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Thyroid Hormone Signaling in Oligodendrocytes: from Extracellular Transport to Intracellular Signal

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Abstract

Thyroid hormone plays an important role in central nervous system (CNS) development, including the myelination of variable axonal calibers. It is well-established that thyroid hormone is required for the terminal differentiation of oligodendrocyte precursor cells (OPCs) into myelinating oligodendrocytes by inducing rapid cell-cycle arrest and constant transcription of pro-differentiation genes. This is well supported by the hypomyelinating phenotypes exhibited by patients with congenital hypothyroidism, cretinism. During development, myelinating oligodendrocytes only appear after the formation of neural circuits, indicating that the timing of oligodendrocyte differentiation is important. Since fetal and post-natal serum thyroid hormone levels peak at the stage of active myelination, it is suspected that the timing of oligodendrocyte development is finely controlled by thyroid hormone. The essential machinery for thyroid hormone signaling such as deiodinase activity (utilized by cells to auto-regulate the level of thyroid hormone), and nuclear thyroid hormone receptors (for gene transcription) are expressed on oligodendrocytes. In this review, we discuss the known and potential thyroid hormone signaling pathways that may regulate oligodendrocyte development and CNS myelination. Moreover, we evaluate the potential of targeting thyroid hormone signaling for white matter injury or disease.

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References

  1. Cheng SY, Leonard JL, Davis PJ (2010) Molecular aspects of thyroid hormone actions. Endocr Rev 31(2):139–170. doi:10.1210/er.2009-0007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Williams GR (2008) Neurodevelopmental and neurophysiological actions of thyroid hormone. J Neuroendocrinol 20(6):784–794. doi:10.1111/j.1365-2826.2008.01733.x

    Article  CAS  PubMed  Google Scholar 

  3. Moog NK, Entringer S, Heim C, Wadhwa PD, Kathmann N, Buss C (2015) Influence of maternal thyroid hormones during gestation on fetal brain development. Neuroscience. doi:10.1016/j.neuroscience.2015.09.070

  4. Bernal J, Guadano-Ferraz A, Morte B (2015) Thyroid hormone transporters—functions and clinical implications. Nat Rev Endocrinol 11(9):506. doi:10.1038/nrendo.2015.113

    PubMed  Google Scholar 

  5. Rasband MN, Peles E (2015) The nodes of Ranvier: molecular assembly and maintenance. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a020495

  6. Tokumoto YM, Tang DG, Raff MC (2001) Two molecularly distinct intracellular pathways to oligodendrocyte differentiation: role of a p53 family protein. Embo J 20(18):5261–5268. doi:10.1093/emboj/20.18.5261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Billon N, Terrinoni A, Jolicoeur C, McCarthy A, Richardson WD, Melino G, Raff M (2004) Roles for p53 and p73 during oligodendrocyte development. Development 131(6):1211–1220. doi:10.1242/dev.01035

    Article  CAS  PubMed  Google Scholar 

  8. Farsetti A, Mitsuhashi T, Desvergne B, Robbins J, Nikodem VM (1991) Molecular basis of thyroid hormone regulation of myelin basic protein gene expression in rodent brain. J Biol Chem 266(34):23226–23232

    CAS  PubMed  Google Scholar 

  9. Dugas JC, Ibrahim A, Barres BA (2012) The T3-induced gene KLF9 regulates oligodendrocyte differentiation and myelin regeneration. Mol Cell Neurosci 50(1):45–57. doi:10.1016/j.mcn.2012.03.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Fernandez M, Giuliani A, Pirondi S, D’Intino G, Giardino L, Aloe L, Levi-Montalcini R, Calza L (2004) Thyroid hormone administration enhances remyelination in chronic demyelinating inflammatory disease. Proc Natl Acad Sci U S A 101(46):16363–16368. doi:10.1073/pnas.0407262101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yuen TJ, Silbereis JC, Griveau A, Chang SM, Daneman R, Fancy SP, Zahed H, Maltepe E, Rowitch DH (2014) Oligodendrocyte-encoded HIF function couples postnatal myelination and white matter angiogenesis. Cell 158(2):383–396. doi:10.1016/j.cell.2014.04.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Friesema EC, Ganguly S, Abdalla A, Manning Fox JE, Halestrap AP, Visser TJ (2003) Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J Biol Chem 278(41):40128–40135. doi:10.1074/jbc.M300909200

    Article  CAS  PubMed  Google Scholar 

  13. Friesema EC, Grueters A, Biebermann H, Krude H, von Moers A, Reeser M, Barrett TG, Mancilla EE, Svensson J, Kester MH, Kuiper GG, Balkassmi S, Uitterlinden AG, Koehrle J, Rodien P, Halestrap AP, Visser TJ (2004) Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet 364(9443):1435–1437. doi:10.1016/S0140-6736(04)17226-7

    Article  CAS  PubMed  Google Scholar 

  14. Dumitrescu AM, Liao XH, Best TB, Brockmann K, Refetoff S (2004) A novel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene. Am J Hum Genet 74(1):168–175. doi:10.1086/380999

    Article  CAS  PubMed  Google Scholar 

  15. Vaurs-Barriere C, Deville M, Sarret C, Giraud G, Des Portes V, Prats-Vinas JM, De Michele G, Dan B, Brady AF, Boespflug-Tanguy O, Touraine R (2009) Pelizaeus-Merzbacher-Like disease presentation of MCT8 mutated male subjects. Ann Neurol 65(1):114–118. doi:10.1002/ana.21579

    Article  CAS  PubMed  Google Scholar 

  16. Armour CM, Kersseboom S, Yoon G, Visser TJ (2015) Further Insights into the Allan-Herndon-Dudley syndrome: clinical and functional characterization of a novel MCT8 mutation. PLoS One 10(10):e0139343. doi:10.1371/journal.pone.0139343

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Tonduti D, Vanderver A, Berardinelli A, Schmidt JL, Collins CD, Novara F, Genni AD, Mita A, Triulzi F, Brunstrom-Hernandez JE, Zuffardi O, Balottin U, Orcesi S (2013) MCT8 deficiency: extrapyramidal symptoms and delayed myelination as prominent features. J Child Neurol 28(6):795–800. doi:10.1177/0883073812450944

    Article  PubMed  Google Scholar 

  18. La Piana R, Vanasse M, Brais B, Bernard G (2015) Myelination delay and Allan-Herndon-Dudley syndrome caused by a novel mutation in the SLC16A2 gene. J Child Neurol 30(10):1371–1374. doi:10.1177/0883073814555189

    Article  PubMed  Google Scholar 

  19. Di Cosmo C, Liao XH, Dumitrescu AM, Philp NJ, Weiss RE, Refetoff S (2010) Mice deficient in MCT8 reveal a mechanism regulating thyroid hormone secretion. J Clin Invest 120(9):3377–3388. doi:10.1172/JCI42113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Mayerl S, Visser TJ, Darras VM, Horn S, Heuer H (2012) Impact of Oatp1c1 deficiency on thyroid hormone metabolism and action in the mouse brain. Endocrinology 153(3):1528–1537. doi:10.1210/en.2011-1633

    Article  CAS  PubMed  Google Scholar 

  21. Roberts LM, Woodford K, Zhou M, Black DS, Haggerty JE, Tate EH, Grindstaff KK, Mengesha W, Raman C, Zerangue N (2008) Expression of the thyroid hormone transporters monocarboxylate transporter-8 (SLC16A2) and organic ion transporter-14 (SLCO1C1) at the blood–brain barrier. Endocrinology 149(12):6251–6261. doi:10.1210/en.2008-0378

    Article  CAS  PubMed  Google Scholar 

  22. Mayerl S, Muller J, Bauer R, Richert S, Kassmann CM, Darras VM, Buder K, Boelen A, Visser TJ, Heuer H (2014) Transporters MCT8 and OATP1C1 maintain murine brain thyroid hormone homeostasis. J Clin Invest 124(5):1987–1999. doi:10.1172/JCI70324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zada D, Tovin A, Lerer-Goldshtein T, Vatine GD, Appelbaum L (2014) Altered behavioral performance and live imaging of circuit-specific neural deficiencies in a zebrafish model for psychomotor retardation. PLoS Genet 10(9):e1004615. doi:10.1371/journal.pgen.1004615

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Mobius W, Patzig J, Nave KA, Werner HB (2008) Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection. Neuron Glia Biol 4(2):111–127. doi:10.1017/S1740925X0900009X

    Article  PubMed  Google Scholar 

  25. Chan SY, Hancox LA, Martin-Santos A, Loubiere LS, Walter MN, Gonzalez AM, Cox PM, Logan A, McCabe CJ, Franklyn JA, Kilby MD (2014) MCT8 expression in human fetal cerebral cortex is reduced in severe intrauterine growth restriction. J Endocrinol 220(2):85–95. doi:10.1530/JOE-13-0400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Jarvis S, Glinianaia SV, Blair E (2006) Cerebral palsy and intrauterine growth. Clin Perinatol 33(2):285–300. doi:10.1016/j.clp.2006.03.009

    Article  PubMed  Google Scholar 

  27. Morton PD, Ishibashi N, Jonas RA, Gallo V (2015) Congenital cardiac anomalies and white matter injury. Trends Neurosci 38(6):353–363. doi:10.1016/j.tins.2015.04.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tolcos M, Bateman E, O’Dowd R, Markwick R, Vrijsen K, Rehn A, Rees S (2011) Intrauterine growth restriction affects the maturation of myelin. Exp Neurol 232(1):53–65. doi:10.1016/j.expneurol.2011.08.002

    Article  CAS  PubMed  Google Scholar 

  29. Reid MV, Murray KA, Marsh ED, Golden JA, Simmons RA, Grinspan JB (2012) Delayed myelination in an intrauterine growth retardation model is mediated by oxidative stress upregulating bone morphogenetic protein 4. J Neuropathol Exp Neurol 71(7):640–653. doi:10.1097/NEN.0b013e31825cfa81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Silbereis JC, Huang EJ, Back SA, Rowitch DH (2010) Towards improved animal models of neonatal white matter injury associated with cerebral palsy. Dis Model Mech 3(11–12):678–688. doi:10.1242/dmm.002915

    Article  PubMed  PubMed Central  Google Scholar 

  31. Lee JY, Kim MJ, Stanley EG, Elefanty AG, Petratos S (2015) Monocarboxylate transporter 8 is expressed on oligodendrocyte progenitors derived from human embryonic stem cells. International Journal of Developmental Neuroscience: the Official Journal of the International Society for Developmental Neuroscience 47 (Pt A):69. doi:10.1016/j.ijdevneu.2015.04.189

  32. Stenman JM, Rajagopal J, Carroll TJ, Ishibashi M, McMahon J, McMahon AP (2008) Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 322(5905):1247–1250. doi:10.1126/science.1164594

    Article  CAS  PubMed  Google Scholar 

  33. Daneman R, Agalliu D, Zhou L, Kuhnert F, Kuo CJ, Barres BA (2009) Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc Natl Acad Sci U S A 106(2):641–646. doi:10.1073/pnas.0805165106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Simonides WS, Mulcahey MA, Redout EM, Muller A, Zuidwijk MJ, Visser TJ, Wassen FW, Crescenzi A, da-Silva WS, Harney J, Engel FB, Obregon MJ, Larsen PR, Bianco AC, Huang SA (2008) Hypoxia-inducible factor induces local thyroid hormone inactivation during hypoxic-ischemic disease in rats. J Clin Invest 118(3):975–983. doi:10.1172/JCI32824

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Vose LR, Vinukonda G, Jo S, Miry O, Diamond D, Korumilli R, Arshad A, Zia MT, Hu F, Kayton RJ, La Gamma EF, Bansal R, Bianco AC, Ballabh P (2013) Treatment with thyroxine restores myelination and clinical recovery after intraventricular hemorrhage. J Neurosci 33(44):17232–17246. doi:10.1523/JNEUROSCI.2713-13.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Fancy SP, Kotter MR, Harrington EP, Huang JK, Zhao C, Rowitch DH, Franklin RJ (2010) Overcoming remyelination failure in multiple sclerosis and other myelin disorders. Exp Neurol 225(1):18–23. doi:10.1016/j.expneurol.2009.12.020

    Article  CAS  PubMed  Google Scholar 

  37. Davies AL, Desai RA, Bloomfield PS, McIntosh PR, Chapple KJ, Linington C, Fairless R, Diem R, Kasti M, Murphy MP, Smith KJ (2013) Neurological deficits caused by tissue hypoxia in neuroinflammatory disease. Ann Neurol 74(6):815–825. doi:10.1002/ana.24006

    Article  CAS  PubMed  Google Scholar 

  38. Gereben B, Zavacki AM, Ribich S, Kim BW, Huang SA, Simonides WS, Zeold A, Bianco AC (2008) Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev 29(7):898–938. doi:10.1210/er.2008-0019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Bernal J (2007) Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab 3(3):249–259. doi:10.1038/ncpendmet0424

    Article  CAS  PubMed  Google Scholar 

  40. Kaplan MM, McCann UD, Yaskoski KA, Larsen PR, Leonard JL (1981) Anatomical distribution of phenolic and tyrosyl ring iodothyronine deiodinases in the nervous system of normal and hypothyroid rats. Endocrinology 109(2):397–402. doi:10.1210/endo-109-2-397

    Article  CAS  PubMed  Google Scholar 

  41. Kaplan MM, Yaskoski KA (1980) Phenolic and tyrosyl ring deiodination of iodothyronines in rat brain homogenates. J Clin Invest 66(3):551–562. doi:10.1172/JCI109887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Courtin F, Zrouri H, Lamirand A, Li WW, Mercier G, Schumacher M, Goascogne CL, Pierre M (2005) Thyroid hormone deiodinases in the central and peripheral nervous system. Thyroid 15(8):931–942. doi:10.1089/thy.2005.15.931

    Article  CAS  PubMed  Google Scholar 

  43. Guadano-Ferraz A, Obregon 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 U S A 94(19):10391–10396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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(8):3359–3368. doi:10.1210/endo.138.8.5318

    Article  CAS  PubMed  Google Scholar 

  45. 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(2):784–790. doi:10.1210/endo.140.2.6486

    Article  CAS  PubMed  Google Scholar 

  46. Mottis A, Mouchiroud L, Auwerx J (2013) Emerging roles of the corepressors NCoR1 and SMRT in homeostasis. Genes Dev 27(8):819–835. doi:10.1101/gad.214023.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hermanson O, Jepsen K, Rosenfeld MG (2002) N-CoR controls differentiation of neural stem cells into astrocytes. Nature 419(6910):934–939. doi:10.1038/nature01156

    Article  CAS  PubMed  Google Scholar 

  48. Jepsen K, Solum D, Zhou T, McEvilly RJ, Kim HJ, Glass CK, Hermanson O, Rosenfeld MG (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450(7168):415–419. doi:10.1038/nature06270

    Article  CAS  PubMed  Google Scholar 

  49. Castelo-Branco G, Lilja T, Wallenborg K, Falcao AM, Marques SC, Gracias A, Solum D, Paap R, Walfridsson J, Teixeira AI, Rosenfeld MG, Jepsen K, Hermanson O (2014) Neural stem cell differentiation is dictated by distinct actions of nuclear receptor corepressors and histone deacetylases. Stem Cell Reports 3(3):502–515. doi:10.1016/j.stemcr.2014.07.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yang XJ, Seto E (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9(3):206–218. doi:10.1038/nrm2346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wang J, Weaver IC, Gauthier-Fisher A, Wang H, He L, Yeomans J, Wondisford F, Kaplan DR, Miller FD (2010) CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev Cell 18(1):114–125. doi:10.1016/j.devcel.2009.10.023

    Article  CAS  PubMed  Google Scholar 

  52. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12(7):829–838. doi:10.1038/nn.2333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lopez-Juarez A, Remaud S, Hassani Z, Jolivet P, Pierre Simons J, Sontag T, Yoshikawa K, Price J, Morvan-Dubois G, Demeneix BA (2012) Thyroid hormone signaling acts as a neurogenic switch by repressing Sox2 in the adult neural stem cell niche. Cell Stem Cell 10(5):531–543. doi:10.1016/j.stem.2012.04.008

    Article  CAS  PubMed  Google Scholar 

  54. Lemkine GF, Raj A, Alfama G, Turque N, Hassani Z, Alegria-Prevot O, Samarut J, Levi G, Demeneix BA (2005) Adult neural stem cell cycling in vivo requires thyroid hormone and its alpha receptor. Faseb J 19(7):863–865. doi:10.1096/fj.04-2916fje

    CAS  PubMed  Google Scholar 

  55. Carlson DJ, Strait KA, Schwartz HL, Oppenheimer JH (1994) Immunofluorescent localization of thyroid hormone receptor isoforms in glial cells of rat brain. Endocrinology 135(5):1831–1836. doi:10.1210/endo.135.5.7525253

    Article  CAS  PubMed  Google Scholar 

  56. Baas D, Fressinaud C, Ittel ME, Reeber A, Dalencon D, Puymirat J, Sarlieve LL (1994) Expression of thyroid hormone receptor isoforms in rat oligodendrocyte cultures. Effect of 3,5,3′-triiodo-l-thyronine. Neurosci Lett 176(1):47–51

    Article  CAS  PubMed  Google Scholar 

  57. Billon N, Tokumoto Y, Forrest D, Raff M (2001) Role of thyroid hormone receptors in timing oligodendrocyte differentiation. Dev Biol 235(1):110–120. doi:10.1006/dbio.2001.0293

    Article  CAS  PubMed  Google Scholar 

  58. 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(23):6452–6460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Sarlieve LL, Rodriguez-Pena A, Langley K (2004) Expression of thyroid hormone receptor isoforms in the oligodendrocyte lineage. Neurochem Res 29(5):903–922

    Article  CAS  PubMed  Google Scholar 

  60. Baas D, Puymirat J, Sarlieve LL (1998) Posttranscriptional regulation of oligodendroglial thyroid hormone (T3) receptor beta 1 by T3. Int J Dev Neurosci 16(6):461–467

    Article  CAS  PubMed  Google Scholar 

  61. Bury F, Carre JL, Vega S, Ghandour MS, Rodriguez-Pena A, Langley K, Sarlieve LL (2002) Coexpression of thyroid hormone receptor isoforms in mouse oligodendrocytes. J Neurosci Res 67(1):106–113

    Article  CAS  PubMed  Google Scholar 

  62. Strait KA, Carlson DJ, Schwartz HL, Oppenheimer JH (1997) Transient stimulation of myelin basic protein gene expression in differentiating cultured oligodendrocytes: a model for 3,5,3′-triiodothyronine-induced brain development. Endocrinology 138(2):635–641. doi:10.1210/endo.138.2.4946

    Article  CAS  PubMed  Google Scholar 

  63. Rodriguez-Pena A (1999) Oligodendrocyte development and thyroid hormone. J Neurobiol 40(4):497–512

    Article  CAS  PubMed  Google Scholar 

  64. Baas D, Legrand C, Samarut J, Flamant F (2002) Persistence of oligodendrocyte precursor cells and altered myelination in optic nerve associated to retina degeneration in mice devoid of all thyroid hormone receptors. Proc Natl Acad Sci U S A 99(5):2907–2911. doi:10.1073/pnas.052482299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Flamant F, Gauthier K (2013) Thyroid hormone receptors: the challenge of elucidating isotype-specific functions and cell-specific response. Biochim Biophys Acta 1830(7):3900–3907. doi:10.1016/j.bbagen.2012.06.003

    Article  CAS  PubMed  Google Scholar 

  66. Picou F, Fauquier T, Chatonnet F, Flamant F (2012) A bimodal influence of thyroid hormone on cerebellum oligodendrocyte differentiation. Mol Endocrinol 26(4):608–618. doi:10.1210/me.2011-1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Dong H, Yauk CL, Rowan-Carroll A, You SH, Zoeller RT, Lambert I, Wade MG (2009) Identification of thyroid hormone receptor binding sites and target genes using ChIP-on-chip in developing mouse cerebellum. PLoS One 4(2):e4610. doi:10.1371/journal.pone.0004610

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Dudazy-Gralla S, Nordstrom K, Hofmann PJ, Meseh DA, Schomburg L, Vennstrom B, Mittag J (2013) Identification of thyroid hormone response elements in vivo using mice expressing a tagged thyroid hormone receptor alpha1. Biosci Rep 33(2):e00027. doi:10.1042/BSR20120124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Bass J, Muirhead S (2000) Radiological case of the month. Pyriform sinus fistula to the left lobe of the thyroid. Arch Pediatr Adolesc Med 154(5):523–524

    Article  CAS  PubMed  Google Scholar 

  70. Brent GA, Williams GR, Harney JW, Forman BM, Samuels HH, Moore DD, Larsen PR (1991) Effects of varying the position of thyroid hormone response elements within the rat growth hormone promoter: implications for positive and negative regulation by 3,5,3′-triiodothyronine. Mol Endocrinol 5(4):542–548. doi:10.1210/mend-5-4-542

    Article  CAS  PubMed  Google Scholar 

  71. Pombo PM, Barettino D, Ibarrola N, Vega S, Rodriguez-Pena A (1999) Stimulation of the myelin basic protein gene expression by 9-cis-retinoic acid and thyroid hormone: activation in the context of its native promoter. Brain Res Mol Brain Res 64(1):92–100

    Article  CAS  PubMed  Google Scholar 

  72. Hall MG, Quignodon L, Desvergne B (2008) Peroxisome proliferator-activated receptor beta/delta in the brain: facts and hypothesis. PPAR Res 2008:780452. doi:10.1155/2008/780452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Baas D, Prufer K, Ittel ME, Kuchler-Bopp S, Labourdette G, Sarlieve LL, Brachet P (2000) Rat oligodendrocytes express the vitamin D(3) receptor and respond to 1,25-dihydroxyvitamin D(3). Glia 31(1):59–68

    Article  CAS  PubMed  Google Scholar 

  74. Hsu JH, Zavacki AM, Harney JW, Brent GA (1995) Retinoid-X receptor (RXR) differentially augments thyroid hormone response in cell lines as a function of the response element and endogenous RXR content. Endocrinology 136(2):421–430. doi:10.1210/endo.136.2.7835272

    Article  CAS  PubMed  Google Scholar 

  75. Kakizawa T, Miyamoto T, Kaneko A, Yajima H, Ichikawa K, Hashizume K (1997) Ligand-dependent heterodimerization of thyroid hormone receptor and retinoid X receptor. J Biol Chem 272(38):23799–23804

    Article  CAS  PubMed  Google Scholar 

  76. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, Kagechika H, Bauer J, Zhao C, Evercooren AB, Chambon P, Ffrench-Constant C, Franklin RJ (2011) Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 14(1):45–53. doi:10.1038/nn.2702

    Article  CAS  PubMed  Google Scholar 

  77. Stacpoole SR, Spitzer S, Bilican B, Compston A, Karadottir R, Chandran S, Franklin RJ (2013) High yields of oligodendrocyte lineage cells from human embryonic stem cells at physiological oxygen tensions for evaluation of translational biology. Stem cell reports 1(5):437–450. doi:10.1016/j.stemcr.2013.09.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Baxi EG, Schott JT, Fairchild AN, Kirby LA, Karani R, Uapinyoying P, Pardo-Villamizar C, Rothstein JR, Bergles DE, Calabresi PA (2014) A selective thyroid hormone beta receptor agonist enhances human and rodent oligodendrocyte differentiation. Glia 62(9):1513–1529. doi:10.1002/glia.22697

    Article  PubMed  PubMed Central  Google Scholar 

  79. Cao X, Kambe F, Moeller LC, Refetoff S, Seo H (2005) Thyroid hormone induces rapid activation of Akt/protein kinase B-mammalian target of rapamycin-p70S6K cascade through phosphatidylinositol 3-kinase in human fibroblasts. Mol Endocrinol 19(1):102–112. doi:10.1210/me.2004-0093

    Article  CAS  PubMed  Google Scholar 

  80. Bergh JJ, Lin HY, Lansing L, Mohamed SN, Davis FB, Mousa S, Davis PJ (2005) Integrin alphaVbeta3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 146(7):2864–2871. doi:10.1210/en.2005-0102

    Article  CAS  PubMed  Google Scholar 

  81. Lin HY, Sun M, Tang HY, Lin C, Luidens MK, Mousa SA, Incerpi S, Drusano GL, Davis FB, Davis PJ (2009) l-Thyroxine vs. 3,5,3′-triiodo-l-thyronine and cell proliferation: activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase. Am J Physiol Cell Physiol 296(5):C980–991. doi:10.1152/ajpcell.00305.2008

    Article  CAS  PubMed  Google Scholar 

  82. Martin NP, Marron Fernandez de Velasco E, Mizuno F, Scappini EL, Gloss B, Erxleben C, Williams JG, Stapleton HM, Gentile S, Armstrong DL (2014) A rapid cytoplasmic mechanism for PI3 kinase regulation by the nuclear thyroid hormone receptor, TRbeta, and genetic evidence for its role in the maturation of mouse hippocampal synapses in vivo. Endocrinology 155(9):3713–3724. doi:10.1210/en.2013-2058

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Cao HJ, Lin HY, Luidens MK, Davis FB, Davis PJ (2009) Cytoplasm-to-nucleus shuttling of thyroid hormone receptor-beta1 (Trbeta1) is directed from a plasma membrane integrin receptor by thyroid hormone. Endocr Res 34(1–2):31–42. doi:10.1080/07435800902911810

    PubMed  Google Scholar 

  84. Flores AI, Narayanan SP, Morse EN, Shick HE, Yin X, Kidd G, Avila RL, Kirschner DA, Macklin WB (2008) Constitutively active Akt induces enhanced myelination in the CNS. J Neurosci 28(28):7174–7183. doi:10.1523/JNEUROSCI.0150-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Harrington EP, Zhao C, Fancy SP, Kaing S, Franklin RJ, Rowitch DH (2010) Oligodendrocyte PTEN is required for myelin and axonal integrity, not remyelination. Ann Neurol 68(5):703–716. doi:10.1002/ana.22090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Milner R, Ffrench-Constant C (1994) A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development 120(12):3497–3506

    CAS  PubMed  Google Scholar 

  87. Blaschuk KL, Frost EE, ffrench-Constant C (2000) The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins. Development 127(9):1961–1969

    CAS  PubMed  Google Scholar 

  88. Baron W, Shattil SJ, ffrench-Constant C (2002) The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. Embo J 21(8):1957–1966. doi:10.1093/emboj/21.8.1957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Baas D, Bourbeau D, Sarlieve LL, Ittel ME, Dussault JH, Puymirat J (1997) Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia 19(4):324–332

    Article  CAS  PubMed  Google Scholar 

  90. Tokumoto YM, Durand B, Raff MC (1999) An analysis of the early events when oligodendrocyte precursor cells are triggered to differentiate by thyroid hormone, retinoic acid, or PDGF withdrawal. Dev Biol 213(2):327–339. doi:10.1006/dbio.1999.9397

    Article  CAS  PubMed  Google Scholar 

  91. Alsanie WF, Niclis JC, Petratos S (2013) Human embryonic stem cell-derived oligodendrocytes: protocols and perspectives. Stem Cells Dev 22(18):2459–2476. doi:10.1089/scd.2012.0520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Liu X, Li Y, Zhang Y, Lu Y, Guo W, Liu P, Zhou J, Xiang Z, He C (2011) SHP-2 promotes the maturation of oligodendrocyte precursor cells through Akt and ERK1/2 signaling in vitro. PLoS One 6(6):e21058. doi:10.1371/journal.pone.0021058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Ehrman LA, Nardini D, Ehrman S, Rizvi TA, Gulick J, Krenz M, Dasgupta B, Robbins J, Ratner N, Nakafuku M, Waclaw RR (2014) The protein tyrosine phosphatase Shp2 is required for the generation of oligodendrocyte progenitor cells and myelination in the mouse telencephalon. J Neurosci 34(10):3767–3778. doi:10.1523/JNEUROSCI.3515-13.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Davis PJ, Davis FB, Blas SD (1982) Studies on the mechanism of thyroid hormone stimulation in vitro of human red cell Ca2+−ATPase activity. Life Sci 30(7–8):675–682

    Article  CAS  PubMed  Google Scholar 

  95. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW (2000) Ligand binding to integrins. J Biol Chem 275(29):21785–21788. doi:10.1074/jbc.R000003200

    Article  CAS  PubMed  Google Scholar 

  96. Rowitch DH, Kriegstein AR (2010) Developmental genetics of vertebrate glial-cell specification. Nature 468(7321):214–222. doi:10.1038/nature09611

    Article  CAS  PubMed  Google Scholar 

  97. Hasebe M, Ohta E, Imagawa T, Uehara M (2008) Expression of sonic hedgehog regulates morphological changes of rat developing cerebellum in hypothyroidism. J Toxicol Sci 33(4):473–477

    Article  CAS  PubMed  Google Scholar 

  98. Desouza LA, Sathanoori M, Kapoor R, Rajadhyaksha N, Gonzalez LE, Kottmann AH, Tole S, Vaidya VA (2011) Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult Mammalian brain. Endocrinology 152(5):1989–2000. doi:10.1210/en.2010-1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Freitas BC, Gereben B, Castillo M, Kallo I, Zeold A, Egri P, Liposits Z, Zavacki AM, Maciel RM, Jo S, Singru P, Sanchez E, Lechan RM, Bianco AC (2010) Paracrine signaling by glial cell-derived triiodothyronine activates neuronal gene expression in the rodent brain and human cells. J Clin Invest 120(6):2206–2217. doi:10.1172/JCI41977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Fernandez M, Pirondi S, Manservigi M, Giardino L, Calza L (2004) Thyroid hormone participates in the regulation of neural stem cells and oligodendrocyte precursor cells in the central nervous system of adult rat. Eur J Neurosci 20(8):2059–2070. doi:10.1111/j.1460-9568.2004.03664.x

    Article  CAS  PubMed  Google Scholar 

  101. Orentas DM, Hayes JE, Dyer KL, Miller RH (1999) Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development 126(11):2419–2429

    CAS  PubMed  Google Scholar 

  102. Alves C, Eidson M, Engle H, Sheldon J, Cleveland WW (1989) Changes in brain maturation detected by magnetic resonance imaging in congenital hypothyroidism. J Pediatr 115(4):600–603

    Article  CAS  PubMed  Google Scholar 

  103. Gupta RK, Bhatia V, Poptani H, Gujral RB (1995) Brain metabolite changes on in vivo proton magnetic resonance spectroscopy in children with congenital hypothyroidism. J Pediatr 126(3):389–392

    Article  CAS  PubMed  Google Scholar 

  104. Jagannathan NR, Tandon N, Raghunathan P, Kochupillai N (1998) Reversal of abnormalities of myelination by thyroxine therapy in congenital hypothyroidism: localized in vivo proton magnetic resonance spectroscopy (MRS) study. Brain Res Dev Brain Res 109(2):179–186

    Article  CAS  PubMed  Google Scholar 

  105. Barres BA, Lazar MA, Raff MC (1994) A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120(5):1097–1108

    CAS  PubMed  Google Scholar 

  106. Nygard M, Wahlstrom GM, Gustafsson MV, Tokumoto YM, Bondesson M (2003) Hormone-dependent repression of the E2F-1 gene by thyroid hormone receptors. Mol Endocrinol 17(1):79–92. doi:10.1210/me.2002-0107

    Article  CAS  PubMed  Google Scholar 

  107. 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(3):812–818. doi:10.1172/JCI116301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Ibarrola N, Rodriguez-Pena A (1997) Hypothyroidism coordinately and transiently affects myelin protein gene expression in most rat brain regions during postnatal development. Brain Res 752(1–2):285–293

    Article  CAS  PubMed  Google Scholar 

  109. Barradas PC, Vieira RS, De Freitas MS (2001) Selective effect of hypothyroidism on expression of myelin markers during development. J Neurosci Res 66(2):254–261

    Article  CAS  PubMed  Google Scholar 

  110. Farsetti A, Desvergne B, Hallenbeck P, Robbins J, Nikodem VM (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(22):15784–15788

    CAS  PubMed  Google Scholar 

  111. Lalonde R, Strazielle C (2007) Brain regions and genes affecting postural control. Prog Neurobiol 81(1):45–60. doi:10.1016/j.pneurobio.2006.11.005

    Article  CAS  PubMed  Google Scholar 

  112. Martel J, Cayrou C, Puymirat J (2002) Identification of new thyroid hormone-regulated genes in rat brain neuronal cultures. Neuroreport 13(15):1849–1851

    Article  CAS  PubMed  Google Scholar 

  113. Cayrou C, Denver RJ, Puymirat J (2002) Suppression of the basic transcription element-binding protein in brain neuronal cultures inhibits thyroid hormone-induced neurite branching. Endocrinology 143(6):2242–2249. doi:10.1210/endo.143.6.8856

    Article  CAS  PubMed  Google Scholar 

  114. Denver RJ, Williamson KE (2009) Identification of a thyroid hormone response element in the mouse Kruppel-like factor 9 gene to explain its postnatal expression in the brain. Endocrinology 150(8):3935–3943. doi:10.1210/en.2009-0050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Moore DL, Blackmore MG, Hu Y, Kaestner KH, Bixby JL, Lemmon VP, Goldberg JL (2009) KLF family members regulate intrinsic axon regeneration ability. Science 326(5950):298–301. doi:10.1126/science.1175737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Avci HX, Lebrun C, Wehrle R, Doulazmi M, Chatonnet F, Morel MP, Ema M, Vodjdani G, Sotelo C, Flamant F, Dusart I (2012) Thyroid hormone triggers the developmental loss of axonal regenerative capacity via thyroid hormone receptor alpha1 and kruppel-like factor 9 in Purkinje cells. Proc Natl Acad Sci U S A 109(35):14206–14211. doi:10.1073/pnas.1119853109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Haas MJ, Mreyoud A, Fishman M, Mooradian AD (2004) Microarray analysis of thyroid hormone-induced changes in mRNA expression in the adult rat brain. Neurosci Lett 365(1):14–18. doi:10.1016/j.neulet.2004.04.028

    Article  CAS  PubMed  Google Scholar 

  118. Jo S, Kallo I, Bardoczi Z, Arrojo e Drigo R, Zeold A, Liposits Z, Oliva A, Lemmon VP, Bixby JL, Gereben B, Bianco AC (2012) Neuronal hypoxia induces Hsp40-mediated nuclear import of type 3 deiodinase as an adaptive mechanism to reduce cellular metabolism. J Neurosci 32(25):8491–8500. doi:10.1523/JNEUROSCI.6514-11.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Fuss B, Baba H, Phan T, Tuohy VK, Macklin WB (1997) Phosphodiesterase I, a novel adhesion molecule and/or cytokine involved in oligodendrocyte function. J Neurosci 17(23):9095–9103

    CAS  PubMed  Google Scholar 

  120. Fox MA, Colello RJ, Macklin WB, Fuss B (2003) Phosphodiesterase-Ialpha/autotaxin: a counteradhesive protein expressed by oligodendrocytes during onset of myelination. Mol Cell Neurosci 23(3):507–519

    Article  CAS  PubMed  Google Scholar 

  121. Dennis J, White MA, Forrest AD, Yuelling LM, Nogaroli L, Afshari FS, Fox MA, Fuss B (2008) Phosphodiesterase-Ialpha/autotaxin’s MORFO domain regulates oligodendroglial process network formation and focal adhesion organization. Mol Cell Neurosci 37(2):412–424. doi:10.1016/j.mcn.2007.10.018

    Article  CAS  PubMed  Google Scholar 

  122. Wheeler NA, Lister JA, Fuss B (2015) The autotaxin-lysophosphatidic acid axis modulates histone acetylation and gene expression during oligodendrocyte differentiation. J Neurosci 35(32):11399–11414. doi:10.1523/JNEUROSCI.0345-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Mosser J, Douar AM, Sarde CO, Kioschis P, Feil R, Moser H, Poustka AM, Mandel JL, Aubourg P (1993) Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361(6414):726–730. doi:10.1038/361726a0

    Article  CAS  PubMed  Google Scholar 

  124. Fouquet F, Zhou JM, Ralston E, Murray K, Troalen F, Magal E, Robain O, Dubois-Dalcq M, Aubourg P (1997) Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system. Neurobiol Dis 3(4):271–285. doi:10.1006/nbdi.1997.0127

    Article  CAS  PubMed  Google Scholar 

  125. Moser HW, Mahmood A, Raymond GV (2007) X-linked adrenoleukodystrophy. Nat Clin Pract Neurol 3(3):140–151. doi:10.1038/ncpneuro0421

    Article  PubMed  Google Scholar 

  126. Hein S, Schonfeld P, Kahlert S, Reiser G (2008) Toxic effects of X-linked adrenoleukodystrophy-associated, very long chain fatty acids on glial cells and neurons from rat hippocampus in culture. Hum Mol Genet 17(12):1750–1761. doi:10.1093/hmg/ddn066

    Article  CAS  PubMed  Google Scholar 

  127. Kemp S, Wei HM, Lu JF, Braiterman LT, McGuinness MC, Moser AB, Watkins PA, Smith KD (1998) Gene redundancy and pharmacological gene therapy: implications for X-linked adrenoleukodystrophy. Nat Med 4(11):1261–1268. doi:10.1038/3242

    Article  CAS  PubMed  Google Scholar 

  128. Pai GS, Khan M, Barbosa E, Key LL, Craver JR, Cure JK, Betros R, Singh I (2000) Lovastatin therapy for X-linked adrenoleukodystrophy: clinical and biochemical observations on 12 patients. Mol Genet Metab 69(4):312–322

    Article  CAS  PubMed  Google Scholar 

  129. Jang J, Kang HC, Kim HS, Kim JY, Huh YJ, Kim DS, Yoo JE, Lee JA, Lim B, Lee J, Yoon TM, Park IH, Hwang DY, Daley GQ, Kim DW (2011) Induced pluripotent stem cell models from X-linked adrenoleukodystrophy patients. Ann Neurol 70(3):402–409. doi:10.1002/ana.22486

    Article  PubMed  Google Scholar 

  130. Fourcade S, Savary S, Gondcaille C, Berger J, Netik A, Cadepond F, El Etr M, Molzer B, Bugaut M (2003) Thyroid hormone induction of the adrenoleukodystrophy-related gene (ABCD2). Mol Pharmacol 63(6):1296–1303. doi:10.1124/mol.63.6.1296

    Article  CAS  PubMed  Google Scholar 

  131. Weinhofer I, Kunze M, Rampler H, Forss-Petter S, Samarut J, Plateroti M, Berger J (2008) Distinct modulatory roles for thyroid hormone receptors TRalpha and TRbeta in SREBP1-activated ABCD2 expression. Eur J Cell Biol 87(12):933–945. doi:10.1016/j.ejcb.2008.08.002

    Article  CAS  PubMed  Google Scholar 

  132. Genin EC, Gondcaille C, Trompier D, Savary S (2009) Induction of the adrenoleukodystrophy-related gene (ABCD2) by thyromimetics. J Steroid Biochem Mol Biol 116(1–2):37–43. doi:10.1016/j.jsbmb.2009.04.006

    Article  CAS  PubMed  Google Scholar 

  133. Kassmann CM (2014) Myelin peroxisomes—essential organelles for the maintenance of white matter in the nervous system. Biochimie 98:111–118. doi:10.1016/j.biochi.2013.09.020

    Article  CAS  PubMed  Google Scholar 

  134. Kassmann CM, Lappe-Siefke C, Baes M, Brugger B, Mildner A, Werner HB, Natt O, Michaelis T, Prinz M, Frahm J, Nave KA (2007) Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat Genet 39(8):969–976. doi:10.1038/ng2070

    Article  CAS  PubMed  Google Scholar 

  135. Calza L, Fernandez M, Giuliani A, Aloe L, Giardino L (2002) Thyroid hormone activates oligodendrocyte precursors and increases a myelin-forming protein and NGF content in the spinal cord during experimental allergic encephalomyelitis. Proc Natl Acad Sci U S A 99(5):3258–3263. doi:10.1073/pnas.052704499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Fernandez M, Paradisi M, Del Vecchio G, Giardino L, Calza L (2009) Thyroid hormone induces glial lineage of primary neurospheres derived from non-pathological and pathological rat brain: implications for remyelination-enhancing therapies. Int J Dev Neurosci 27(8):769–778. doi:10.1016/j.ijdevneu.2009.08.011

    Article  CAS  PubMed  Google Scholar 

  137. D’Intino G, Lorenzini L, Fernandez M, Taglioni A, Perretta G, Del Vecchio G, Villoslada P, Giardino L, Calza L (2011) Triiodothyronine administration ameliorates the demyelination/remyelination ratio in a non-human primate model of multiple sclerosis by correcting tissue hypothyroidism. J Neuroendocrinol 23(9):778–790. doi:10.1111/j.1365-2826.2011.02181.x

    Article  PubMed  CAS  Google Scholar 

  138. Franco PG, Silvestroff L, Soto EF, Pasquini JM (2008) Thyroid hormones promote differentiation of oligodendrocyte progenitor cells and improve remyelination after cuprizone-induced demyelination. Exp Neurol 212(2):458–467. doi:10.1016/j.expneurol.2008.04.039

    Article  CAS  PubMed  Google Scholar 

  139. Harsan LA, Steibel J, Zaremba A, Agin A, Sapin R, Poulet P, Guignard B, Parizel N, Grucker D, Boehm N, Miller RH, Ghandour MS (2008) Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J Neurosci 28(52):14189–14201. doi:10.1523/JNEUROSCI.4453-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Silvestroff L, Bartucci S, Pasquini J, Franco P (2012) Cuprizone-induced demyelination in the rat cerebral cortex and thyroid hormone effects on cortical remyelination. Exp Neurol 235(1):357–367. doi:10.1016/j.expneurol.2012.02.018

    Article  CAS  PubMed  Google Scholar 

  141. Castelo-Branco G, Stridh P, Guerreiro-Cacais AO, Adzemovic MZ, Falcao AM, Marta M, Berglund R, Gillett A, Hamza KH, Lassmann H, Hermanson O, Jagodic M (2014) Acute treatment with valproic acid and l-thyroxine ameliorates clinical signs of experimental autoimmune encephalomyelitis and prevents brain pathology in DA rats. Neurobiol Dis 71:220–233. doi:10.1016/j.nbd.2014.08.019

    Article  CAS  PubMed  Google Scholar 

  142. Hung PL, Huang CC, Huang HM, Tu DG, Chang YC (2013) Thyroxin treatment protects against white matter injury in the immature brain via brain-derived neurotrophic factor. Stroke 44(8):2275–2283. doi:10.1161/STROKEAHA.113.001552

    Article  CAS  PubMed  Google Scholar 

  143. McLachlan SM, Rapoport B (2014) Breaking tolerance to thyroid antigens: changing concepts in thyroid autoimmunity. Endocr Rev 35(1):59–105. doi:10.1210/er.2013-1055

    Article  CAS  PubMed  Google Scholar 

  144. Nakano A, Watanabe M, Iida T, Kuroda S, Matsuzuka F, Miyauchi A, Iwatani Y (2007) Apoptosis-induced decrease of intrathyroidal CD4(+)CD25(+) regulatory T cells in autoimmune thyroid diseases. Thyroid 17(1):25–31. doi:10.1089/thy.2006.0231

    Article  CAS  PubMed  Google Scholar 

  145. Zambrano A, Garcia-Carpizo V, Gallardo ME, Villamuera R, Gomez-Ferreria MA, Pascual A, Buisine N, Sachs LM, Garesse R, Aranda A (2014) The thyroid hormone receptor beta induces DNA damage and premature senescence. J Cell Biol 204(1):129–146. doi:10.1083/jcb.201305084

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Robbins DS, Shirazi Y, Drysdale BE, Lieberman A, Shin HS, Shin ML (1987) Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J Immunol 139(8):2593–2597

    CAS  PubMed  Google Scholar 

  147. Selmaj KW, Raine CS (1988) Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 23(4):339–346. doi:10.1002/ana.410230405

    Article  CAS  PubMed  Google Scholar 

  148. Andrews T, Zhang P, Bhat NR (1998) TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res 54(5):574–583

    Article  CAS  PubMed  Google Scholar 

  149. Merrill JE (1991) Effects of interleukin-1 and tumor necrosis factor-alpha on astrocytes, microglia, oligodendrocytes, and glial precursors in vitro. Dev Neurosci 13(3):130–137

    Article  CAS  PubMed  Google Scholar 

  150. Boelen A, Kwakkel J, Platvoet-ter Schiphorst M, Baur A, Kohrle J, Wiersinga WM (2004) Contribution of interleukin-12 to the pathogenesis of non-thyroidal illness. Horm Metab Res 36(2):101–106. doi:10.1055/s-2004-814219

    Article  CAS  PubMed  Google Scholar 

  151. Schang AL, Van Steenwinckel J, Chevenne D, Alkmark M, Hagberg H, Gressens P, Fleiss B (2014) Failure of thyroid hormone treatment to prevent inflammation-induced white matter injury in the immature brain. Brain Behav Immun 37:95–102. doi:10.1016/j.bbi.2013.11.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Mdzinarishvili A, Sutariya V, Talasila PK, Geldenhuys WJ, Sadana P (2013) Engineering triiodothyronine (T3) nanoparticle for use in ischemic brain stroke. Drug Deliv Transl Res 3(4):309–317. doi:10.1007/s13346-012-0117-8

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

JYL is supported by a Multiple Sclerosis Research Australia Postgraduate Scholarship and the Trish Multiple Sclerosis Research Foundation; SP is supported by a National Multiple Sclerosis Society Project grant (no. RG4398A1/1), an International Progressive Multiple Sclerosis Alliance Challenge award (no. PA0065), and the Trish Multiple Sclerosis Research Foundation administered through the Multiple Sclerosis Research Australia Project grant (no. 15-022).

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Lee, J.Y., Petratos, S. Thyroid Hormone Signaling in Oligodendrocytes: from Extracellular Transport to Intracellular Signal. Mol Neurobiol 53, 6568–6583 (2016). https://doi.org/10.1007/s12035-016-0013-1

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