Thyroid hormone regulated genes in cerebral cortex development

Journal of Endocrinology

Volumn 232, Issue 2, 2017, Pages R83-R97

  Bernal, Juan ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Brain; Development; Fetus; Gene expression; Metabolism; Thyroid hormone

Indexed keywords

LIOTHYRONINE; SCLEROPROTEIN; THYROID HORMONE; THYROID HORMONE RECEPTOR;

BRAIN CELL; BRAIN CORTEX; BRAIN CORTEX LAYER; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CAJAL RETZIUS CELL; CELL MIGRATION; DEIODINATION; FETUS DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; GENETIC CODE; GENETIC TRANSCRIPTION; GLIA CELL; HORMONE SENSITIVITY; HORMONE TRANSPORT; HUMAN; NERVE PROJECTION; NONHUMAN; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; REVIEW; SECOND TRIMESTER PREGNANCY; SIGNAL TRANSDUCTION; SUBPLATE NEURON; THYROID HORMONE BLOOD LEVEL; THYROID HORMONE METABOLISM; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CEREBRAL CORTEX; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HUMANS; NEURONS; RECEPTORS, THYROID HORMONE; THYROID HORMONES;

EID: 85012024582     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-16-0424     Document Type: Review

References (97)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR & Begley DJ 2010 Structure and function of the blood-brain barrier. Neurobiology Disease 37 13-25. (doi:10.1016/j.nbd.2009.07.030)
2. Alvarez-Dolado M, Ruiz M, Del Rio JA, Alcantara S, Burgaya F, Sheldon M, Nakajima K, Bernal J, Howell BW, Curran T, et al. 1999 Thyroid hormone regulates reelin and dab1 expression during brain development. Journal of Neuroscience 19 6979-6993.
3. Anderson DW, Schray RC, Duester G & Schneider JS 2011 Functional significance of aldehyde dehydrogenase ALDH1A1 to the nigrostriatal dopamine system. Brain Research 1408 81-87. (doi:10.1016/j. brainres.2011.06.051)
4. Baqui M, Botero D, Gereben B, Curcio C, Harney JW, Salvatore D, Sorimachi K, Larsen PR & Bianco AC 2003 Human type 3 iodothyronine selenodeiodinase is located in the plasma membrane and undergoes rapid internalization to endosomes. Journal of Biological Chemistry 278 1206-1211. (doi:10.1074/jbc.M210266200)
5. Barca-Mayo O, Liao XH, Alonso M, Di Cosmo C, Hernandez A, Refetoff S & Weiss RE 2011 Thyroid hormone receptor alpha and regulation of type 3 deiodinase. Molecular Endocrinology 25 575-583. (doi:10.1210/me.2010-0213)
6. Bell MA, Ross AP & Goodman G 2016 Assessing infant cognitive development after prenatal iodine supplementation. American Journal of Clinical Nutrition 104 928S-934S. (doi:10.3945/ajcn.115.110411)
7. Berbel P, Navarro D & Roman GC 2014 An evo-devo approach to thyroid hormones in cerebral and cerebellar cortical development: etiological implications for autism. Frontiers in Endocrinology 5 146. (doi:10.3389/fendo.2014.00146)
8. Berbel P, Auso E, Garcia-Velasco JV, Molina ML & Camacho M 2001 Role of thyroid hormones in the maturation and organisation of rat barrel cortex. Neuroscience 107 383-394. (doi:10.1016/S0306-4522(01)00368-2)
9. Bernal J & Pekonen F 1984 Ontogenesis of the nuclear 3, 5, 3'-triiodothyronine receptor in the human fetal brain. Endocrinology 114 677-679. (doi:10.1210/endo-114-2-677)
10. Bernal J, Guadano-Ferraz A & Morte B 2015 Thyroid hormone transporters-functions and clinical implications. Nature Reviews Endocrinology 11 406-417. (doi:10.1038/nrendo.2015.66)
11. Bianco AC 2011 Minireview: cracking the metabolic code for thyroid hormone signaling. Endocrinology 152 3306-3311. (doi:10.1210/en.2011-1104)
12. Bianco AC, Salvatore D, Gereben B, Berry MJ & Larsen PR 2002 Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocrine Reviews 23 38-89. (doi:10.1210/edrv.23.1.0455)
13. Bradley DJ, Towle HC & Young WS 3rd 1992 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 12 2288-2302.
14. Brown RS 2004 Minireview: developmental regulation of thyrotropin receptor gene expression in the fetal and newborn thyroid. Endocrinology 145 4058-4061. (doi:10.1210/en.2004-0458)
15. Burrow GN, Fisher DA & Larsen PR 1994 Maternal and fetal thyroid function. New England Journal of Medicine 331 1072-1078. (doi:10.1056/NEJM199410203311608)
16. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, et al. 2008 A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. Journal of Neuroscience 28 264-278. (doi:10.1523/JNEUROSCI.4178-07.2008)
17. Calvo RM, Jauniaux E, Gulbis B, Asuncion M, Gervy C, Contempre B & Morreale de Escobar G 2002 Fetal tissues are exposed to biologically relevant free thyroxine concentrations during early phases of development. Journal of Clinical Endocrinology and Metabolism 87 1768-1777. (doi:10.1210/jcem.87.4.8434)
18. Campos-Barros A, Hoell T, Musa A, Sampaolo S, Stoltenburg G, Pinna G, Eravci M, Meinhold H & Baumgartner A 1996 Phenolic and tyrosyl ring iodothyronine deiodination and thyroid hormone concentrations in the human central nervous system. Journal of Clinical Endocrinology and Metabolism 81 2179-2185. (doi:10.1210/jc.81.6.2179)
19. Castelo-Branco G, Lilja T, Wallenborg K, Falcao AM, Marques SC, Gracias A, Solum D, Paap R, Walfridsson J, Teixeira AI, et al. 2014 Neural stem cell differentiation is dictated by distinct actions of nuclear receptor corepressors and histone deacetylases. Stem Cell Reports 3 502-515. (doi:10.1016/j.stemcr.2014.07.008)
20. Ceballos A, Belinchon MM, Sanchez-Mendoza E, Grijota-Martinez C, Dumitrescu AM, Refetoff S, Morte B & Bernal J 2009 Importance of monocarboxylate transporter 8 for the blood-brain barrier-dependent availability of 3, 5, 3'-triiodo-L-thyronine. Endocrinology 150 2491-2496. (doi:10.1210/en.2008-1616)
21. Chan SY, Martin-Santos A, Loubiere LS, Gonzalez AM, Stieger B, Logan A, McCabe CJ, Franklyn JA & Kilby MD 2011 The expression of thyroid hormone transporters in the human fetal cerebral cortex during early development and in N-Tera-2 neurodifferentiation. Journal of Physiology 589 2827-2845. (doi:10.1113/jphysiol.2011.207290)
22. Chantoux F & Francon J 2002 Thyroid hormone regulates the expression of NeuroD/BHF1 during the development of rat cerebellum. Molecular and Cellular Endocrinology 194 157-163. (doi:10.1016/S0303-7207(02)00133-8)
23. Chatonnet F, Guyot R, Benoit G & Flamant F 2013 Genome-wide analysis of thyroid hormone receptors shared and specific functions in neural cells. PNAS 110 E766-E775. (doi:10.1073/pnas.1210626110)
24. de Graaf-Peters VB & Hadders-Algra M 2006 Ontogeny of the human central nervous system: what is happening when? Early Human Development 82 257-266. (doi:10.1016/j.earlhumdev.2005.10.013)
25. 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 1989-2000. (doi:10.1210/en.2010-1396)
26. Dillman AA, Hauser DN, Gibbs JR, Nalls MA, McCoy MK, Rudenko IN, Galter D & Cookson MR 2013 mRNA expression, splicing and editing in the embryonic and adult mouse cerebral cortex. Nature Neuroscience 16 499-506. (doi:10.1038/nn.3332)
27. Dong H, You SH, Williams A, Wade MG, Yauk CL & Thomas Zoeller R 2014 Transient maternal hypothyroxinemia potentiates the transcriptional response to exogenous thyroid hormone in the fetal cerebral cortex before the onset of fetal thyroid function: a messenger and microRNA profiling study. Cerebral Cortex 25 1735-1745. (doi:10.1093/cercor/bht364)
28. Ercan-Fang S, Schwartz HL & Oppenheimer JH 1996 Isoform-specific 3, 5, 3'-triiodothyronine receptor binding capacity and messenger ribonucleic acid content in rat adenohypophysis: effect of thyroidal state and comparison with extrapituitary tissues. Endocrinology 137 3228-3233. (doi:10.1210/en.137.8.3228)
29. Garcia-Fernandez LF, Rausell E, Urade Y, Hayaishi O, Bernal J & Munoz A 1997 Hypothyroidism alters the expression of prostaglandin D2 synthase/beta trace in specific areas of the developing rat brain. European Journal of Neuroscience 9 1566-1573. (doi:10.1111/j.1460-9568.1997.tb01514.x)
30. Gilbert ME, Sui L, Walker MJ, Anderson W, Thomas S, Smoller SN, Schon JP, Phani S & Goodman JH 2007 Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology 148 92-102. (doi:10.1210/en.2006-0164)
31. Gil-Ibanez P, Bernal J & Morte B 2014 Thyroid hormone regulation of gene expression in primary cerebrocortical cells: role of thyroid hormone receptor subtypes and interactions with retinoic acid and glucocorticoids. PLoS ONE 9 e91692. (doi:10.1371/journal. pone.0091692)
32. Gil-Ibanez P, Garcia-Garcia F, Dopazo J, Bernal J & Morte B 2015 Global transcriptome analysis of primary cerebrocortical cells: identification of genes regulated by triiodothyronine in specific cell types. Cerebral Cortex bhv273. (doi:10.1093/cercor/bhv273)
33. Gottschall PE & Howell MD 2015 ADAMTS expression and function in central nervous system injury and disorders. Matrix Biology 44-46 70-76. (doi:10.1016/j.matbio.2015.01.014)
34. Grijota-Martinez C, Diez D, Morreale de Escobar G, Bernal J & Morte B 2011 Lack of action of exogenously administered T3 on the fetal rat brain despite expression of the monocarboxylate transporter 8. Endocrinology 152 1713-1721. (doi:10.1210/en.2010-1014)
35. Guadano-Ferraz A, Escamez MJ, Rausell E & Bernal J 1999 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 19 3430-3439.
36. 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. PNAS 94 10391-10396. (doi:10.1073/pnas.94.19.10391)
37. Guibourdenche J, Noel M, Chevenne D, Vuillard E, Volumenie JL, Polak M, Boissinot C, Porquet D & Luton D 2001 Biochemical investigation of foetal and neonatal thyroid function using the ACS-180SE analyser: clinical application. Annals of Clinical Biochemistry 38 520-526. (doi:10.1177/000456320103800509)
38. Hernandez A, Morte B, Belinchon MM, Ceballos A & Bernal J 2012 Critical role of types 2 and 3 deiodinases in the negative regulation of gene expression by T(3)in the mouse cerebral cortex. Endocrinology 153 2919-2928. (doi:10.1210/en.2011-1905)
39. Hoerder-Suabedissen A & Molnar Z 2013 Molecular diversity of earlyborn subplate neurons. Cerebral Cortex 23 1473-1483. (doi:10.1093/cercor/bhs137)
40. Hoerder-Suabedissen A & Molnar Z 2015 Development, evolution and pathology of neocortical subplate neurons. Nature Reviews Neuroscience 16 133-146. (doi:10.1038/nrn3915)
41. Hoerder-Suabedissen A, Oeschger FM, Krishnan ML, Belgard TG, Wang WZ, Lee S, Webber C, Petretto E, Edwards AD & Molnar Z 2013 Expression profiling of mouse subplate reveals a dynamic gene network and disease association with autism and schizophrenia. PNAS 110 3555-3560. (doi:10.1073/pnas.1218510110)
42. Iskaros J, Pickard M, Evans I, Sinha A, Hardiman P & Ekins R 2000 Thyroid hormone receptor gene expression in first trimester human fetal brain. Journal of Clinical Endocrinology and Metabolism 85 2620-2623. (doi:10.1210/jcem.85.7.6766)
43. Ito K, Uchida Y, Ohtsuki S, Aizawa S, Kawakami H, Katsukura Y, Kamiie J & Terasaki T 2011 Quantitative membrane protein expression at the blood-brain barrier of adult and younger cynomolgus monkeys. Journal of Pharmaceutical Sciences 100 3939-3950. (doi:10.1002/jps.22487)
44. Kaas JH 2006 Evolution of the neocortex. Current Biology 16 R910-R914. (doi:10.1016/j.cub.2006.09.057)
45. Kalyanaraman H, Schwappacher R, Joshua J, Zhuang S, Scott BT, Klos M, Casteel DE, Frangos JA, Dillmann W, Boss GR, et al. 2014 Nongenomic thyroid hormone signaling occurs through a plasma membrane-localized receptor. Science Signaling 7 ra48. (doi:10.1126/scisignal.2004911)
46. Kapoor R, van Hogerlinden M, Wallis K, Ghosh H, Nordstrom K, Vennstrom B & Vaidya VA 2010 Unliganded thyroid hormone receptor alpha1 impairs adult hippocampal neurogenesis. FASEB Journal 24 4793-4805. (doi:10.1096/fj.10-161802)
47. Kester MH, Martinez de Mena R, Obregon MJ, Marinkovic D, Howatson A, Visser TJ, Hume R & Morreale de Escobar G 2004 Iodothyronine levels in the human developing brain: major regulatory roles of iodothyronine deiodinases in different areas. Journal of Clinical Endocrinology and Metabolism 89 3117-3128. (doi:10.1210/jc.2003-031832)
48. Kilby MD, Gittoes N, McCabe C, Verhaeg J & Franklyn JA 2000 Expression of thyroid receptor isoforms in the human fetal central nervous system and the effects of intrauterine growth restriction. Clinical Endocrinology 53 469-477. (doi:10.1046/j.1365-2265.2000.01074.x)
49. Kinne A, Schulein R & Krause G 2011 Primary and secondary thyroid hormone transporters. Thyroid Research 4 (Supplement 1) S7. (doi:10.1186/1756-6614-4-S1-S7)
50. Kurian MA & Jungbluth H 2014 Genetic disorders of thyroid metabolism and brain development. Developmental Medicine and Child Neurology 56 627-634. (doi:10.1111/dmcn.12445)
51. Kyono Y, Subramani A, Ramadoss P, Hollenberg AN, Bonett RM & Denver RJ 2016 Liganded thyroid hormone receptors transactivate the DNA methyltransferase 3a gene in mouse neuronal cells. Endocrinology 157 3647-3657. (doi:10.1210/en.2015-1529)
52. Liu YY & Brent GA 2002 A complex deoxyribonucleic acid response element in the rat Ca(2+)/calmodulin-dependent protein kinase IV gene 5'-flanking region mediates thyroid hormone induction and chicken ovalbumin upstream promoter transcription factor 1 repression. Molecular Endocrinology 16 2439-2451. (doi:10.1210/me.2001-0324)
53. Liu G, Yu J, Ding J, Xie C, Sun L, Rudenko I, Zheng W, Sastry N, Luo J, Rudow G, et al. 2014 Aldehyde dehydrogenase 1 defines and protects a nigrostriatal dopaminergic neuron subpopulation. Journal of Clinical Investigation 124 3032-3046. (doi:10.1172/JCI72176)
54. Lopez-Espindola D, Morales-Bastos C, Grijota-Martinez C, Liao XH, Lev D, Sugo E, Verge CF, Refetoff S, Bernal J & Guadano-Ferraz A 2014 Mutations of the thyroid hormone transporter MCT8 cause prenatal brain damage and persistent hypomyelination. Journal of Clinical Endocrinology and Metabolism 99 E2799-E2804. (doi:10.1210/jc.2014-2162)
55. Lucio RA, Garcia JV, Ramon Cerezo J, Pacheco P, Innocenti GM & Berbel P 1997 The development of auditory callosal connections in normal and hypothyroid rats. Cerebral Cortex 7 303-316. (doi:10.1093/cercor/7.4.303)
56. Luo T, Sakai Y, Wagner E & Drager UC 2006 Retinoids, eye development, and maturation of visual function. Journal of Neurobiology 66 677-686. (doi:10.1002/neu.20239)
57. Maeda N 2015 Proteoglycans and neuronal migration in the cerebral cortex during development and disease. Frontiers in Neuroscience 9 98. (doi:10.3389/fnins.2015.00098)
58. 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. Journal of Clinical Investigation 124 1987-1999. (doi:10.1172/JCI70324)
59. Mellstrom B, Naranjo JR, Santos A, Gonzalez AM & Bernal J 1991 Independent expression of the alpha and beta c-erbA genes in developing rat brain. Molecular Endocrinology 5 1339-1350. (doi:10.1210/mend-5-9-1339)
60. Messier N & Langlois MF 2000 Triac regulation of transcription is T(3) receptor isoform-and response element-specific. Molecular and Cellular Endocrinology 165 57-66. (doi:10.1016/S0303-7207(00)00266-5)
61. Mohan V, Sinha RA, Pathak A, Rastogi L, Kumar P, Pal A & Godbole MM 2012 Maternal thyroid hormone deficiency affects the fetal neocorticogenesis by reducing the proliferating pool, rate of neurogenesis and indirect neurogenesis. Experimental Neurology 237 477-488. (doi:10.1016/j.expneurol.2012.07.019)
62. Moleti M, Trimarchi F, Tortorella G, Candia Longo A, Giorgianni G, Sturniolo G, Alibrandi A & Vermiglio F 2016 Effects of maternal iodine nutrition and thyroid status on cognitive development in offspring: a pilot study. Thyroid 26 296-305. (doi:10.1089/thy.2015.0336)
63. Morte B, Ceballos A, Diez D, Grijota-Martinez C, Dumitrescu AM, Di Cosmo C, Galton VA, Refetoff S & Bernal J 2010 Thyroid hormoneregulated mouse cerebral cortex genes are differentially dependent on the source of the hormone: a study in monocarboxylate transporter-8-and deiodinase-2-deficient mice. Endocrinology 151 2381-2387. (doi:10.1210/en.2009-0944)
64. Mouw JK, Ou G & Weaver VM 2014 Extracellular matrix assembly: a multiscale deconstruction. Nature Reviews Molecular Cell Biology 15 771-785. (doi:10.1038/nrm3902)
65. Navarro D, Alvarado M, Morte B, Berbel D, Sesma J, Pacheco P, Morreale de Escobar G, Bernal J & Berbel P 2014 Late maternal hypothyroidism alters the expression of Camk4 in neocortical subplate neurons: a comparison with Nurr1 labeling. Cerebral Cortex 24 2694-2706. (doi:10.1093/cercor/bht129)
66. Ohtaka-Maruyama C & Okado H 2015 Molecular pathways underlying projection neuron production and migration during cerebral cortical development. Frontiers in Neuroscience 9 447. (doi:10.3389/fnins.2015.00447)
67. Olson EC 2014 Analysis of preplate splitting and early cortical development illuminates the biology of neurological disease. Frontiers in Pediatrics 2 121. (doi:10.3389/fped.2014.00121)
68. O'Rahilly R & Muller F 2008 Significant features in the early prenatal development of the human brain. Annals of Anatomy 190 105-118. (doi:10.1016/j.aanat.2008.01.001)
69. Pardridge WM 1983 Brain metabolism: a perspective from the bloodbrain barrier. Physiological Reviews 63 1481-1535.
70. Perez-Castillo A, Bernal J, Ferreiro B & Pans T 1985 The early ontogenesis of thyroid hormone receptor in the rat fetus. Endocrinology 117 2457-2461. (doi:10.1210/endo-117-6-2457)
71. Rakic P 2009 Evolution of the neocortex: a perspective from developmental biology. Nature Reviews Neuroscience 10 724-735. (doi:10.1038/nrn2719)
72. Refetoff S & Dumitrescu AM 2007 Syndromes of reduced sensitivity to thyroid hormone: genetic defects in hormone receptors, cell transporters and deiodination. Best Practice and Research Clinical Endocrinology and Metabolism 21 277-305. (doi:10.1016/j. beem.2007.03.005)
73. Rice DS & Curran T 2001 Role of the reelin signaling pathway in central nervous system development. Annual Review of Neuroscience 24 1005-1039. (doi:10.1146/annurev.neuro.24.1.1005)
74. 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 bloodbrain barrier. Endocrinology 149 6251-6261. (doi:10.1210/en.2008-0378)
75. Shepard TH 1967 Onset of function in the human fetal thyroid: biochemical and radioautographic studies from organ culture. Journal of Clinical Endocrinology and Metabolism 27 945-958. (doi:10.1210/jcem-27-7-945)
76. Sidman RL & Rakic P 1973 Neuronal migration, with special reference to developing human brain: a review. Brain Research 62 1-35. (doi:10.1016/0006-8993(73)90617-3)
77. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T, et al. 2009 Retinoic acid from the meninges regulates cortical neuron generation. Cell 139 597-609. (doi:10.1016/j.cell.2009.10.004)
78. Smith D, Wagner E, Koul O, McCaffery P & Drager UC 2001 Retinoic acid synthesis for the developing telencephalon. Cerebral Cortex 11 894-905. (doi:10.1093/cercor/11.10.894)
79. Stenzel D, Wilsch-Brauninger M, Wong FK, Heuer H & Huttner WB 2014 Integrin alphavbeta3 and thyroid hormones promote expansion of progenitors in embryonic neocortex. Development 141 795-806. (doi:10.1242/dev.101907)
80. Stohn JP, Martinez ME, Matoin K, Morte B, Bernal J, Galton VA, St Germain D & Hernandez A 2016 MCT8 Deficiency in male mice mitigates the phenotypic abnormalities associated with the absence of a functional type 3 deiodinase. Endocrinology 157 3266-3277. (doi:10.1210/en.2016-1162)
81. Strait KA, Schwartz HL, Perez-Castillo A & Oppenheimer JH 1990 Relationship of c-erbA mRNA content to tissue triiodothyronine nuclear binding capacity and function in developing and adult rats. Journal of Biological Chemistry 265 10514-10521.
82. Takiguchi-Hayashi K, Sekiguchi M, Ashigaki S, Takamatsu M, Hasegawa H, Suzuki-Migishima R, Yokoyama M, Nakanishi S & Tanabe Y 2004 Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. Journal of Neuroscience 24 2286-2295. (doi:10.1523/JNEUROSCI.4671-03.2004)
83. Thorpe-Beeston JG & Nicolaides KH 1993 Fetal thyroid function. Fetal Diagnosis and Therapy 8 60-72. (doi:10.1159/000263749)
84. Thorpe-Beeston JG, Nicolaides KH, Felton CV, Butler J & McGregor AM 1991 Maturation of the secretion of thyroid hormone and thyroidstimulating hormone in the fetus. New England Journal of Medicine 324 532-536. (doi:10.1056/NEJM199102213240805)
85. Toma K & Hanashima C 2015 Switching modes in corticogenesis: mechanisms of neuronal subtype transitions and integration in the cerebral cortex. Frontiers in Neuroscience 9 274. (doi:10.3389/fnins.2015.00274)
86. Toth G, Mazak K, Hosztafi S, Kokosi J & Noszal B 2013 Species-specific lipophilicity of thyroid hormones and their precursors in view of their membrane transport properties. Journal of Pharmaceutical and Biomedical Analysis 76 112-118. (doi:10.1016/j.jpba.2012.12.010)
87. Trajkovic M, Visser TJ, Mittag J, Horn S, Lukas J, Darras VM, Raivich G, Bauer K & Heuer H 2007 Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter 8. Journal of Clinical Investigation 117 627-635. (doi:10.1172/JCI28253)
88. Tu HM, Kim SW, Salvatore D, Bartha T, Legradi G, Larsen PR & Lechan RM 1997 Regional distribution of type 2 thyroxine deiodinase messenger ribonucleic acid in rat hypothalamus and pituitary and its regulation by thyroid hormone. Endocrinology 138 3359-3368. (doi:10.1210/en.138.8.3359)
89. van Gucht AL, Meima ME, Zwaveling-Soonawala N, Visser WE, Fliers E, Wennink JM, Henny C, Visser TJ, Peeters RP & van Trotsenburg AS 2016 Resistance to thyroid hormone alpha in an 18-month-old girl: clinical, therapeutic, and molecular characteristics. Thyroid 26 338-346. (doi:10.1089/thy.2015.0463)
90. van Mullem AA, van Gucht AL, Visser WE, Meima ME, Peeters RP & Visser TJ 2016 Effects of thyroid hormone transporters MCT8 and MCT10 on nuclear activity of T3. Molecular and Cellular Endocrinology 437 252-260. (doi:10.1016/j.mce.2016.07.037)
91. Visser WE, Heemstra KA, Swagemakers SM, Ozgur Z, Corssmit EP, Burggraaf J, van Ijcken WF, van der Spek PJ, Smit JW & Visser TJ 2009 Physiological thyroid hormone levels regulate numerous skeletal muscle transcripts. Journal of Clinical Endocrinology and Metabolism 94 3487-3496. (doi:10.1210/jc.2009-0782)
92. Wagner E, Luo T & Drager UC 2002 Retinoic acid synthesis in the postnatal mouse brain marks distinct developmental stages and functional systems. Cerebral Cortex 12 1244-1253. (doi:10.1093/cercor/12.12.1244)
93. Wallis K, Dudazy S, van Hogerlinden M, Nordstrom K, Mittag J & Vennstrom B 2010 The thyroid hormone receptor alpha1 protein is expressed in embryonic postmitotic neurons and persists in most adult neurons. Molecular Endocrinology 24 1904-1916. (doi:10.1210/me.2010-0175)
94. Yamazaki H, Sekiguchi M, Takamatsu M, Tanabe Y & Nakanishi S 2004 Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis. PNAS 101 14509-14514. (doi:10.1073/pnas.0406295101)
95. Zeisel A, Munoz-Manchado AB, Codeluppi S, Lonnerberg P, La Manno G, Jureus A, Marques S, Munguba H, He L, Betsholtz C, et al. 2015 Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347 1138-1142. (doi:10.1126/science. aaa1934)
96. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O'Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, et al. 2014 An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. Journal of Neuroscience 34 11929-11947. (doi:10.1523/JNEUROSCI.1860-14.2014)
97. Zhang Y, Sloan SA, Clarke LE, Caneda C, Plaza CA, Blumenthal PD, Vogel H, Steinberg GK, Edwards MS, Li G, et al. 2016 Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron 89 37-53. (doi:10.1016/j. neuron.2015.11.013)