Imprinting of maternal thyroid hormones in the offspring

References

• Yen PM, Ando S, Feng X, et al. Thyroid hormone action at the cellular, genomic and target gene levels. Mol Cell Endocrinol 2006;246:121–7.
   PubMed Web of Science ®Google Scholar
• De Nayer P. Thyroid hormone action at the cellular level. Horm Res 1987;26:48–57.
   PubMedGoogle Scholar
• Vanderpump MP. The epidemiology of thyroid disease. Br Med Bull 2011;99:39–51.
   PubMed Web of Science ®Google Scholar
• Garber JR, Cobin RH, Gharib H, et al. Clinical practice guidelines for hypothyroidism in adults: cosponsored by the American association of clinical endocrinologists and the American thyroid association. Thyroid 2012;22:1200–1235.
   PubMed Web of Science ®Google Scholar
• Aoki Y, Belin RM, Clickner R, et al. Serum TSH and total T4 in the United States population and their association with participant characteristics: National health and nutrition examination survey (NHANES 1999–2002). Thyroid 2007;17:1211– 1223.
   PubMed Web of Science ®Google Scholar
• Okosieme O, Gilbert J, Abraham P, et al. Management of primary hypothyroidism: statement by the British thyroid association executive committee. Clin Endocrinol (Oxf) 2016;84:799–808.
   PubMed Web of Science ®Google Scholar
• Vanderpump MP, Tunbridge WM, French JM, et al. The incidence of thyroid disorders in the community: a twenty-source follow-up of the Whickham Survey. Clin Endocrinol (Oxf) 1995;43:55–68.
   PubMed Web of Science ®Google Scholar
• Klein RZ, Haddow JE, Faix JD, et al. Prevalence of thyroid deficiency in pregnant women. Clin Endocrinol (Oxf) 1991;35:41–46.
   PubMed Web of Science ®Google Scholar
• Lazarus JH. Epidemiology and prevention of thyroid disease in pregnancy. Thyroid 2002;12:861–865.
   PubMed Web of Science ®Google Scholar
• Pitt-Rivers R, Tata JR. The thyroid hormones. Pergamon Press; 2013. DOI: 10.1016/B978-0-08-009203-4.50008-2
   Google Scholar
• NIH National Institue of Health. Iodine; 2016. https://ods.od.nih.gov/factsheets/Iodine-Health- Professional/
   Google Scholar
• Pearce EN, Andersson M, Zimmermann MB. Global iodine nutrition: Where do we stand in 2013?. Thyroid 2013;23:523–528.
   PubMed Web of Science ®Google Scholar
• Ahmed OM, El-Gareib AW, El-bakry AM, et al. Thyroid hormones states and brain development interactions. Int J Dev Neurosci 2008;26:147–209.
   PubMed Web of Science ®Google Scholar
• De Vito P, Balducci V, Leone S, et al. Nongenomic effects of thyroid hormones on the immune system cells: New targets, old players. Steroids: Elsevier Inc.; 2012. p. 1–8.
   Google Scholar
• Berbel P, Navarro D, Auso E, et al. Role of late maternal thyroid hormones in cerebral cortex development: an experimental model for human prematurity. Cereb Cortex 2010;20:1462–1475.
   PubMed Web of Science ®Google Scholar
• Patel J, Landers K, Li H, et al. Thyroid hormones and fetal neurological development. J Endocrinol 2011;209:1–8.
   PubMed Web of Science ®Google Scholar
• Bianco AC, Larsen PR. Cellular and structural biology of the deiodinases. Thyroid 2005;15:777–786.
   PubMed Web of Science ®Google Scholar
• Anderson GW. Thyroid hormones and the brain. Front Neuroendocrinol 2001;22:1–17.
   PubMed Web of Science ®Google Scholar
• Pascual A, Aranda A. Thyroid hormone receptors, cell growth and differentiation. Biochim Biophys Acta 2013;1830:3908–3916.
   PubMed Web of Science ®Google Scholar
• Zhang J, Lazar MA. The mechanism of action of thyroid hormones. Annu Rev Physiol 2000;62:439–466.
   PubMed Web of Science ®Google Scholar
• Brent GA. Mechanisms of thyroid hormone action. J Clin Invest 2012;122:3035–3043.
   PubMed Web of Science ®Google Scholar
• Ausó E, Lavado-Autric R, Cuevas E, et al. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 2004;145:4037–4047.
   PubMed Web of Science ®Google Scholar
• Osorio J. Thyroid gland: Human thyroid gland development and function–angiogenesis in the spotlight. Nat Rev Endocrinol 2014;10:444.
   Google Scholar
• Iskaros J, Pickard M, Evans I, Sinha A. Thyroid hormone receptor gene expression in first trimester human fetal brain. J Clin Endocrinol Metab 2000;85:2620– 2623.
   PubMed Web of Science ®Google Scholar
• Forhead AJ, Fowden AL. Thyroid hormones in fetal growth and prepartum maturation. J Endocrinol. 2014;221:R87–R103.
   PubMed Web of Science ®Google Scholar
• Raymond J, LaFranchi SH. Fetal and neonatal thyroid function: review and summary of significant new findings. Curr Opin Endocrinol, Diabetes, Obes. 2010;17:1–7.
   PubMed Web of Science ®Google Scholar
• Glinoer D, De Nayer P, Bordoux P, et al. Regulation of maternal thyroid during pregnancy. J Clin Endocrinol Metab 1990;71:276–287.
   PubMed Web of Science ®Google Scholar
• Fantz CRC, Dagogo-Jack SS, Ladenson JHJ, Gronowski AMA. Thyroid function during pregnancy. Clin Chem 1999:2250–2258.
   PubMed Web of Science ®Google Scholar
• Ramprasad M, Bhattacharyya SS, Bhattacharyya A. Thyroid disorders in pregnancy. Indian J Endocr Metab 2012;16:S167–S170.
   PubMedGoogle Scholar
• Schroeder AC, Privalsky ML. Thyroid hormones, T3 and T4, in the brain. Front. Endocrinol. 2014;5:40.
   PubMed Web of Science ®Google Scholar
• Zimmermann MB. Iodine deficiency. Endocr Rev 2009;30:376–408.
   PubMed Web of Science ®Google Scholar
• Parkes IL, Schenker JG, Shufaro Y. Thyroid disorders during pregnancy. Gynecol Endocrinol 2012;28:993–998.
   PubMed Web of Science ®Google Scholar
• ATA. American Thyroid Association. 2015.
   Google Scholar
• Hypothyroidism. The Lancet 2004:793–803.
   Google Scholar
• Negro R. Thyroid insufficiency during pregnancy: complications and implications for screening. Expert Rev Endocrinol Metab 2008;3:137–146.
   Google Scholar
• Gessl A, Lemmens-Gruber R, Kautzky-Willer A. Thyroid disorders. Handb Exp Pharmacol 2012:361–386.
   PubMedGoogle Scholar
• Stagnaro-Green A, Abalovich M, Alexander E, et al. Guidelines of the American thyroid association for the diagnosis and management of thyroid disease during pregnancy and postpartum. Thyroid 2011;21:1081–1125.
   PubMed Web of Science ®Google Scholar
• Negro R, Soldin OP, Obregon M-J, Stagnaro-Green A. Hypothyroxinemia and pregnancy. Endocr Prac: Off J Am Coll Endocrinol Am Assoc Clin Endocrinologists 2011;17:422–9.
   Google Scholar
• Buimer M, van Wassenaer AG, Ganzevoort W, et al. Transient hypothyroxinemia in severe hypertensive disorders of pregnancy. Obstet Gynecol 2005;106:973–979.
   PubMed Web of Science ®Google Scholar
• Moleti M, Trimarchi F, Vermiglio F. Doubts and concerns about isolated maternal hypothyroxinemia. J Thyroid Res 2011;2011:1–7.
   Google Scholar
• Somberg J, Molnar J. Adverse reactions of amiodarone on the thyroid. Cardiology 2016;134:364–365.
   PubMed Web of Science ®Google Scholar
• Collazos J, Ibarra S, Mayo J. Thyroid hormones in HIV-infected patients in the highly active antiretroviral therapy era: evidence of an interrelation between the thyroid axis and the immune system. Aids 2003;17:763–765.
   PubMed Web of Science ®Google Scholar
• Grinspoon SK, Bilezikian JP. HIV disease and the endocrine system. N Engl J Med 1992;327:1360–1365.
   PubMed Web of Science ®Google Scholar
• Chang DLF, Pearce EN. Screening for maternal thyroid dysfunction in pregnancy: a review of the clinical evidence and current guidelines. J Thyroid Res 2013;2013:851326.
   PubMedGoogle Scholar
• Pop VJ, Brouwers EP, Vader HL, et al. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-source follow-up study. Clin Endocrinol (Oxf) 2003;59:282–8.
   PubMed Web of Science ®Google Scholar
• Bernal J, Morte B. Thyroid hormone receptor activity in the absence of ligand: physiological and developmental implications. Biochim Biophys Acta 2013;1830:3893–3899.
   PubMed Web of Science ®Google Scholar
• Klecha AJ. Integrative study of hypothalamus-pituitary-thyroid-immune system interaction: thyroid hormone-mediated modulation of lymphocyte activity through the protein kinase C signaling pathway. J Endocrinol 2006;189:45–55.
   PubMed Web of Science ®Google Scholar
• Cheng S-Y, Leonard JL, Davis PJ. Molecular aspects of thyroid hormone actions. Endocr Rev 2010;31:139–170.
   PubMed Web of Science ®Google Scholar
• Pop VJ, Kuijpens JL, van Baar AL, et al. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol (Oxf) 1999;50:149–155.
   PubMed Web of Science ®Google Scholar
• Kooistra L, Crawford S, van Baar AL, et al. Neonatal effects of maternal hypothyroxinemia during early pregnancy. Pediatrics 2006;117:161–167.
   PubMed Web of Science ®Google Scholar
• Pop VJ, Brouwers EP, Vader HL, et al. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-source follow-up study. Clin Endocrinol (Oxf) 2003;59:282–288.
   PubMed Web of Science ®Google Scholar
• Li Y, Shan Z, Teng W, et al. Abnormalities of maternal thyroid function during pregnancy affect neuropsychological development of their children at 25–30 months. Clin Endocrinol (Oxf) 2010;72:825–829.
   PubMed Web of Science ®Google Scholar
• Henrichs J, Bongers-Schokking JJ, Schenk JJ, et al. Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the generation R study. J Clin Endocrinol Metab 2010;95:4227–4234.
   PubMed Web of Science ®Google Scholar
• Finken MJJ, van Eijsden M, Loomans EM, et al. Maternal hypothyroxinemia in early pregnancy predicts reduced performance in reaction time tests in 5- to 6-source-old offspring. J Clin Endocrinol Amp; Metab 2013;98:1417–1426.
   PubMed Web of Science ®Google Scholar
• Polanczyk G, de Lima MS, Horta BL, et al.. The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry 2007;164:942–948.
   PubMed Web of Science ®Google Scholar
• Vermiglio F, Lo Presti VP, Moleti M, et al. Attention deficit and hyperactivity disorders in the offspring of mothers exposed to mild-moderate iodine deficiency: a possible novel iodine deficiency disorder in developed countries. J Clin Endocrinol Metab 2004;89:6054–6060.
   PubMed Web of Science ®Google Scholar
• Andersen SL, Laurberg P, Wu CS, Olsen J. Attention deficit hyperactivity disorder and autism spectrum disorder in children born to mothers with thyroid dysfunction: a Danish nationwide cohort study. BJOG: an Int J Obstet Gynaecol 2014:1365–1374.
   PubMed Web of Science ®Google Scholar
• Päkkilä F, Männistö T, Pouta A, et al. The impact of gestational thyroid hormone concentrations on ADHD symptoms of the child. J Clin Endocrinol Amp; Metab 2014;99:E1–E8.
   PubMed Web of Science ®Google Scholar
• Aylward GP. Cognitive and neuropsychological outcomes: more than IQ scores. Ment Retard Dev Disabil Res Rev 2002;8:234–240.
   PubMedGoogle Scholar
• Ghassabian A, El Marroun H, Peeters RP, et al. Downstream effects of maternal hypothyroxinemia in early pregnancy: nonverbal IQ and brain morphology in school-age children. J Clin Endocrinol Metab 2014;99:2383–2390.
   PubMed Web of Science ®Google Scholar
• Park HR, Lee JM, Moon HE, et al. A short review on the current understanding of autism spectrum disorders. Exp Neurobiol 2016;25:1–13.
   PubMed Web of Science ®Google Scholar
• Pearce EN. Severe maternal hypothyroxinemia is associated with probable autism in offspring. Clin Thyroidology 2013;25:252–253.
   Google Scholar
• Román GC, Ghassabian A, Bongers-Schokking JJ, et al. Association of gestational maternal hypothyroxinemia and increased autism risk. Ann Neurol 2013:733–742.
   PubMed Web of Science ®Google Scholar
• Gyllenberg D, Sourander A, Surcel H-M, et al. Hypothyroxinemia during gestation and offspring schizophrenia in a national birth cohort. Biol Psychiatry 2016;79:962–970.
   PubMed Web of Science ®Google Scholar
• Leonard JL, Farwell AP, Yen PM, et al. Differential expression of thyroid hormone receptor isoforms in neurons and astroglial cells. Endocrinology 1994;135:548–555.
   PubMed Web of Science ®Google Scholar
• Billon N, Tokumoto Y, Forrest D, Raff M. Role of thyroid hormone receptors in timing oligodendrocyte differentiation. Dev Biol 2001;235:110–120.
   PubMed Web of Science ®Google Scholar
• Trentin AG. Thyroid hormone and astrocyte morphogenesis. J Endocrinol 2006;189:189–197.
   PubMed Web of Science ®Google Scholar
• Cuevas E, Auso E, Telefont M, et al. Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminence-derived neurons. Eur J Neurosci 2005;22:541–551.
   PubMed Web of Science ®Google Scholar
• Martinez-Galan JR, Pedraza P, Santacana M, et al. Early effects of iodine deficiency on radial glial cells of the hippocampus of the rat fetus. A model of neurological cretinism. J Clin Invest 1997;99:2701–2709.
   PubMed Web of Science ®Google Scholar
• Leuner B, Gould E. Structural plasticity and hippocampal function. Annu Rev Psychol 2010;61:111–140, C1–3.
   PubMed Web of Science ®Google Scholar
• Opazo MC, Gianini A, Pancetti F, et al. Maternal hypothyroxinemia impairs spatial learning and synaptic nature and function in the offspring. Endocrinology 2008;149:5097–5106.
   PubMed Web of Science ®Google Scholar
• Koromilas C, Liapi C, Schulpis KH, et al. Structural and functional alterations in the hippocampus due to hypothyroidism. Metab Brain Dis 2010;25:339–354.
   PubMed Web of Science ®Google Scholar
• Cisternas P, Louveau A, Bueno SM, et al. Gestational hypothyroxinemia affects glutamatergic synaptic protein distribution and neuronal plasticity through neuron-astrocyte interplay. Mol Neurobiol 2015. doi: 10.1007/s12035-015-9609-0
   Web of Science ®Google Scholar
• Wang Y, Dong J, Wang Y, et al. Developmental hypothyroxinemia and hypothyroidism reduce parallel fiber-purkinje cell synapses in rat offspring by downregulation of neurexin1/Cbln1/GluD2 tripartite complex. Biol Trace Elem Res 2016;173:465.
   PubMed Web of Science ®Google Scholar
• Corrales JD, Rocco GL, Blaess S, et al. Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 2004;131:5581–5590.
   PubMed Web of Science ®Google Scholar
• Evans IM, Sinha AK, Pickard MR, et al. Maternal hypothyroxinemia disrupts neurotransmitter metabolic enzymes in developing brain. J Endocrinol 1999;161:273–279.
   PubMed Web of Science ®Google Scholar
• Koromilas C, Liapi C, Zarros A, Stolakis V. Effects of experimentally-induced maternal hypothyroidism on crucial offspring rat brain enzyme activities. Int J Dev Neurosci 2014:1–6.
   PubMed Web of Science ®Google Scholar
• Cattani D, Goulart PB, de Liz Oliveira Cavalli VL, et al. Congenital hypothyroidism alters the oxidative status, enzyme activities and morphological parameters in the hippocampus of developing rats. Mol Cell Endocrinol 2013;375:14–26.
   PubMed Web of Science ®Google Scholar
• Wu P-C, Fann M-J, Kao L-S. Characterization of Ca2+ signaling pathways in mouse adrenal medullary chromaffin cells. J Neurochem 2010;112:1210–1222.
   PubMed Web of Science ®Google Scholar
• Carageorgiou H, Pantos C, Zarros A, et al. Changes in acetylcholinesterase, Na+,K+-ATPase, and Mg2+-ATPase activities in the frontal cortex and the hippocampus of hyper- and hypothyroid adult rats. Metabolism 2007;56:1104–1110.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Fan Y, Yu X, et al. Maternal subclinical hypothyroidism impairs neurodevelopment in rat offspring by inhibiting the CREB signaling pathway. Mol Neurobiol 2014;52:432–441.
   PubMed Web of Science ®Google Scholar
• Barco A, Alarcon JM, Kandel ER. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 2002;108:689–703.
   PubMed Web of Science ®Google Scholar
• Bernal J, Guadano-Ferraz A, Morte B. Perspectives in the study of thyroid hormone action on brain development and function. Thyroid 2003;13:1005–1012.
   PubMed Web of Science ®Google Scholar
• Calzà L, Fernandez M, Giuliani A, et al. Thyroid hormone and remyelination in adult central nervous system: a lesson from an inflammatory-demyelinating disease. Brain Res Brain Res Rev 2005:339–346.
   PubMedGoogle Scholar
• Calza L, Fernandez M, Giuliani A, et al. Thyroid hormone and remyelination in adult central nervous system: a lesson from an inflammatory-demyelinating disease. Brain Res Brain Res Rev 2005;48:339–346.
   PubMedGoogle Scholar
• O'Shea PJ, Williams GR. Insight into the physiological actions of thyroid hormone receptors from genetically modified mice. J Endocrinol 2002;175:553–570.
   PubMed Web of Science ®Google Scholar
• Pombo PM, Barettino D, Ibarrola N, et al. 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 1999;64:92–100.
   PubMedGoogle Scholar
• Ibarrola N, Rodriguez-Pena A. Hypothyroidism coordinately and transiently affects myelin protein gene expression in most rat brain regions during postnatal development. Brain Res 1997;752:285–293.
   PubMed Web of Science ®Google Scholar
• Lothian C, Prakash N, Lendahl U, Wahlstrom GM. Identification of both general and region-specific embryonic CNS enhancer elements in the nestin promoter. Exp Cell Res 1999;248:509–519.
   PubMed Web of Science ®Google Scholar
• Durand B, Raff M. A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 2000;22:64–71.
   PubMed Web of Science ®Google Scholar
• Yap N, Yu CL, Cheng SY. Modulation of the transcriptional activity of thyroid hormone receptors by the tumor suppressor p53. Proc Natl Acad Sci U S A 1996;93:4273–4277.
   PubMed Web of Science ®Google Scholar
• Sarlieve LL, Rodriguez-Pena A, Langley K. Expression of thyroid hormone receptor isoforms in the oligodendrocyte lineage. Neurochem Res 2004;29:903–922.
   PubMed Web of Science ®Google Scholar
• Yusta B, Besnard F, Ortiz-Caro J, et al. Evidence for the presence of nuclear 3,5,3′-triiodothyronine receptors in secondary cultures of pure rat oligodendrocytes. Endocrinology 1988;122:2278–2284.
   PubMed Web of Science ®Google Scholar
• Nathan N, Sullivan SD. Thyroid disorders during pregnancy. Endocrinol Metab Clin N Am 2014;43:573– 597.
   PubMed Web of Science ®Google Scholar
• Cooper DS, Laurberg P. Hyperthyroidism in pregnancy. Lancet Diabetes Endocrinol 2013;1:238–249.
   PubMed Web of Science ®Google Scholar
• Coulon AL, Savagner F, Briet C, et al. Prolonged and severe gestational thyrotoxicosis due to enhanced hCG sensitivity of a mutant thyrotropin receptor. J Clin Endocrinol Metab 2016;101:10–1.
   PubMed Web of Science ®Google Scholar
• Bolz M, Korber S, Schober HC. TSH secreting adenoma of pituitary gland (TSHom) - rare cause of hyperthyroidism in pregnancy. Dtsch Med Wochenschr 2013;138:362–366.
   PubMed Web of Science ®Google Scholar
• Nazarpour S, Ramezani Tehrani F, Simbar M, Azizi F. Thyroid dysfunction and pregnancy outcomes. Iran J Reprod Med 2015;13:387–396.
   PubMedGoogle Scholar
• Anselmo J, Cao D, Karrison T, et al. Fetal loss associated with excess thyroid hormone exposure. Jama 2004;292:691–695.
   PubMed Web of Science ®Google Scholar
• Polak M, Luton D. Fetal thyroidology. Best Pract Res Clin Endocrinol Metab 2014;28:161–173.
   PubMed Web of Science ®Google Scholar
• Davis LE, Lucas MJ, Hankins GD, et al. Thyrotoxicosis complicating pregnancy. Am J Obstet Gynecol 1989;160:63–70.
   PubMed Web of Science ®Google Scholar
• Gargallo Fernandez M. Hyperthyroidism and pregnancy. Endocrinol y nutr: organo de la Soc Esp de Endocrinol y Nutr 2013;60:535–543.
   Google Scholar
• Millar LK, Wing DA, Leung AS, et al. Low birth weight and preeclampsia in pregnancies complicated by hyperthyroidism. Obstet Gynecol 1994;84:946–949.
   PubMed Web of Science ®Google Scholar
• Zimmerman D. Fetal and neonatal hyperthyroidism. Thyroid 1999;9:727–733.
   PubMed Web of Science ®Google Scholar
• Desilets V, Audibert F, Society of O, Gynaecologists of C. Investigation and management of non-immune fetal hydrops. J Obstet Gynaecol Can. 2013;35:923–938.
   PubMedGoogle Scholar
• Polak M. Thyroid disorders during pregnancy: impact on the fetus. Horm Res Paediatr 2011;76 Suppl 1:97–101.
   PubMed Web of Science ®Google Scholar
• Batra CM. Fetal and neonatal thyrotoxicosis. Indian J Endocrinol Metab 2013;17:S50–S54.
   PubMedGoogle Scholar
• Momotani N, Ito K, Hamada N, et al. Maternal hyperthyroidism and congenital malformation in the offspring. Clin Endocrinol (Oxf) 1984;20:695–700.
   PubMed Web of Science ®Google Scholar
• Messer PM, Hauffa BP, Olbricht T, et al. Antithyroid drug treatment of Graves' disease in pregnancy: long-term effects on somatic growth, intellectual development and thyroid function of the offspring. Acta Endocrinol 1990;123:311–316.
   PubMedGoogle Scholar
• Lauder JM. Effects of early hypo- and hyperthyroidism on development of rat cerebellar cortex. IV. The parallel fibers. Brain Res 1978;142:25–39.
   PubMed Web of Science ®Google Scholar
• Nicholson JL, Altman J. Synaptogenesis in the rat cerebellum: effects of early hypo- and hyperthyroidism. Science 1972;176:530–532.
   PubMed Web of Science ®Google Scholar
• Ahmed OM, Ahmed RG, El-Gareib AW, et al. Effects of experimentally induced maternal hypothyroidism and hyperthyroidism on the development of rat offspring: II-the developmental pattern of neurons in relation to oxidative stress and antioxidant defense system. Int J Dev Neurosci 2012;30:517–537.
   PubMed Web of Science ®Google Scholar
• Ahmed OM, Abd El-Tawab SM, Ahmed RG. Effects of experimentally induced maternal hypothyroidism and hyperthyroidism on the development of rat offspring: I. The development of the thyroid hormones-neurotransmitters and adenosinergic system interactions. Int J Dev Neurosci 2010;28:437–454.
   PubMed Web of Science ®Google Scholar
• Strobl MJ, Freeman D, Patel J, et al. Opposing effects of maternal hypo- and hyperthyroidism on the stability of thalamocortical synapses in the visual cortex of adult offspring. Cereb Cortex 2016.
   Web of Science ®Google Scholar
• Chen C, Zhou Z, Zhong M, et al. Excess thyroid hormone inhibits embryonic neural stem/progenitor cells proliferation and maintenance through STAT3 signalling pathway. Neurotoxicity Res 2011;20:15–25.
   PubMed Web of Science ®Google Scholar
• He F, Ge W, Martinowich K, et al. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 2005;8:616–625.
   PubMed Web of Science ®Google Scholar
• Pasquini JM, Adamo AM. Thyroid hormones and the central nervous system. Dev Neurosci 1994;16:1–8.
   PubMed Web of Science ®Google Scholar
• Marta CB, Adamo AM, Soto EF, Pasquini JM. Sustained neonatal hyperthyroidism in the rat affects myelination in the central nervous system. J Neurosci Res 1998;53:251–259.
   PubMed Web of Science ®Google Scholar
• Teerds KJ, de Rooij DG, de Jong FH, van Haaster LH. Development of the adult-type Leydig cell population in the rat is affected by neonatal thyroid hormone levels. Biol Reprod 1998;59:344–350.
   PubMed Web of Science ®Google Scholar
• Cabanillas AM, Smith GE, Darling DS. T3-activation of the rat growth hormone gene is inhibited by a zinc finger/homeodomain protein. Mol Cell Endocrinol 2001;181:131–137.
   PubMed Web of Science ®Google Scholar
• Halperin Y, Surks MI, Shapiro LE. L-triiodothyronine (T3) regulates cellular growth rate, growth hormone production, and levels of nuclear T3 receptors via distinct dose-response ranges in cultured GC cells. Endocrinology 1990;126:2321–2326.
   PubMed Web of Science ®Google Scholar
• Kumara-Siri MH, Surks MI. Regulation of growth hormone mRNA synthesis by 3,5,3′-triiodo-L-thyronine in cultured growth hormone-producing rat pituitary tumor cells (GC cells). Dissociation between nuclear iodothyronine receptor concentration and growth hormone mRNA synthesis during the deoxyribonucleic acid synthesis phase of the cell cycle. J Biol Chem 1985;260:14529–14537.
   PubMed Web of Science ®Google Scholar
• de Picoli Souza K, Silva FG, Nunes MT. Effect of neonatal hyperthyroidism on GH gene expression reprogramming and physiological repercussions in rat adulthood. J Endocrinol 2006;190:407–414.
   PubMed Web of Science ®Google Scholar
• Lynch MA, Mills K. Immunology meets neuroscience–Opportunities for immune intervention in neurodegenerative diseases. Brain, Behavoir Immun 2012;26:1–10.
   PubMed Web of Science ®Google Scholar
• Dedecjus M, Stasiolek M, Brzezinski J, et al. Thyroid hormones influence human dendritic cells phenotype, function, and subsets distribution. Thyroid 2011;21:533– 540.
   PubMed Web of Science ®Google Scholar
• Schultz KT, Grieder F. Structure and function of the immune system. Toxicol Pathol 1987;15:262–264.
   PubMed Web of Science ®Google Scholar
• Csaba G, Kovács P, Pállinger E. Immunologically demonstrable hormones and hormone-like molecules in rat white blood cells and mast cells. Cell Biol Int 2004;28:487–490.
   PubMed Web of Science ®Google Scholar
• Pállinger E, Horváth Z, Csóka M, et al. Decreased hormone content of immune cells in children during acute lymphocytic leukemia - effect of treatment. Acta Microbiol Immunol Hung 2011;58:41–50.
   PubMed Web of Science ®Google Scholar
• Wang HC, Klein JR. Immune function of thyroid stimulating hormone and receptor. Crit Rev Immunol 2001;21:323–337.
   PubMed Web of Science ®Google Scholar
• Chabaud O, Lissitzky S. Thyrotropin-specific binding to human peripheral blood monocytes and polymorphonuclear leukocytes. Mol Cell Endocrinol 1977;7:79–87.
   PubMed Web of Science ®Google Scholar
• Ohashi H, Itoh M. Effects of thyroid hormones on the lymphocyte phenotypes in rats: changes in lymphocyte subsets related to thyroid function. Endocr Regul 1994;28:117–123.
   PubMedGoogle Scholar
• Coutelier JP, Kehrl JH, Bellur SS, et al. Binding and functional effects of thyroid stimulating hormone on human immune cells. J Clin Immunol 1990;10:204–210.
   PubMed Web of Science ®Google Scholar
• Bagriacik EU, Klein JR. The thyrotropin (thyroid-stimulating hormone) receptor is expressed on murine dendritic cells and on a subset of CD45RBhigh lymph node T cells: functional role for thyroid-stimulating hormone during immune activation. J Immunol 2000;164:6158–6165.
   PubMed Web of Science ®Google Scholar
• Provinciali M, Di Stefano G, Fabris N. Improvement in the proliferative capacity and natural killer cell activity of murine spleen lymphocytes by thyrotropin. Int J Immunopharmacol 1992;14:865–870.
   PubMed Web of Science ®Google Scholar
• Klein JR. Physiological relevance of thyroid stimulating hormone and thyroid stimulating hormone receptor in tissues other than the thyroid. Autoimmunity 2003;36:417–421.
   PubMed Web of Science ®Google Scholar
• Mascanfroni ID, Montesinos MdM, Alamino VA, et al. Nuclear factor (NF)-kappaB-dependent thyroid hormone receptor beta1 expression controls dendritic cell function via Akt signaling. J Biol Chem 2010;285:9569–9582.
   PubMed Web of Science ®Google Scholar
• Mascanfroni I, Montesinos Mdel M, Susperreguy S, et al. Control of dendritic cell maturation and function by triiodothyronine. FASEB J 2008;22:1032–1042.
   PubMed Web of Science ®Google Scholar
• Perrotta C, Buldorini M, Assi E, et al. The thyroid hormone triiodothyronine controls macrophage maturation and functions: protective role during inflammation. Am J Pathol 2014;184:230–247.
   PubMed Web of Science ®Google Scholar
• El-Shaikh KA, Gabry MS, Othman GA. Recovery of age-dependent immunological deterioration in old mice by thyroxine treatment. J Anim Physiol Anim Nutr (Berl) 2006;90:244–254.
   PubMed Web of Science ®Google Scholar
• Vereyken EJF, Heijnen PDAM, Baron W, et al.. Classically and alternatively activated bone marrow derived macrophages differ in cytoskeletal functions and migration towards specific CNS cell types. J Neuroinflammation 2011;8:58.
   PubMed Web of Science ®Google Scholar
• Stein-Streilein J, Zakarija M, Papic M, McKenzie JM. Hyperthyroxinemic mice have reduced natural killer cell activity. Evidence for a defective trigger mechanism. J Immunol 1987;139:2502–2507.
   PubMed Web of Science ®Google Scholar
• De Vito P, Incerpi S, Pedersen JZ, et al.. Thyroid hormones as modulators of immune activities at the cellular level. Thyroid 2011;21:879–890.
   PubMed Web of Science ®Google Scholar
• Chandel AS, Chatterjee S. Immunomodulatory role of thyroid hormones: effect on humoral immune response to Salmonella typhi O antigen. Indian J Exp Biology 1989;27:1013–1016.
   PubMed Web of Science ®Google Scholar
• Rosa LF, Safi DA, Curi R. Effect of hypo- and hyperthyroidism on the function and metabolism of macrophages in rats. Cell Biochem Funct 1995;13:141–147.
   PubMed Web of Science ®Google Scholar
• Ortega E, Forner MA, Garcia JJ, et al. Enhanced chemotaxis of macrophages by strenuous exercise in trained mice: thyroid hormones as possible mediators. Mol Cell Biochem 1999;201:41–47.
   PubMed Web of Science ®Google Scholar
• Rittenhouse PA, Redei E. Thyroxine administration prevents streptococcal cell wall-induced inflammatory responses. Endocrinology 1997;138:1434– 1439.
   PubMed Web of Science ®Google Scholar
• Nishizawa Y, Fushiki S, Amakata Y, Nishizawa Y. Thyroxine-induced production of superoxide anion by human alveolar neutrophils and macrophages: a possible mechanism for the exacerbation of bronchial asthma with the development of hyperthyroidism. In vivo 1998;12:253–257.
   PubMed Web of Science ®Google Scholar
• Vinayagamoorthi R, Koner BC, Kavitha S, et al. Potentiation of humoral immune response and activation of NF-kappaB pathway in lymphocytes in experimentally induced hyperthyroid rats. Cell Immunol 2005;238:56–60.
   PubMed Web of Science ®Google Scholar
• Yao C, Zhang J, Wang L, et al. Inhibitory effects of thyroxine on cytokine production by T cells in mice. Int Immunopharmacol 2007. p. 1747–1754.
   PubMed Web of Science ®Google Scholar
• Forner MA, Barriga C, Ortega E. Exercise-induced stimulation of murine macrophage phagocytosis may be mediated by thyroxine. J Appl Physiol 1996;80:899– 903.
   PubMed Web of Science ®Google Scholar
• Owen JJ, Jenkinson EJ. Regulatory factors in lymphoid development. Br Med Bull 1989;45:350–360.
   PubMed Web of Science ®Google Scholar
• Chambers CA, Sullivan TJ, Allison JP. Lymphoproliferation in CTLA-4-deficient mice is mediated by costimulation-dependent activation of CD4+ T cells. Immunity 1997;7:885–895.
   PubMed Web of Science ®Google Scholar
• Csaba G. Hormones in the immune system and their possible role. A critical review. Acta Microbiol Immunol Hung 2014;61:241–260.
   PubMed Web of Science ®Google Scholar
• Rooney AA, Fournier M, Bernier J, Cyr DG. Neonatal exposure to propylthiouracil induces a shift in lymphoid cell sub-populations in the developing postnatal male rat spleen and thymus. Cell Immunol 2003:91–102.
   PubMed Web of Science ®Google Scholar
• Cano-Europa E, Blas-Valdivia V, Franco-Colin M, et al. Methimazole-induced hypothyroidism causes cellular damage in the spleen, heart, liver, lung and kidney. Acta Histochemica 2011;113:1–5.
   PubMed Web of Science ®Google Scholar
• Nakamura R, Teshima R, Hachisuka A, et al. Effects of developmental hypothyroidism induced by maternal administration of methimazole or propylthiouracil on the immune system of rats. Int Immunopharmacol 2007;7:1630–1638.
   PubMed Web of Science ®Google Scholar
• Coria MJ, Viglianco Y, Marra CA. Hypothyroidism modifies lipid composition of polymorphonuclear leukocytes. Cell Physiol Biochem 2012;29:713–724.
   PubMed Web of Science ®Google Scholar
• Hassman R, Weetman AP, Gunn C, et al. The effects of hyperthyroidism on experimental autoimmune thyroiditis in the rat. Endocrinology 1985;116:1253– 1258.
   PubMed Web of Science ®Google Scholar
• Kakehasi AM, Dias VN, Duarte JE. Thyroid abnormalities in systemic lupus erythematosus: a study in 100 Brazilian patients. Rev Bras de Reumatologia 2006;46:375–379.
   Google Scholar
• Pyne D, Isenberg DA. Autoimmune thyroid disease in systemic lupus erythematosus. Ann Rheum Dis 2002;61:70–72.
   PubMed Web of Science ®Google Scholar
• Lisnevskaia L, Murphy G, Isenberg D. Systemic lupus erythematosus. Lancet 2014;384:1878–1888.
   PubMed Web of Science ®Google Scholar
• Blich M, Rozin A, Edoute Y. Systemic lupus erythematosus and thyroid disease. Prevalence 2004;6:218–220.
   Google Scholar
• Weetman AP, Walport MJ. The association of autoimmune thyroiditis with systemic lupus erythematosus. Rheumatology 1987;26:359–361.
   Web of Science ®Google Scholar
• Antonelli A, Fallahi P, Mosca M, et al. Prevalence of thyroid dysfunctions in systemic lupus erythematosus. Metabolism 2010;59:896–900.
   PubMed Web of Science ®Google Scholar
• Costa LP, Bonfá E, Martinago CD. Juvenile onset systemic lupus erythematosus thyroid dysfunction: A subgroup with mild disease? J Autoimmun 2009;33:121–124.
   PubMed Web of Science ®Google Scholar
• Green LM, LaBue M, Lazarus JP, Colburn KK. Characterization of autoimmune thyroiditis in MRL-lpr/lpr mice. Lupus 1995;4:187–196.
   PubMed Web of Science ®Google Scholar
• Wahren-Herlenius M, Dörner T. Immunopathogenic mechanisms of systemic autoimmune disease. Lancet 2013;382:819–831.
   PubMed Web of Science ®Google Scholar
• Chambers CA. The expanding world of co-stimulation: the two-signal model revisited. Trends Immunol 2001;22:217–223.
   PubMed Web of Science ®Google Scholar
• Holt PG, Jones CA. The development of the immune system during pregnancy and early life. Allergy 2000;55:688–697.
   PubMed Web of Science ®Google Scholar
• Erf GF. Immune development in young-adult C.RF-hyt mice is affected by congenital and maternal hypothyroidism. Proc Soc Exp Biol Med 1993;204:40–48.
   PubMed Web of Science ®Google Scholar
• Nylander A, Hafler DA. Multiple sclerosis. J Clin Invest 2012;122:1180–1188.
   PubMed Web of Science ®Google Scholar
• Lutton JD, Winston R, Rodman TC. Multiple sclerosis: etiological mechanisms and future directions. Exp Biol Med (Maywood) 2004;229:12–20.
   PubMed Web of Science ®Google Scholar
• Hickey WF, Hsu BL, Kimura H. T-lymphocyte entry into the central nervous system. J Neurosci Res 1991;28:254–260.
   PubMed Web of Science ®Google Scholar
• Minagar A, Alexander JS. Blood-brain barrier disruption in multiple sclerosis. Mult Scler 2003;9:540–549.
   PubMed Web of Science ®Google Scholar
• Hemmer B, Archelos JJ, Hartung HP. New concepts in the immunopathogenesis of multiple sclerosis. Nat Rev Neurosci 2002;3:291–301.
   PubMed Web of Science ®Google Scholar
• Croxford AL, Kurschus FC, Waisman A. Mouse models for multiple sclerosis: historical facts and future implications. Biochim Biophys Acta 2011. p. 177–183.
   PubMed Web of Science ®Google Scholar
• Miller SD, Karpus WJ. Experimental autoimmune encephalomyelitis in the mouse. Current protocols in immunology / edited by John E Coligan [et al] 2007; Chapter 15:Unit 15 1.
   Google Scholar
• Albornoz EA, Carreño LJ, Cortés C, et al. Gestational hypothyroidism increases the severity of experimental autoimmune encephalomyelitis in adult offspring. Thyroid 2013;23:1627–1637.
   PubMed Web of Science ®Google Scholar
• Nieto PA, Penaloza HF, Salazar-Echegarai FJ, et al. Gestational hypothyroidism improves the ability of the female offspring to clear Streptococcus pneumoniae infection and to recover from pneumococcal pneumonia. Endocrinology 2016:en20151957.
   Web of Science ®Google Scholar
• Betterle C, Zanchetta R. Update on autoimmune polyendocrine syndromes (APS). Acta Bio-Medica: Atenei Parmensis 2003;74:9–33.
   PubMedGoogle Scholar
• Calvo CR, Amsen D, Kruisbeek AM. Cytotoxic T lymphocyte antigen 4 (CTLA-4) interferes with extracellular signal-regulated kinase (ERK) and Jun NH2-terminal kinase (JNK) activation, but does not affect phosphorylation of T cell receptor zeta and ZAP70. J Exp Med 1997;186:1645–1653.
   PubMed Web of Science ®Google Scholar
• Cutolo M. Autoimmune polyendocrine syndromes. Autoimmun Rev 2014;13:85–89.
   PubMed Web of Science ®Google Scholar