Maternal Hypothyroxinemia-Induced Neurodevelopmental Impairments in the Progeny

Molecular Neurobiology

Volumn 53, Issue 3, 2016, Pages 1613-1624

  Min, Hui ^a   Dong, Jing ^a   Wang, Yi ^a   Wang, Yuan ^a   Teng, Weiping ^a   Xi, Qi ^b   Chen, Jie ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Cognition; Hypothyroxinemia; Neurodevelopment; Pregnancy; Psychomotor development

Indexed keywords

ACTIN BINDING PROTEIN; BIOLOGICAL MARKER; ENDOCRINE DISRUPTOR; F ACTIN; HERBICIDE; IODIDE; IODIDE PEROXIDASE; IODINE; LEAD; LIOTHYRONINE; MONOCARBOXYLATE TRANSPORTER 8; MYELIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NITRATE; PERCHLORATE; PHOSPHOPROTEIN PHOSPHATASE 1; POSTSYNAPTIC DENSITY PROTEIN 95; PROPYLTHIOURACIL; PROTEIN C FOS; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SODIUM IODIDE SYMPORTER; THIAMAZOLE; THYROID HORMONE RECEPTOR; THYROID PEROXIDASE ANTIBODY; THYROTROPIN; THYROXINE; THYROXINE BINDING GLOBULIN; TYPE 1 IODOTHYRONINE DEIODINASE; TYPE 2 IODOTHYRONINE DEIODINASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; THYROID HORMONE;

ACTIN FILAMENT; AUTOIMMUNE THYROIDITIS; BRAIN DEVELOPMENT; CEREBELLUM; COGNITIVE DEFECT; COGNITIVE DEVELOPMENT; DEVELOPMENTAL DISORDER; DIETARY INTAKE; DISEASE SEVERITY; EVIDENCE BASED MEDICINE; GENE; HIPPOCAMPUS; HORMONE ACTION; HORMONE METABOLISM; HUMAN; INCIDENCE; IODINATION; IODINE DEFICIENCY; LIOTHYRONINE BLOOD LEVEL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MATERNAL HYPOTHYROXINEMIA; MENTAL DISEASE; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PREGNANCY; PREMATURITY; PROGENY; PROPHYLAXIS; PROTEIN PHOSPHORYLATION; PSYCHOMOTOR DEVELOPMENT; PSYCHOMOTOR DISORDER; PUBLIC HEALTH; RATING SCALE; REVIEW; RISK ASSESSMENT; RISK FACTOR; THYROID DISEASE; THYROID FUNCTION; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; TRALPHA1 GENE; TRANSCRIPTION REGULATION; TRANSIENT HYPOTHYROXINEMIA OF PREMATURITY; TRBETA GENE; BLOOD; BRAIN; COHORT ANALYSIS; DEFICIENCY; EMBRYOLOGY; FEMALE; FORECASTING; INFANT, PREMATURE, DISEASES; NEURODEVELOPMENTAL DISORDERS; NEWBORN; OBSERVATIONAL STUDY; PHYSIOLOGY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE;

BRAIN; COHORT STUDIES; ENDOCRINE DISRUPTORS; FEMALE; FORECASTING; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, PREMATURE, DISEASES; IODINE; NEURODEVELOPMENTAL DISORDERS; OBSERVATIONAL STUDIES AS TOPIC; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; THYROID HORMONES; THYROIDITIS, AUTOIMMUNE; THYROXINE;

EID: 84961125705     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9101-x     Document Type: Review

References (112)

1. Morreale de Escobar G, Obregon MJ, Escobar del Rey F (2000) Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J Clin Endocrinol Metab 85:3975–3987
2. Stagnaro-Green A, Abalovich M, Alexander E, Azizi F, Mestman J, Negro R, Nixon A, Pearce EN et al (2011) Guidelines of the American Thyroid Association for the diagnosis and management of thyroid disease during pregnancy and postpartum. Thyroid 21(10):1081–1125
3. Finken MJ, van Eijsden M, Loomans EM, Vrijkotte TG, Rotteveel J (2013) Maternal hypothyroxinemia in early pregnancy predicts reduced performance in reaction time tests in 5- to 6-year-old offspring. J Clin Endocrinol Metab 98(4):1417–1426
4. Boelaert K, Franklyn JA (2005) Thyroid hormone in health and disease. J Endocrinol 187(1):1–15
5. Pinazo-Durán MD, Pons-Vázquez S, Gallego-Pinazo R, Galbis Estrada C, Zanón-Moreno V, Vila Bou V, Sanz Solana P (2011) Thyroid hormone deficiency disrupts rat eye neurodevelopment. Brain Res 1392:16–26
6. Williams GR (2008) Neurodevelopmental and neurophysiological actions of thyroid hormone. J Neuroendocrinol 20:784–794
7. Bernal J, Guadaño-Ferraz A, Morte B (2003) Perspectives in the study of thyroid hormone action on brain development and function. Thyroid 13(11):1005–1012
8. Cheng SY, Leonard JL, Davis PJ (2010) Molecular aspects of thyroid hormone actions. Endocr Rev 31:139–170
9. Chen C, Zhou Z, Zhong M, Zhang Y, Li M, Zhang L, Qu M, Yang J, et al (2012) Thyroid hormone promotes neuronal differentiation of embryonic neural stem cells by inhibiting STAT3 signaling through TRα1. Stem Cells Dev 21:2667–2681
10. Patel J, Landers K, Li H, Mortimer RH, Richard K (2011) Thyroid hormones and fetal neurological development. J Endocrinol 209:1–8
11. König S, Moura Neto V (2002) Thyroid hormone actions on neural cells. Cell Mol Neurobiol 22(5–6):517–544
12. Ausó E, Lavado-Autric R, Cuevas E, Del Rey FE, Morreale De Escoba G, Berbel P (2004) A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 145:4037–4047
13. Henrichs J, Ghassabian A, Peeters RP, Tiemeier H (2013) Maternal hypothyroxinemia and effects on cognitive functioning in childhood: how and why? Clin Endocrinol (Oxf) 79:152–162
14. Kooistra L, Crawford S, van Baar AL, Brouwers EP, Pop VJ (2006) Neonatal effects of maternal hypothyroxinemia during early pregnancy. Pediatrics 117:161–167
15. Li Y, Shan Z, Teng W, Yu X, Li Y, Fan C, Teng X, Guo R et al (2010) Abnormalities of maternal thyroid function during pregnancy affect neuropsychological development of their children at 25–30 months. Clin Endocrinol (Oxf) 72:825–829
16. Opazo MC, Gianini A, Pancetti F, Azkcona G, Alarcón L, Lizana R, Noches V, Gonzalez PA et al (2008) Maternal hypothyroxinemia impairs spatial learning and synaptic nature and function in the offspring. Endocrinology 149(10):5097–5106
17. Wei W, Wang Y, Wang Y, Dong J, Min H, Song B, Teng W, Xi Q et al (2013) Developmental hypothyroxinemia induced by maternal mild iodine deficiency delays hippocampal axonal growth in the rat offspring. J Neuroendocrinol 25:852–862
18. Wang Y, Wang Y, Dong J, Wei W, Song B, Min H, Teng W, Chen J (2014) Developmental hypothyroxinemia and hypothyroidism limit dendritic growth of cerebellar purkinje cells in rat offspring: involvement of MAP2 and stathmin. Neuropathol Appl Neurobiol 40:398–415
19. Henrichs J, Bongers-Schokking JJ, Schenk JJ, Ghassabian A, Schmidt HG, Visser TJ, Hooijkaas H, de Muinck Keizer-Schrama SM et al (2010) Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the generation R study. J Clin Endocrinol Metab 95(9):4227–4234
20. Suárez-Rodríguez M, Azcona-San Julián C, Alzina de Aguilar V (2012) Hypothyroxinemia during pregnancy: the effect on neurodevelopment in the child. Int J Dev Neurosci 30(6):435–438
21. Moleti M, Lo Presti VP, Mattina F, Mancuso A, De Vivo A, Giorgianni G, Di Bella B, Trimarchi F et al (2009) Gestational thyroid function abnormalities in conditions of mild iodine deficiency: early screening versus continuous monitoring of maternal thyroid status. Eur J Endocrinol 160(4):611–617
22. de Escobar GM, Ares S, Berbel P, Obregón MJ, del Rey FE (2008) The changing role of maternal thyroid hormone in fetal brain development. Semin Perinatol 32(6):380–386
23. Krassas GE, Poppe K, Glinoer D (2010) Thyroid function and human reproductive health. Endocr Rev 31(5):702–755
24. Poppe K, Glinoer D (2003) Thyroid autoimmunity and hypothyroidism before and during pregnancy. Hum Reprod Update 9:149–161
25. Hu X, Teng X, Zheng H, Shan Z, Li J, Jin T, Xiong C, Zhang H et al (2014) Iron deficiency without anemia causes maternal hypothyroxinemia in pregnant rats. Nutr Res 34(7):604–612
26. Vermiglio F, Lo Presti VP, Moleti M, Sidoti M, Tortorella G, Scaffidi G, Castagna MG, Mattina F et al (2004) Attention deficit and hyperactivity disorders in the offspring of mothers exposed to mild-moderate ID: a possible novel ID disorder in developed countries. J Clin Endocrinol Metab 89:6054–6060
27. Zimmermann MB (2009) Iodine deficiency. Endocr Rev 30:376–408
28. Zimmermann MB, Andersson M (2012) Update on iodine status worldwide. Curr Opin Endocrinol Diabetes Obes 19:382–387
29. Pearce EN, Andersson M, Zimmermann MB (2013) Global iodine nutrition: where do we stand in 2013? Thyroid 23:523–528
30. Saira S, Khattak RM, Rehman AU, Khan AA, Khattak MNK (2014) Prevalence of goiter and iodine status in 6–12 years school children and pregnant women of district Charsadda, Pakistan. Acta Endocrinol (Buc) 10:65–75
31. Andersson M, Karumbunathan V, Zimmermann MB (2012) Global iodine status in 2011 and trends over the past decade. J Nutr 142:744–750
32. Walker SP, Wachs TD, Gardner JM, Lozoff B, Wasserman GA, Pollitt E, Carter JA (2007) Child development: risk factors for adverse outcomes in developing countries. Lancet 369:145–157
33. Kerac M, Postels DG, Mallewa M, Jalloh AA, Voskuijl WP, Groce N, Gladstone M, Molyneux E (2014) The interaction of malnutrition and neurological disability in Africa. Semin Pediatr Neurol 21:42–49
34. Clifton VL, Hodyl NA, Fogarty PA, Torpy DJ, Roberts R, Nettelbeck T, Ma G, Hetzel B (2013) The impact of iodine supplementation and bread fortification on urinary iodine concentrations in a mildly iodine deficient population of pregnant women in South Australia. Nutr J 12:32
35. Bath SC, Rayman MP (2013) Iodine deficiency in the UK: an overlooked cause of impaired neurodevelopment? Proc Nutr Soc 72:226–235
36. Gowachirapant S, Melse-Boonstra A, Winichagoon P, Zimmermann MB (2014) Overweight increases risk of first trimester hypothyroxinaemia in iodine-deficient pregnant women. Matern Child Nutr 10:61–71
37. World Health Organization/UNICEF/ICCIDD (2007) Assessment of ID disorders and monitoring their elimination: a guide for programme managers, 3rd edn. World Health Organization, Geneva, Available from http://whqlibdoc.who.int/publications/2007/9789241595827_eng.pdf
38. Román GC (2007) Autism: transient in utero hypothyroxinemia related to maternal flavonoid ingestion during pregnancy and to other environmental antithyroid agents. J Neurol Sci 262(1–2):15–26
39. Ozpinar A, Kelestimur F, Songur Y, Can O, Valentin L, Caldwell K, Arikan E, Unsal I et al (2014) Iodine status in Turkish populations and exposure to iodide uptake inhibitors. PLoS One 9(2):e88206
40. Rogan WJ, Paulson JA, Baum C, Brock-Utne AC, Brumberg HL, Campbell CC, Lanphear BP, Lowry JA et al (2014) Iodine deficiency, pollutant chemicals, and the thyroid: new information on an old problem. Pediatrics 133:1163–1166
41. Tonacchera M, Viacava P, Fanelli G, Agretti P, De Marco G, De Servi M, Di Cosmo C, Chiovato L et al (2004) The sodium-iodide symporter protein is always present at a low expression and confined to the cell membrane in nonfunctioning nonadenomatous nodules of toxic nodular goitre. Clin Endocrinol (Oxf) 61(1):40–45
42. Kirk AB (2006) Environmental perchlorate: why it matters. Anal Chim Acta 567(1):4–12
43. Lumen A, Mattie DR, Fisher JW (2013) Evaluation of perturbations in serum thyroid hormones during human pregnancy due to dietary iodide and perchlorate exposure using a biologically based dose–response model. Toxicol Sci 133(2):320–341
44. Melse-Boonstra A, Mackenzie I (2013) Iodine deficiency, thyroid function and hearing deficit: a review. Nutr Res Rev 26(2):110–117
45. Conde-Agudelo A, Romero R (2009) Antenatal magnesium sulfate for the prevention of cerebral palsy in preterm infants less than 34 weeks’ gestation: a systematic review and metaanalysis. Am J Obstet Gynecol 200(6):595–609
46. Román GC, Ghassabian A, Bongers-Schokking JJ, Jaddoe VW, Hofman A, de Rijke YB, Verhulst FC, Tiemeier H (2013) Association of gestational maternal hypothyroxinemia and increased autism risk. Ann Neurol 74(5):733–742
47. Hynes KL, Otahal P, Hay I, Burgess JR (2013) Mild iodine deficiency during pregnancy is associated with reduced educational outcomes in the offspring: 9-year follow-up of the gestational iodine cohort. J Clin Endocrinol Metab 98:1954–1962
48. Bath SC, Steer CD, Golding J, Emmett P, Rayman MP (2013) Effect of inadequate iodine status in UK pregnant women on cognitive outcomes in their children: results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Lancet 382:331–337
49. Berbel P, Mestre JL, Santamaría A, Palazón I, Franco A, Graells M, González-Torga A, de Escobar GM (2009) Delayed neurobehavioral development in children born to pregnant women with mild hypothyroxinemia during the first month of gestation: the importance of early iodine supplementation. Thyroid 19:511–519
50. Pop VJ, Kuijpens JL, van Baar AL, Verkerk G, van Son MM, de Vijlder JJ, Vulsma T, Wiersinga WM et al (1999) Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol (Oxf) 50:149–155
51. Pop VJ, Brouwers EP, Vader HL, Vulsma T, van Baar AL (2003) Maternal hypothyroxinemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin Endocrinol (Oxf) 59:282–288
52. Skeaff SA (2011) Iodine deficency in pregnancy: the effect on neurodevelopment in the child. Nutrients 3:265–273
53. Costeira MJ, Oliveira P, Santos NC, Ares S, Saenz-Rico B, de Escobar GM, Palha JA (2011) Psychomotor development of children from an iodine-deficient region. J Pediatr 159:447–453
54. Korevaar TI, Schalekamp-Timmermans S, de Rijke YB, Visser WE, Visser W, de Muinck Keizer-Schrama SM, Hofman A, Ross HA et al (2013) Hypothyroxinemia and TPO-antibody positivity are risk factors for premature delivery: the generation R study. J Clin Endocrinol Metab 98(11):4382–4390
55. Ares S, Escobar-Morreale HF, Quero J, Durán S, Presas MJ, Herruzo R, Morreale de Escobar G (1997) Neonatal hypothyroxinemia: effects of iodine intake and premature birth. J Clin Endocrinol Metab 82(6):1704–1712
56. van Wassenaer AG, Kok JH (2004) Hypothyroxinaemia and thyroid function after preterm birth. Semin Neonatol 9(1):3–11
57. Williams FL, Hume R (2008) Perinatal factors affecting thyroid hormone status in extreme preterm infants. Semin Perinatol 32:398–402
58. Williams FL, Mires GJ, Barnett C, Ogston SA, van Toor H, Visser TJ, Hume R, Scottish Preterm Thyroid Group (2005) Transient hypothyroxinemia in preterm infants: the role of cord sera thyroid hormone levels adjusted for prenatal and intrapartum factors. J Clin Endocrinol Metab 90:4599–4606
59. Hong T, Paneth N (2008) Maternal and infant thyroid disorders and cerebral palsy. Semin Perinatol 32(6):438–445
60. Rovet J, Simic N (2008) The role of transient hypothyroxinemia of prematurity in development of visual abilities. Semin Perinatol 32(6):431–437
61. Allen MC (2008) Neurodevelopmental outcomes of preterm infants. Curr Opin Neurol 21(2):123–128
62. Reuss ML, Paneth N, Pinto-Martin JA, Lorenz JM, Susser M (1996) The relation of transient hypothyroxinemia in preterm infants to neurologic development at two years of age. N Engl J Med 334(13):821–827
63. Hamm MP, Cherry NM, Martin JW, Bamforth F, Burstyn I (2009) The impact of isolated maternal hypothyroxinemia on perinatal morbidity. J Obstet Gynaecol Can 31(11):1015–1021
64. Storey NM, Gentile S, Ullah H, Russo A, Muessel M, Erxleben C, Armstrong DL (2006) Rapid signaling at the plasma membrane by a nuclear receptor for thyroid hormone. Proc Natl Acad Sci U S A 103:5197–5201
65. Wiesner RJ, Kurowski TT, Zak R (1992) Regulation by thyroid hormone of nuclear and mitochondrial genes encoding subunits of cytochrome-c oxidase in rat liver and skeletal muscle. Mol Endocrinol 6:1458–1467
66. Zamoner A, Pessoa-Pureur R (2011) Nongenomic actions of thyroid hormones: every why has a wherefore. Immunol Endocr Metab Agents Med Chem 11:165–178
67. Berbel P, Navarro D, Román GC (2014) An evo-devo approach to thyroid hormones and cerebral cortex development: etiological implications for autism. Front Endocrinol 5:146. doi:10.3389/fendo.2014.00146
68. Chatonnet F, Flamant F, Morte B (2014) A temporary compendium of thyroid hormone target genes in brain. Biochim Biophys Acta. doi:10.1016/j.bbagrm.2014.05.023
69. 2+/calmodulin-dependent protein kinase IV pathway. Endocrinology 151:810–820
70. Siegrist-Kaiser CA, Juge-Aubry C, Tranter MP, Ekenbarger DM, Leonard JL (1990) Thyroxine-dependent modulation of actin polymerization in cultured astrocytes. A novel, extranuclear action of thyroid hormone. J Biol Chem 265:5296–5302
71. Leonard JL, Farwell AP (1997) TH-regulated actin polymerization in brain. Thyroid 7:147–151
72. Davis PJ, Shih A, Lin HY, Martino LJ, Davis FB (2000) Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J Biol Chem 275:38032–38039
73. Visser WE, Friesema EC, Visser TJ (2011) Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol Endocrinol 25(1):1–14
74. Schwartz CE, Stevenson RE (2007) The MCT8 thyroid hormone transporter and Allan-Herndon-Dudley syndrome. Best Pract Res Clin Endocrinol Metab 21:307–321
75. Babu S, Sinha RA, Mohan V, Rao G, Pal A, Pathak A, Singh M, Godbole MM (2011) Effect of hypothyroxinemia on thyroid hormone responsiveness and action during rat postnatal neocortical development. Exp Neurol 228(1):91–98
76. Chan S, Kilby MD (2000) Thyroid hormone and central nervous system development. J Endocrinol 165(1):1–8
77. Heuer H, Mason CA (2003) Thyroid hormone induces cerebellar Purkinje cell dendritic development via the thyroid hormone receptor α1. J Neurosci 23(33):10604–10612
78. Gao FB, Apperly J, Raff M (1998) Cell-intrinsic timers and thyroid hormone regulate the probability of cell-cycle withdrawal and differentiation of oligodendrocyte precursor cells. Dev Biol 197:54–66
79. Billon N, Tokumoto Y, Forrest D, Raff M (2001) Role of thyroid hormone receptors in timing oligodendrocyte differentiation. Dev Biol 235(1):110–120
80. Billon N, Jolicoeur C, Tokumoto Y, Vennström B, Raff M (2002) Normal timing of oligodendrocyte development depends on thyroid hormone receptor alpha 1 (TRα1). EMBO J 21(23):6452–6460
81. Tsunekawa K, Murakami M (2014) Thyroid disease caused by receptor abnormality. Rinsho Byori 62(1):60–66
82. Shi C, Meng Q, Wood DW (2014) Analysis of the roles of mutations in thyroid hormone receptor-β by a bacterial biosensor system. J Mol Endocrinol 52(1):55–66
83. Glinoer D (2001) Pregnancy and iodine. Thyroid 11:471–481
84. Moleti M, Trimarchi F, Vermiglio F (2014) Thyroid physiology in pregnancy. Endocr Pract 20(6):589–596
85. Patel J, Landers K, Li H, Mortimer RH, Richard K (2011) Delivery of maternal thyroid hormones to the fetus. Trends Endocrinol Metab 22:164–170
86. Puig-Domingo M, Vila L (2013) The implications of iodine and its supplementation during pregnancy in fetal brain development. Curr Clin Pharmacol 8(2):97–109
87. Pearce EN (2012) Effects of iodine deficiency in pregnancy. J Trace Elem Med Biol 26:131–133
88. Moleti M, Trimarchi F, Vermiglio F (2011) Doubts and concerns about isolated maternal hypothyroxinemia. J Thyroid Res 2011:463029
89. Pedraza PE, Obregon MJ, Escobar-Morreale HF, del Rey FE, de Escobar GM (2006) Mechanisms of adaptation to iodine deficiency in rats: thyroid status is tissue specific. Its relevance for man. Endocrinology 147(5):2098–2108
90. Sharlin DS, Tighe D, Gilbert ME, Zoeller RT (2008) The balance between oligodendrocyte and astrocyte production in major white matter tracts in linearly related to serum total thyroxine. Endocrinology 149(5):2527–2536
91. Sinha RA, Pathak A, Mohan V, Bandyopadhyay S, Rastogi L, Godbole MM (2008) Maternal thyroid hormone: a strong repressor of neuronal nitric oxide synthase in rat embryonic neocortex. Endocrinology 149(9):4396–4401
92. Lavado-Autric R, Ausó E, García-Velasco JV, Arufe Mdel C, Escobar del Rey F, Berbel P, Morreale de Escobar G (2003) Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 111:1073–1082
93. Gilbert ME, Ramos RL, McCloskey DP, Goodman JH (2014) Subcortical band heterotopia in rat offspring following maternal hypothyroxinemia: structural and functional characteristics. J Neuroendocrinol 26(8):528–541
94. Farwell AP, Dubord-Tomasetti SA, Pietrzykowski AZ, Stachelek SJ, Leonard JL (2005) Regulation of cerebellar neuronal migration and neurite outgrowth by thyroxine and 3,3′,5′-triiodothyronine. Brain Res Dev Brain Res 154(1):121–135
95. Zamoner A, Funchal C, Jacques-Silva MC, Gottfried C, Barreto Silva FR, Pessoa-Pureur R (2007) Thyroid hormones reorganize the cytoskeleton of glial cells through Gfap phosphorylation and RhoA-dependent mechanisms. Cell Mol Neurobiol 27(7):845–865
96. Davis PJ, Leonard JL, Davis FB (2008) Mechanisms of nongenomic actions of thyroid hormone. Front Neuroendocrinol 29(2):211–218
97. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1(9):761–772
98. Wang Y, Wei W, Wang Y, Dong J, Song B, Min H, Teng W, Chen J (2013) Neurotoxicity of developmental hypothyroxinemia and hypothyroidism in rats: impairments of long-term potentiation are mediated by phosphatidylinositol 3-kinase signaling pathway. Toxicol Appl Pharmacol 271:257–265
99. Wang Y, Wei W, Song B, Wang Y, Dong J, Min H, Chen J (2014) Developmental hypothyroxinemia caused by mild iodine deficiency leads to HFS-induced LTD in rat hippocampal CA1 region: involvement of AMPA receptor. Mol Neurobiol 50(2):348–357
100. Wei W, Wang Y, Dong J, Wang Y, Min H, Song B, Shan Z, Teng W et al (2014) Hypothyroxinemia induced by maternal mild iodine deficiency impairs hippocampal myelinated growth in lactational rats. Environ Toxicol. doi:10.1002/tox.21997
101. Brooks VB (1984) Cerebellar functions in motor control. Hum Neurobiol 2:251–260
102. Wang Y, Wang Y, Dong J, Wei W, Song B, Min H, Yu Y, Lei X et al (2014) Developmental hypothyroxinemia and hypothyroidism reduce proliferation of cerebellar granule neuron precursors in rat offspring by downregulation of the sonic hedgehog signaling pathway. Mol Neurobiol 49:1143–1152
103. Harry GJ, Hooth MJ, Vallant M, Behl M, Travlos GS, Howard JL, Price CJ, McBride S et al (2014) Developmental neurotoxicity of 3,3′,4,4′-tetrachloroazobenzene with thyroxine deficit: sensitivity of glia and dentate granule neurons in the absence of behavioral changes. Toxics 2(3):496–532
104. Zhang L, Sun YN, Li YM, Lin LX, Ye Y, Yan YQ, Chen ZP (2011) Effect of different iodine nutrition on cerebellum Pcp-2 in rat offspring during lactation. Biol Trace Elem Res 143:1629–1639
105. Man EB (1972) Thyroid function in pregnancy and infancy. Maternal hypothyroxinemia and retardation of progeny. CRC Crit Rev Clin Lab Sci 3(2):203–225
106. Trentin AG (2006) Thyroid hormone and astrocyte morphogenesis. J Endocrinol 189(2):189–197
107. Vila L, Velasco I, González S, Morales F, Sánchez E, Torrejón S, Soldevila B, Stagnaro-Green A et al (2013) Controversies in endocrinology. On the need for universal thyroid screening in pregnant women. Eur J Endocrinol 170(1):R17–R30
108. Lazarus JH, Bestwick JP, Channon S, Paradice R, Maina A, Rees R, Chiusano E, John R et al (2012) Antenatal thyroid screening and childhood cognitive function. N Engl J Med 366(6):493–501
109. Trumpff C, De Schepper J, Tafforeau J, Van Oyen H, Vanderfaeillie J, Vandevijvere S (2013) Mild iodine deficiency in pregnancy in Europe and its consequences for cognitive and psychomotor development of children: a review. J Trace Elem Med Biol 27(3):174–183
110. Zhou SJ, Anderson AJ, Gibson RA, Makrides M (2013) Effect of iodine supplementation in pregnancy on child development and other clinical outcomes: a systematic review of randomized controlled trials. Am J Clin Nutr 98(5):1241–1254
111. Ferreir SM, Navarro AM, Magalhães PK, Maciel LM (2014) Iodine insufficiency in pregnant women from the State of São Paulo. Arq Bras Endocrinol Metabol 58:282–287
112. Méndez-Villa L, Elton-Puente JE, Solís-S JC, Sampson-Zaldívar E, García-G C, Villalobos P, Colarossi A, García OP et al (2014) Iodine nutrition and thyroid function assessment in childbearing age women from Queretaro, Mexico. Nutr Hosp 29:204–211