Effects of thyroid hormone transporters MCT8 and MCT10 on nuclear activity of T3

Molecular and Cellular Endocrinology

Volumn 437, Issue , 2016, Pages 252-260

  van Mullem, Alies A ^a   van Gucht, Anja L M ^a   Visser, W Edward ^a   Meima, Marcel E ^a   Peeters, Robin P ^a   Visser, Theo J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Deiodinase; Nuclear receptor; Thyroid hormone; Transporter

Indexed keywords

CELL NUCLEUS RECEPTOR; CRYSTALLIN; LIOTHYRONINE; LUCIFERASE; MONOCARBOXYLATE TRANSPORTER; MONOCARBOXYLATE TRANSPORTER 10; MONOCARBOXYLATE TRANSPORTER 8; THYROID HORMONE RECEPTOR BETA; THYROXINE DEIODINASE; TYPE 3 DEIODINASE; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; SLC16A10 PROTEIN, HUMAN; SLC16A2 PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHORIOCARCINOMA CELL LINE; CONTROLLED STUDY; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; THYROID HORMONE METABOLISM; BIOLOGICAL MODEL; DRUG EFFECTS; ENDOCYTOSIS; GENETIC TRANSFECTION; METABOLISM; REPORTER GENE; TUMOR CELL LINE;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; CELL LINE, TUMOR; CELL NUCLEUS; ENDOCYTOSIS; GENES, REPORTER; HUMANS; MODELS, BIOLOGICAL; MONOCARBOXYLIC ACID TRANSPORTERS; TRANSFECTION; TRIIODOTHYRONINE;

EID: 84984652054     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2016.07.037     Document Type: Article

References (47)

1. Abe, S., Katagiri, T., Saito-Hisaminato, A., Usami, S., Inoue, Y., Tsunoda, T., Nakamura, Y., Identification of CRYM as a candidate responsible for nonsyndromic deafness, through cDNA microarray analysis of human cochlear and vestibular tissues. Am. J. Hum. Genet. 72 (2003), 73–82.
2. Alkemade, A., Friesema, E.C., Unmehopa, U.A., Fabriek, B.O., Kuiper, G.G., Leonard, J.L., Wiersinga, W.M., Swaab, D.F., Visser, T.J., Fliers, E., Neuroanatomical pathways for thyroid hormone feedback in the human hypothalamus. J. Clin. Endocrinol. Metab. 90 (2005), 4322–4334.
3. Baqui, M., Botero, D., Gereben, B., Curcio, C., Harney, J.W., Salvatore, D., Sorimachi, K., Larsen, P.R., Bianco, A.C., Human type 3 iodothyronine selenodeiodinase is located in the plasma membrane and undergoes rapid internalization to endosomes. J. Biol. Chem. 278 (2003), 1206–1211.
4. 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 140 (1999), 844–851.
5. Beslin, A., Vie, M.P., Blondeau, J.P., Francon, J., Identification by photoaffinity labelling of a pyridine nucleotide-dependent tri-iodothyronine-binding protein in the cytosol of cultured astroglial cells. Biochem. J. 305:Pt 3 (1995), 729–737.
6. 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 59 (2011), 463–471.
7. Capri, Y., Friesema, E.C., Kersseboom, S., Touraine, R., Monnier, A., Eymard-Pierre, E., Des Portes, V., De Michele, G., Brady, A.F., Boespflug-Tanguy, O., Visser, T.J., Vaurs-Barriere, C., Relevance of different cellular models in determining the effects of mutations on SLC16A2/MCT8 thyroid hormone transporter function and genotype-phenotype correlation. Hum. Mutat. 34 (2013), 1018–1025.
8. Ceballos, A., Belinchon, M.M., Sanchez-Mendoza, E., Grijota-Martinez, C., Dumitrescu, A.M., Refetoff, S., Morte, B., Bernal, J., Importance of monocarboxylate transporter 8 for the blood-brain barrier-dependent availability of 3,5,3'-triiodo-L-thyronine. Endocrinology 150 (2009), 2491–2496.
9. 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. 74 (2004), 168–175.
10. 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 147 (2006), 4036–4043.
11. 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. 278 (2003), 40128–40135.
12. 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 364 (2004), 1435–1437.
13. Friesema, E.C., Kuiper, G.G., Jansen, J., Visser, T.J., Kester, M.H., Thyroid hormone transport by the human monocarboxylate transporter 8 and its rate-limiting role in intracellular metabolism. Mol. Endocrinol. 20 (2006), 2761–2772.
14. Friesema, E.C., Jansen, J., Heuer, H., Trajkovic, M., Bauer, K., Visser, T.J., Mechanisms of disease: psychomotor retardation and high T3 levels caused by mutations in monocarboxylate transporter 8. Nat. Clin. Pract. Endocrinol. Metab. 2 (2006), 512–523.
15. Friesema, E.C., Jansen, J., Jachtenberg, J.W., Visser, W.E., Kester, M.H., Visser, T.J., Effective cellular uptake and efflux of thyroid hormone by human monocarboxylate transporter 10. Mol. Endocrinol. 22 (2008), 1357–1369.
16. Hallen, A., Cooper, A.J., Jamie, J.F., Haynes, P.A., Willows, R.D., Mammalian forebrain ketimine reductase identified as mu-crystallin; potential regulation by thyroid hormones. J. Neurochem. 118 (2011), 379–387.
17. Hernandez, A., Structure and function of the type 3 deiodinase gene. Thyroid 15 (2005), 865–874.
18. Heuer, H., The importance of thyroid hormone transporters for brain development and function. Best Pract. Res. Clin. Endocrinol. Metab. 21 (2007), 265–276.
19. 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 146 (2005), 1701–1706.
20. Jansen, J., Friesema, E.C., Kester, M.H., Schwartz, C.E., Visser, T.J., Genotype-phenotype relationship in patients with mutations in thyroid hormone transporter MCT8. Endocrinology 149 (2008), 2184–2190.
21. Kester, M.H., Martinez de Mena, R., Obregon, M.J., Marinkovic, D., Howatson, A., Visser, T.J., Hume, R., Morreale de Escobar, G., Iodothyronine levels in the human developing brain: major regulatory roles of iodothyronine deiodinases in different areas. J. Clin. Endocrinol. Metab. 89 (2004), 3117–3128.
22. Kim, D.K., Kanai, Y., Matsuo, H., Kim, J.Y., Chairoungdua, A., Kobayashi, Y., Enomoto, A., Cha, S.H., Goya, T., Endou, H., The human T-type amino acid transporter-1: characterization, gene organization, and chromosomal location. Genomics 79 (2002), 95–103.
23. Kinne, A., Kleinau, G., Hoefig, C.S., Gruters, A., Kohrle, J., Krause, G., Schweizer, U., Essential molecular determinants for thyroid hormone transport and first structural implications for monocarboxylate transporter 8. J. Biol. Chem. 285 (2010), 28054–28063.
24. Kuiper, G.G., Kester, M.H., Peeters, R.P., Visser, T.J., Biochemical mechanisms of thyroid hormone deiodination. Thyroid 15 (2005), 787–798.
25. Mayerl, S., Muller, J., Bauer, R., Richert, S., Kassmann, C.M., Darras, V.M., Buder, K., Boelen, A., Visser, T.J., Heuer, H., Transporters MCT8 and OATP1C1 maintain murine brain thyroid hormone homeostasis. J. Clin. Invest. 124 (2014), 1987–1999.
26. Mol, J.A., Visser, T.J., Synthesis and some properties of sulfate esters and sulfamates of iodothyronines. Endocrinology 117 (1985), 1–7.
27. Muller, J., Heuer, H., Expression pattern of thyroid hormone transporters in the postnatal mouse brain. Front. Endocrinol. (Lausanne), 5, 2014, 92.
28. Namba, N., Etani, Y., Kitaoka, T., Nakamoto, Y., Nakacho, M., Bessho, K., Miyoshi, Y., Mushiake, S., Mohri, I., Arai, H., Taniike, M., Ozono, K., Clinical phenotype and endocrinological investigations in a patient with a mutation in the MCT8 thyroid hormone transporter. Eur. J. Pediatr. 167 (2008), 785–791.
29. Nishimura, M., Naito, S., Tissue-specific mRNA expression profiles of human solute carrier transporter superfamilies. Drug Metab. Pharmacokinet. 23 (2008), 22–44.
30. Oppenheimer, J.H., Schwartz, H.L., Molecular basis of thyroid hormone-dependent brain development. Endocr. Rev. 18 (1997), 462–475.
31. Peeters, R.P., Hernandez, A., Ng, L., Ma, M., Sharlin, D.S., Pandey, M., Simonds, W.F., St Germain, D.L., Forrest, D., Cerebellar abnormalities in mice lacking type 3 deiodinase and partial reversal of phenotype by deletion of thyroid hormone receptor alpha1. Endocrinology 154 (2013), 550–561.
32. Pol, C.J., Muller, A., Zuidwijk, M.J., van Deel, E.D., Kaptein, E., Saba, A., Marchini, M., Zucchi, R., Visser, T.J., Paulus, W.J., Duncker, D.J., Simonides, W.S., Left-ventricular remodeling after myocardial infarction is associated with a cardiomyocyte-specific hypothyroid condition. Endocrinology 152 (2011), 669–679.
33. 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 149 (2008), 6251–6261.
34. Schwartz, C.E., Stevenson, R.E., The MCT8 thyroid hormone transporter and Allan-Herndon-Dudley syndrome. Best Pract. Res. Clin. Endocrinol. Metab. 21 (2007), 307–321.
35. Schweizer, U., Kohrle, J., Function of thyroid hormone transporters in the central nervous system. Biochim. Biophys. Acta 1830:7 (2013 Jul), 3965–3973 PMID: 22890106.
36. Suzuki, S., Mori, J., Kobayashi, M., Inagaki, T., Inaba, H., Komatsu, A., Yamashita, K., Takeda, T., Miyamoto, T., Ichikawa, K., Hashizume, K., Cell-specific expression of NADPH-dependent cytosolic 3,5,3'-triiodo-L-thyronine-binding protein (p38CTBP). Eur. J. Endocrinol. 148 (2003), 259–268.
37. Suzuki, S., Suzuki, N., Mori, J., Oshima, A., Usami, S., Hashizume, K., micro-Crystallin as an intracellular 3,5,3'-triiodothyronine holder in vivo. Mol. Endocrinol. 21 (2007), 885–894.
38. Suzuki, S., Mori, J., Hashizume, K., mu-crystallin, a NADPH-dependent T(3)-binding protein in cytosol. Trends Endocrinol. Metab. 18 (2007), 286–289.
39. 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. 117 (2007), 627–635.
40. Tu, H.M., Legradi, G., Bartha, T., Salvatore, D., Lechan, R.M., Larsen, P.R., 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 (1999), 784–790.
41. van Mullem, A., van Heerebeek, R., Chrysis, D., Visser, E., Medici, M., Andrikoula, M., Tsatsoulis, A., Peeters, R., Visser, T.J., Clinical phenotype and mutant TRalpha1. N. Engl. J. Med. 366 (2012), 1451–1453.
42. Visser, W.E., Visser, T.J., Finding the way into the brain without MCT8. J. Clin. Endocrinol. Metab. 97 (2012), 4362–4365.
43. Visser, W.E., Jansen, J., Friesema, E.C., Kester, M.H., Mancilla, E., Lundgren, J., van der Knaap, M.S., Lunsing, R.J., Brouwer, O.F., Visser, T.J., Novel pathogenic mechanism suggested by ex vivo analysis of MCT8 (SLC16A2) mutations. Hum. Mutat. 30 (2009), 29–38.
44. Visser, W.E., Friesema, E.C., Visser, T.J., Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol. Endocrinol. 25 (2011), 1–14.
45. 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. 29 (2009), 9439–9449.
46. Zhang, J., Lazar, M.A., The mechanism of action of thyroid hormones. Annu. Rev. Physiol. 62 (2000), 439–466.
47. Zoeller, R.T., Rovet, J., Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 16 (2004), 809–818.