, Schwartz HL. Molecular basis of thyroid hormone-dependent brain development. Endocrine Reviews. 1997;18:462–475
  3. Anderson GW, Schoonover CM, Jones SA. Control of thyroid hormone action in the developing rat brain. Thyroid. 2003;13:1039–1056
  4. Bernal J. Thyroid hormones and brain development. Vitamins and Hormones. 2005;71:95–122
  5. DeLong GR, Stanbury JB, Fierro-Benitez R. Neurological signs in congenital iodine-deficiency disorder (endemic cretinism). Developmental Medicine and Child Neurology. 1985;27:317–324
  6. Forrest D, Reh TA, Rusch A. Neurodevelopmental control by thyroid hormone receptors. Current Opinion in Neurobiology. 2002;12:49–56
  7. Bassett JH, Harvey CB, Williams GR. Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions. Molecular and Cellular Endocrinology. 2003;213:1–11
  8. Flamant F, Baxter JD, Forrest D, et al. International Union of Pharmacology. LIX. The pharmacology and classification of the nuclear receptor superfamily: thyroid hormone receptors. Pharmacological Reviews. 2006;58:705–711
  9. Mellstrom B, Naranjo JR, Santos A, et al. Independent expression of the alpha and beta c-erbA genes in developing rat brain. Molecular Endocrinology. 1991;5:1339–1350
  10. Bradley DJ, Towle HC, Young WS. Spatial and temporal expression of alpha- and beta-thyroid hormone receptor mRNAs, including the beta 2-subtype, in the developing mammalian nervous system. Journal of Neuroscience. 1992;12:2288–2302
  11. Bianco AC, Salvatore D, Gereben B, et al. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocrine Reviews. 2002;23:38–89
  12. Kohrle J. Iodothyronine deiodinases. Methods in Enzymology. 2002;347:125–167
  13. Guadano-Ferraz A, Obregon MJ, St Germain DL, et al. The type 2 iodothyronine deiodinase is expressed primarily in glial cells in the neonatal rat brain. Proceedings of the National Academy of Sciences of the USA. 1997;94:10391–10396
  14. Guadano-Ferraz A, Escamez MJ, Rausell E, et al. 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. Journal of Neuroscience. 1999;19:3430–3439
  15. Tu HM, Legradi G, Bartha T, et al. Regional expression of the type 3 iodothyronine deiodinase messenger ribonucleic acid in the rat central nervous system and its regulation by thyroid hormone. Endocrinology. 1999;140:784–790
  16. Burmeister LA, Pachucki J, St Germain DL. Thyroid hormones inhibit type 2 iodothyronine deiodinase in the rat cerebral cortex by both pre- and posttranslational mechanisms. Endocrinology. 1997;138:5231–5237
  17. Friedrichsen S, Christ S, Heuer H, et al. Regulation of iodothyronine deiodinases in the Pax8-/- mouse model of congenital hypothyroidism. Endocrinology. 2003;144:777–784
  18. Calvo R, Obregon MJ, Ruiz de Ona C, et al. 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. The Journal of Clinical Investigation. 1990;86:889–899
  19. Dratman MB, Crutchfield FL, Schoenhoff MB. Transport of iodothyronines from bloodstream to brain: contributions by blood:brain and choroid plexus:cerebrospinal fluid barriers. Brain Research. 1991;554:229–236
  20. Crantz FR, Silva JE, Larsen PR. 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
  21. Schneider MJ, Fiering SN, Pallud SE, et al. Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Molecular Endocrinology. 2001;15:2137–2148
  22. Galton VA, Wood, E, St Germain EA et al. Thyroid hormone homeostasis and action in the type 2 deiodinase-deficient rodent brain during development. Endocrinology (in press). [Epub ahead of print: 1 March 2007]
  23. Hennemann G, Docter R, Friesema EC, et al. Plasma membrane transport of thyroid hormones and its role in thyroid hormone metabolism and bioavailability. Endocrine Reviews. 2001;22:451–476
  24. Abe T, Kakyo M, Sakagami H, et al. Molecular characterization and tissue distribution of a new organic anion transporter subtype (oatp3) that transports thyroid hormones and taurocholate and comparison with oatp2. The Journal of Biological Chemistry. 1998;273:22395–22401
  25. Friesema EC, Jansen J, Milici C, et al. Thyroid hormone transporters. Vitamins and Hormones. 2005;70:137–167
  26. Jansen J, Friesema EC, Milici C, et al. Thyroid hormone transporters in health and disease. Thyroid. 2005;15:757–768
  27. Friesema EC, Docter R, Moerings EP, et al. Identification of thyroid hormone transporters. Biochemical and Biophysical Research Communications. 1999;254:497–501
  28. Hagenbuch B, Dawson P. The sodium bile salt cotransport family SLC10. Pflügers Archiv. 2004;447:566–570
  29. Ritchie JW, Peter GJ, Shi YB, et al. Thyroid hormone transport by 4F2hc-IU12 heterodimers expressed in Xenopus oocytes. The Journal of Endocrinology. 1999;163:R5–R9
  30. Friesema EC, Docter R, Moerings EP, et al. Thyroid hormone transport by the heterodimeric human system L amino acid transporter. Endocrinology. 2001;142:4339–4348
  31. Pizzagalli F, Hagenbuch B, Stieger B, et al. Identification of a novel human organic anion transporting polypeptide as a high affinity thyroxine transporter. Molecular Endocrinology. 2002;16:2283–2296
  32. Sugiyama D, Kusuhara H, Taniguchi H, et al. Functional characterization of rat brain-specific organic anion transporter (Oatp14) at the blood-brain barrier: high affinity transporter for thyroxine. The Journal of Biological Chemistry. 2003;278:43489–43495
  33. 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
  34. Friesema EC, Ganguly S, Abdalla A, et al. Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. The Journal of Biological Chemistry. 2003;278:40128–40135
  35. Halestrap AP, Meredith D. The SLC16 gene family – from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflügers Archiv. 2004;447:619–628
  36. Friesema EC, Jachtenberg JW, Jansen J, et al. Human monocarboxylate transporter 10 does transport thyroid hormone. Thyroid. 2006;16:913;[77th Annual meeting of the American Thyroid Association]
  37. Chan SY, Franklyn JA, Pemberton HN, et al. Monocarboxylate transporter 8 expression in the human placenta: the effects of severe intrauterine growth restriction. The Journal of Endocrinology. 2006;189:465–471
  38. Heuer H, Maier MK, Iden S, et al. The monocarboxylate transporter 8 linked to human psychomotor retardation is highly expressed in thyroid hormone-sensitive neuron populations. Endocrinology. 2005;146:1701–1706
  39. Friesema EC, Jansen J, Heuer H, et al. Mechanisms of disease: psychomotor retardation and high T3 levels caused by mutations in monocarboxylate transporter 8. Nature Clinical Practice. Endocrinology & Metabolism. 2006;2:512–523
  40. Friesema EC, Grueters A, Biebermann H, et al. Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet. 2004;364:1435–1437
  41. Dumitrescu AM, Liao XH, Best TB, et al. A novel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene. American Journal of Human Genetics. 2004;74:168–175
  42. Biebermann H, Ambrugger P, Tarnow P, et al. Extended clinical phenotype, endocrine investigations and functional studies of a loss-of-function mutation A150V in the thyroid hormone specific transporter MCT8. European Journal of Endocrinology. 2005;153:359–366
  43. Brockmann K, Dumitrescu AM, Best TT, et al. X-linked paroxysmal dyskinesia and severe global retardation caused by defective MCT8 gene. Journal of Neurology. 2005;252:663–666
  44. Holden KR, Zuniga OF, May MM, et al. X-linked MCT8 gene mutations: characterization of the pediatric neurologic phenotype. Journal of Child Neurology. 2005;20:852–857
  45. Schwartz CE, May MM, Carpenter NJ, et al. Allan-Herndon-Dudley syndrome and the monocarboxylate transporter 8 (MCT8) gene. American Journal of Human Genetics. 2005;77:41–53
  46. Maranduba CM, Friesema EC, Kok F, et al. Decreased cellular uptake and metabolism in Allan-Herndon-Dudley syndrome (AHDS) due to a novel mutation in the MCT8 thyroid hormone transporter. Journal of Medical Genetics. 2006;43:457–460
  47. Herzovich V, Vaiani E, Marino R, et al. Unexpected Peripheral Markers of Thyroid Function in a Patient with a Novel Mutation of the MCT8 Thyroid Hormone Transporter Gene. Hormone Research. 2006;67:1–6
  48. Allan W, Herndon CN, Dudley FC. Some examples of the inheritance of mental deficiency: apparently sex-linked idiocy and microcephaly. American Journal of Mental Deficiency. 1944;48:325–334
  49. Dumitrescu AM, Liao XH, Weiss RE, et al. Tissue-specific thyroid hormone deprivation and excess in monocarboxylate transporter (mct) 8-deficient mice. Endocrinology. 2006;147:4036–4043
  50. Trajkovic M, Visser TJ, Mittag J, et al. Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter. The Journal of Clinical Investigation. 2007;117:627–635
  51. Iniguez MA, De Lecea L, Guadano-Ferraz A, et al. Cell-specific effects of thyroid hormone on RC3/neurogranin expression in rat brain. Endocrinology. 1996;137:1032–1041
  52. Guadano-Ferraz A, Escamez MJ, Morte B, et al. Transcriptional induction of RC3/neurogranin by thyroid hormone: differential neuronal sensitivity is not correlated with thyroid hormone receptor distribution in the brain. Brain Research. Molecular Brain Research. 1997;49:37–44
  53. Koibuchi N, Jingu H, Iwasaki T, et al. Current perspectives on the role of thyroid hormone in growth and development of cerebellum. Cerebellum. 2003;2:279–289
  54. Heuer H, Mason CA. Thyroid hormone induces cerebellar Purkinje cell dendritic development via the thyroid hormone receptor alpha1. The Journal of Neuroscience. 2003;23:10604–10612
  55. Gao B, Stieger B, Noe B, et al. Localization of the organic anion transporting polypeptide 2 (Oatp2) in capillary endothelium and choroid plexus epithelium of rat brain. The Journal of Histochemistry and Cytochemistry. 1999;47:1255–1264
  56. Ohtsuki S, Takizawa T, Takanaga H, et al. Localization of organic anion transporting polypeptide 3 (oatp3) in mouse brain parenchymal and capillary endothelial cells. The Journal of Neuroscience. 2004;90:743–749
  57. Ito A, Yamaguchi K, Onogawa T, et al. Distribution of organic anion-transporting polypeptide 2 (oatp2) and oatp3 in the rat retina. Investigative Ophthalmology & Visual Science. 2002;43:858–863
  58. The Gene Expression Nervous System Atlas (GENSAT) Project, NINDS Contract # N01NS02331 to The Rockefeller University (New York, NY), http://www.ncbi.nlm.nih.gov/projects/gensat [search for "oatp 1c1"].

PII: S1521-690X(07)00024-3

doi: 10.1016/j.beem.2007.03.003

Best Practice & Research Clinical Endocrinology & Metabolism
Volume 21, Issue 2 , Pages 265-276 , June 2007

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