Thyroid hormones in fetal growth and prepartum maturation

Journal of Endocrinology

Volumn 221, Issue 3, 2014, Pages

  Forhead, A J ^a,b   Fowden, A L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

Intrauterine growth; Maturation; Neonatal adaptation; Thyroid hormones

Indexed keywords

CATECHOLAMINE; GLUCOSE TRANSPORTER 4; GROWTH HORMONE; LEPTIN; LIOTHYRONINE; MONOCARBOXYLATE TRANSPORTER 10; MONOCARBOXYLATE TRANSPORTER 8; PROSTAGLANDIN; PROTIRELIN; SOMATOMEDIN; THYROID HORMONE; THYROTROPIN; THYROXINE; UNCLASSIFIED DRUG;

BIOAVAILABILITY; BIRTH; BRAIN DEVELOPMENT; BROWN ADIPOSE TISSUE; CALCIUM HOMEOSTASIS; CORDOCENTESIS; ENZYME ACTIVITY; FETUS (ANATOMY); FETUS DEVELOPMENT; FETUS GROWTH; FETUS MATURITY; GESTATIONAL AGE; GLUCOGENESIS; HEART FUNCTION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LUNG FUNCTION; LUNG GAS EXCHANGE; NEGATIVE FEEDBACK; NONHUMAN; OVARY FOLLICLE CELL; PLACENTAL TRANSFER; PRENATAL GROWTH; PRIORITY JOURNAL; RESPIRATORY FUNCTION; REVIEW; THERMOGENESIS; THYROTROPIN BLOOD LEVEL;

INTRAUTERINE GROWTH; MATURATION; NEONATAL ADAPTATION; THYROID HORMONES;

FEMALE; FETAL DEVELOPMENT; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MATERNAL-FETAL EXCHANGE; MODELS, BIOLOGICAL; PITUITARY-ADRENAL SYSTEM; PREGNANCY; THYROXINE; TRIIODOTHYRONINE;

EID: 84900306099     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0025     Document Type: Review

References (158)

1. Akturk M, Oruc AS, Danisman N, Erkek S, Buyukkagnici U, Unlu E & Tazebay UH 2013 NaC/IK symporter and type 3 iodothyronine deiodinase gene expression in amniotic membrane and placenta and its relationship to maternal thyroid hormones. Biological Trace Element Research 154 338-344. (doi:10.1007/s12011-013-9748-y)
2. Allen AL, Fretz PB, Card CE & Doige CE 1998 The effects of partial thyroidectomy on development of the equine fetus. Equine Veterinary Journal 30 53-59. (doi:10.1111/j.2042-3306.1998.tb04088.x)
3. Ayromlooi J, Berg PD, Valderrama E & Tobias MD 1983 Midtrimester thyroidectomy in the ovine fetus. Pediatric Pharmacology 3 15-28.
4. Ballard PL, Hovey ML & Gonzales LK 1984 Thyroid hormone stimulation of phosphatidylcholine synthesis in cultured fetal rabbit lung. Journal of Clinical Investigation 74 898-905. (doi:10.1172/JCI111507)
5. Barker PM, Brown MJ, Ramsden CA, Strang LB & Walters DV 1988 The effects of thyroidectomy in the fetal sheep on lung liquid reabsorption induced by adrenaline or cyclic AMP. Journal of Physiology 407 372-383.
6. Barker PM, Strang LB & Walters DV 1990 The role of thyroid hormones in maturation of the adrenaline-sensitive lung liquid reabsorptive mechanism in fetal sheep. Journal of Physiology 424 473-485.
7. Barker PM, Walters DV, Markiewicz M & Strang LB 1991 Development of the lung liquid reabsorptive mechanism in fetal sheep: synergism of triiodothyronine and hydrocortisone. Journal of Physiology 433 435-449.
8. Bernal J & Pekonen F 1984 Ontogenesis of the nuclear 3,5,30-triiodothyronine receptor in the human fetal brain. Endocrinology 114 677-679. (doi:10.1210/endo-114-2-677)
9. Bhakthavathsalan A, Mann LI, Ayromlooi J, Kunzel W & Liu M 1977 The effects of fetal thyroidectomy in the ovine fetus. American Journal of Obstetrics and Gynecology 127 278-284.
10. 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)
11. Birk E, Tyndall MR, Erickson JC, Rudolph AM & Roberts JM 1992 Effects of thyroid hormone on myocardial adrenergic b-receptor responsiveness and function during late gestation. Pediatric Research 31 468-473. (doi:10.1203/00006450-199205000-00011)
12. Breall JA, Rudolph AM & Heymann MA 1984 Role of thyroid hormones in postnatal circulatory and metabolic adaptations. Journal of Clinical Investigation 73 1418-1424. (doi:10.1172/JCI111346)
13. Brent GA 2012 Mechanisms of thyroid hormone action. Journal of Clinical Investigation 122 3035-3043. (doi:10.1172/JCI60047)
14. Brodie C & Sampson SR 1988 Characterization of thyroid hormone effects on Na-K pump and membrane potential of cultured rat skeletal muscle. Endocrinology 123 891-897. (doi:10.1210/endo-123-2-891)
15. Brown RS 2004 Developmental regulation of thyrotropin receptor gene expression in the fetal and newborn thyroid. Endocrinology 145 4058-4061. (doi:10.1210/en.2004-0458)
16. Calvo R, Obregon MJ, Escobar del Rey F & Morreale de Escobar G 1992 The rat placenta and the transfer of thyroid hormones from the mother to fetus. Effects of maternal thyroid status. Endocrinology 131 357-365.
17. Carey LC, Valego NK, Chen K & Rose JC 2008 Thyroid hormone regulates renocortical COX-2 and PGE2 expression in the late gestation fetal sheep. Reproductive Sciences 15 598-603. (doi:10.1177/1933719108316910)
18. 4 expression by thyroid hormones. Journal of Biological Chemistry 269 5905-5912.
19. Champagne FA 2013 Early environment, glucocorticoid receptors and behavioural epigenetics. Behavioral Neuroscience 127 628-636. (doi:10.1037/a0034186)
20. Chan L, Miller TF, Yuxin J, Farina C, Chander A, Shaffer TH & Wolfson MR 1998 Antenatal triiodothyronine improves neonatal pulmonary function in preterm lambs. Journal of the Society for Gynecologic Investigation 5 122-126. (doi:10.1016/S1071-5576(97)00115-9)
21. Chan S,Kachilele S, McCabe CJ, Tannahill LA, Boelaert K, Gittoes NJ, Visser TJ, Franklyn JA & Kilby MD 2002 Early expression of thyroid hormone deiodinases and receptors in human fetal cerebral cortex. Brain Research 138 109-116. (doi:10.1016/S0165-3806(02)00459-5)
22. Chan S, Kachilele S, Hobbs E, Bulmer JN, Boelaert K, McCabe CJ, Driver PM, Bradwell AR, Kester M, Visser TJ et al. 2003 Placental iodothyronine deiodinase expression in normal and growth-restricted human pregnancies. Journal of Clinical Endocrinology and Metabolism 88 4488-4495. (doi:10.1210/jc.2003-030228)
23. Chan SY, Andrews MH, Lingas R, McCabe CJ, Franklyn JA, Kilby MD & Matthews SG 2005 Maternal nutrient deprivation induces sex-specific changes in thyroid hormone receptor and deiodinase expression in the fetal guinea pig brain. Journal of Physiology 566 467-480. (doi:10.1113/jphysiol.2005.084673)
24. Chan SY, Vasilopoulou E & Kilby MD 2009 The role of the placenta in thyroid hormone delivery to the fetus. Nature Clinical Practice. Endocrinology & Metabolism 5 45-54. (doi:10.1038/ncpendmet1026)
25. 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 fetal cerebral cortex during early development and in N-tera-2 neurodifferentiation. Journal of Physiology 589 2827-2845. (doi:10.1113/jphysiol.2011.207290)
26. Chan SY, Hancox LA, Martin-Santos A, Loubiere LS,Walter MN,Gonzalez AM, Cox PM, Logan A, McCabe CJ, Franklyn JA et al. 2014 MCT8 expression in human fetal cerebral cortex is reduced in severe intrauterine growth retardation. Journal of Endocrinology 220 85-95. (doi:10.1530/JOE-13-0400)
27. Charalambous M & Hernandez A 2013 Genomic imprinting of the type 3 thyroid hormone deiodinase gene: regulation and developmental implications. Biochimica et Biophysica Acta 1830 3946-3955. (doi:10.1016/j.bbagen.2012.03.015)
28. Chattergoon NN, Giraud GD & Thornburg KL 2007 Thyroid hormones inhibit proliferation of fetal cardiac myocytes in vitro. Journal of Endocrinology 192 R1-R8. (doi:10.1677/JOE-06-0114)
29. Chattergoon NN, Giraud GD, Louey S, Stork P, Fowden AL & Thornburg KL 2012a Thyroid hormone drives fetal cardiomyocyte maturation. FASEB Journal 26 397-408. (doi:10.1096/fj.10-179895)
30. Chattergoon NN, Louey S, Stork P, Giraud GD & Thornburg KL 2012b Mid-gestation ovine cadiomyocytes are vulnerable to mitotic suppression by thyroid hormone. Reproductive Sciences 19 642-649. (doi:10.1177/1933719111432860)
31. Chen K, Carey LC, Valego NK, Liu J & Rose JC 2005 Thyroid hormone modulates renin and ANG II receptor expression in fetal sheep. American Journal of Physiology 289 R1006-R1014.
32. Chen K, Carey LC, Valego NK & Rose JC 2007 Thyroid hormone replacement normalises renal renin and angiotensin receptor expression in thyroidectomised fetal sheep. American Journal of Physiology 293 R701-R706.
33. Chi HC, Chen C-Y, Tsai M-M, Tsai C-Y & Lin K-H 2013 Molecular functions of thyroid hormones and their clinical significance in liver-related diseases. Bio Med Research International 2013 601361. (doi:10.1155/2013/601361)
34. Contempre B, Jauniaux E, Calvo R, Jurkovic D, Campbell S & Morreale de Escobar G 1993 Detection of thyroid hormones in human embryonic cavities during the first trimester of pregnancy. Journal of Clinical Endocrinology and Metabolism 17 1719-1722.
35. Crie JS, Wakeland JR, Mayhew BA & Wildenthal K 1983 Direct anabolic effects of thyroid hormone in isolated mouse heart. American Journal of Physiology 245 C328-C333.
36. Darras VM, Visser TJ, Berghman LR & Kuhn ER 1992 Ontogeny of type I and type III deiodinase activities in embryonic and posthatch chicks:relationship with changes in plasma triiodothyronine and growth hormone levels. Comparative Biochemistry and Physiology 103 131-136. (doi:10.1016/0300-9629(92)90252-L)
37. Darras VM, Kotanen SP, Geris KL, Berghman LR & Kuhn ER 1996 Plasma thyroid hormone levels and iodothyronine deiodinase activity following an acute glucocorticoid challenge in embryonic compared with posthatch chickens. General and Comparative Endocrinology 104 203-212. (doi:10.1006/gcen.1996.0163)
38. Das DK, Ayromlooi J, Bandyopadhyay D, Bandyopadhyay S, Neogi A & Steinberg H 1984 Potentiation of surfactant release in fetal lung by thyroid hormone action. Journal of Applied Physiology 56 1621-1626.
39. Dauncey MJ & Geers R 1990 Nuclear 3,5,30-triiodothyronine receptors in skeletal muscle of normal and small-for-gestational-age newborn piglets. Biology of the Neonate 58 291-295. (doi:10.1159/000243281)
40. De Zegher F, Pernasetti F, Vanhole C, Devlieger H, Van Den Berghe G & Martial JA 1995 A prismatic case: the prenatal role of thyroid hormone evidenced by fetomaternal Pit-1 deficiency. Journal of Clinical Endocrinology and Metabolism 80 3127-3130.
41. Edwards JG, Bahl JJ, Flink IL, Cheng SY & Morkin E 1994 Thyroid hormone influences b myosin heavy chain (b MHC) expression. Biochemical and Biophysical Research Communications 199 1482-1488. (doi:10.1006/bbrc.1994.1398)
42. Erenberg A, Omori K, Menkes JH, Oh W & Fisher DA 1974 Growth and development of the thyroidectomized ovine fetus. Pediatric Research 8 783-789. (doi:10.1203/00006450-197409000-00001)
43. Falcone M, Miyamoto T, Fierro-Renoy F, Macchia E & DeGroot LJ 1994 Evaluation of the ontogeny of thyroid hormone receptor isotypes in rat brain and liver using an immunohistochemical technique. European Journal of Endocrinology 130 97-106. (doi:10.1530/eje.0.1300097)
44. Ferreiro B, Bernal J & Potter BJ 1987 Ontogenesis of thyroid hormone receptor in foetal lambs. Acta Endocrinologica 116 205-210.
45. Finkelstein DI, Andrianakis P, Luff AR & Walker D 1991 Effect of thyroidectomy on development of skeletal muscle in fetal sheep. American Journal of Physiology 261 R1300-R1306.
46. Fisher DA 1997 Fetal thyroid function: diagnosis and management of fetal thyroid disorders. Clinical Obstetrics and Gynecology 40 16-31. (doi:10.1097/00003081-199703000-00005)
47. Fisher DA & Polk DH 1989 Development of the thyroid. Baillier̀e's Clinical Endocrinology and Metabolism 3 627-657. (doi:10.1016/S0950-351X(89)80046-1)
48. Forbes K & Westwood M 2008 The IGF axis and placental function: a minireview. Hormone Research 69 129-137. (doi:10.1159/000112585)
49. Forhead AJ & Fowden AL 2002 Effects of thyroid hormones on pulmonary and renal angiotensin-converting enzyme concentrations in fetal sheep near term. Journal of Endocrinology 173 143-150. (doi:10.1677/joe.0. 1730143)
50. Forhead AJ, Li J, Gilmour RS & Fowden AL 1998 Control of hepatic insulinlike growth factor-II gene expression by thyroid hormones in fetal sheep near term. American Journal of Physiology 275 E149-E156.
51. Forhead AJ, Gillespie CE & Fowden AL 2000a Role of cortisol in the ontogenic control of pulmonary and renal angiotensin-converting enzyme in fetal sheep near term. Journal of Physiology 526 409-416. (doi:10.1111/j.1469-7793.2000.00409.x)
52. Forhead AJ, Li J, Saunders JC, Dauncey MJ, Gilmour RS & Fowden AL 2000b Control of ovine hepatic growth hormone receptor and insulin-like growth factor-I by thyroid hormones in utero. American Journal of Physiology 278 E1166-E1174.
53. Forhead AJ, Li J, Gilmour RS, Dauncey MJ & Fowden AL 2002 Thyroid hormones and the mRNA of the growth hormone receptor and insulinlike growth factor-I in skeletal muscle of fetal sheep. American Journal of Physiology 282 E80-E86.
54. Forhead AJ, Poore KR, Mapstone J & Fowden AL 2003 Developmental regulation of hepatic and renal gluconeogenic enzymes by thyroid hormones in fetal sheep during late gestation. Journal of Physiology 548 941-947. (doi:10.1113/jphysiol.2002.035816)
55. Forhead AJ, Curtis K, Kaptein E, Visser TJ & Fowden AL 2006 Developmental control of iodothyronine deiodinases by cortisol in the ovine fetus and placenta near term. Endocrinology 147 5988-5994. (doi:10.1210/en.2006-0712)
56. Forhead AJ, Jellyman JK, Gardner DS, Giussani DA, Kaptein E, Visser TJ & Fowden AL 2007 Differential effects of maternal dexamethasone treatment on circulating thyroid hormone concentrations and tissue deiodinase activity in the pregnant ewe and fetus. Endocrinology 148 800-805. (doi:10.1210/en.2006-1194)
57. Forhead AJ, Cutts S, Matthews P & Fowden AL 2009 Role of thyroid hormones in the developmental control of tissue glycogen in fetal sheep near term. Experimental Physiology 94 1079-1087. (doi:10.1113/expphysiol.2009.048751)
58. Fowden AL 2003 The insulin-like growth factors and feto-placental growth. Placenta 24 803-812. (doi:10.1016/S0143-4004(03)00080-8)
59. Fowden AL & Forhead AJ 2009 Hormones as epigenetic signals in developmental programming. Experimental Physiology 94 607-625. (doi:10.1113/expphysiol.2008.046359)
60. Fowden AL & Forhead AJ 2013 Endocrine interactions in the control of fetal growth. In Maternal and Child Nutrition, vol 74, pp 91-102. Eds J Bhatia, Z Bhutta & SC Kahlan. Nestlé Nutrition Workshop Series. Freiburg, Germany: Karger. (doi:10.1159/000348417)
61. Fowden AL & Silver M 1995 The effects of thyroid hormones on oxygen and glucose metabolism in the sheep fetus during late gestation. Journal of Physiology 482 203-213.
62. Fowden AL, Li J & Forhead AJ 1998 Glucocorticoids and the preparation for life after birth: are there long term consequences of the life insurance? Proceedings of the Nutrition Society 57 113-122. (doi:10.1079/PNS19980017)
63. Fowden AL, Mapstone J & Forhead AJ 2001a Regulation of glucogenesis by thyroid hormones in fetal sheep during late gestation. Journal of Endocrinology 170 461-469. (doi:10.1677/joe.0.1700461)
64. Fowden AL, Ousey JC & Forhead AJ 2001b Comparative aspects of prepartum maturation; provision of nutrients. Pferdeheilkunde 17 653-658.
65. Fowden AL, Sibley C, Reik W & Constancia M 2006 Imprinted genes, placental development and fetal growth. Hormone Research 65 (Suppl 3) 49-57.
66. Friesema ECH, Jansen J & Visser TJ 2005 Thyroid hormone transporters. Biochemical Society Transactions 33 228-232. (doi:10.1042/BST0330228)
67. Gilbert WM, Eby-Wilkens E, Plopper C, Whitsett JA & Tarantal AF 2001 Fetal monkey surfactants after intra-amniotic or maternal administration of betamethasone and thyroid hormones. Obstetrics and Gynecology 98 466-470. (doi:10.1016/S0029-7844(01)01417-X)
68. Gnanalingham MG, Mostyn A, Forhead AJ, Fowden AL, Symonds ME & Stephenson T 2005 Increased uncoupling protein-2 mRNA during late gestation is dependent on plasma cortisol and tri-iodothyronine. Journal of Physiology 567 283-292. (doi:10.1113/jphysiol.2005.091223)
69. Guerra C, Porras A, Roncero C, Benito M & Fernandez M 1994 Triiodothyronine induces expression of the uncoupling protein in long term fetal rat brown adipocyte primary cultures: role of nuclear thyroid hormone receptor expression. Endocrinology 134 1067-1074.
70. Hall JA, Robich S, Christoffolete MA, Simovic G, Correa-Medina M, Patti ME & Bianco AC 2010 Absence of thyroid hormone activation during development underlies a permanent defect in adaptive thermogenesis. Endocrinology 151 4573-4582. (doi:10.1210/en.2010-0511)
71. Hausman GJ 1992 The influence of thyroxine on the differentiation of adipose tissue and skin during fetal development. Pediatric Research 32 204-211. (doi:10.1203/00006450-199208000-00016)
72. Hausman DB, Hausman GJ & Martin RJ 1996 Endocrine regulation of fetal adipose tissue metabolism in the pig: ontogeny of thyroxine influence. Biology of the Neonate 70 41-51. (doi:10.1159/000244347)
73. Hernandez A, Fiering S, Matinez E, Galton VA & St Germain D 2002 The gene locus encoding iodothyronine deiodinase type 3 (Dio3) is imprinted in the fetus and expresses antisense transcripts. Endocrinology 143 4483-4486. (doi:10.1210/en.2002-220800)
74. Hernandez A, Matinez E, Fiering S, Galton VA & St Germain D 2006 Type 3 deiodinase is critical for the maturation and function of the thyroid axis. Journal of Clinical Investigation 116 476-484. (doi:10.1172/JCI26240)
75. Herpin P, Berthin D, Duchamp C, Dauncey MJ & Le Dividich J 1996 Effect of thyroid status in the perinatal period on oxidative capacities and mitochondrial respiration in porcine liver and skeletal muscle. Reproduction, Fertility, and Development 8 147-155. (doi:10.1071/RD9960147)
76. Heuer H & Visser TJ 2013 The pathophysiological consequences of thyroid hormone transporter deficiencies: insights from mouse models. Biochimica et Biophysica Acta 1830 3974-3978. (doi:10.1016/j.bbagen. 2012.04.009)
77. Hillman NH, Kallaour SG & Jobe A 2012 Physiology of transition from intrauterine to extrauterine life. Clinics in Perinatology 39 769-783. (doi:10.1016/j.clp.2012.09.009)
78. Hopkins PS &Thorburn GD 1972 The effects of foetal thyroidectomy on the development of the ovine foetus. Journal of Endocrinology 54 55-66. (doi:10.1677/joe.0.0540055)
79. Hopkins PS, Wallace AL & Thorburn GD 1975 Thyrotrophin concentrations in the plasma of cattle, sheep and foetal lambs as measured by radioimmunoassay. Journal of Endocrinology 64 271-387. (doi:10.1677/joe.0.0640371)
80. Horn S & Heuer H 2010 Thyroid hormone action during brain development: more questions than answers. Molecular and Cellular Endocrinology 315 19-26. (doi:10.1016/j.mce.2009.09.008)
81. Jansen J, Friesema ECH, Milici C & Visser TJ 2005 Thyroid hormone transporters in health and disease. Thyroid 15 757-768. (doi:10.1089/thy.2005.15.757)
82. Jost A 1979 Fetal hormones and fetal growth. Contributions to Gynecology and Obstetrics 5 1-20.
83. Kester MH, Kaptein E, Van Dijk CH, Roest TJ, Tibboel D, Coughtrie MW & Visser TJ 2002 Characterization of iodothyronine sulfatase activities in human and rat liver and placenta. Endocrinology 143 814-819. (doi:10.1210/endo.143.3.8686)
84. Kilby MD, Gittoes VN, Somerset DA, Clark PM & Franklyn JA 1998 Circulating thyroid hormone concentrations and placental thyroid hormone receptor expression in normal human pregnancy and pregnancy complicated by intrauterine growth restriction (IUGR). Journal of Clinical Endocrinology and Metabolism 83 2964-2971. (doi:10.1210/jcem.83.8.5002)
85. Kilby MD, Gittoes N, McCabe CJ, 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)
86. Klein AH, Reviczky A, Padbury JF & Fisher DA 1983 Effects of changes in thyroid status on tissue respiration in fetal and newborn sheep. American Journal of Physiology 244 E603-E606.
87. Klein AH, Reviczky A & Padbury JF 1984 Thyroid hormone augment catecholamine-stimulated brown adipose tissue thermogenesis in the ovine fetus. Endocrinology 114 1065-1069. (doi:10.1210/endo-114-4-1065)
88. Koopdonk-Kool JM, de Vijlder JJ, Veenboer GJ, Ris-Stalpers C, Kok JH, Vulsma T, Boer K & Visser TJ 1996 Type II and type III deiodinase activity in human placenta as a function of gestational age. Journal of Clinical Endocrinology and Metabolism 81 2154-2158.
89. Kruger M, Sachse C, Zimmermann WH, Eshenhagen T, Klede S & Linke WA 2008 Thyroid hormone regulates developmental titin isoform transitions via the phosphatidylinositol-3-kinase/AKT pathway. Circulation Research 102 439-447. (doi:10.1161/CIRCRESAHA.107.162719)
90. Landers KA, Mortimer RH & Richard K 2013 Transthyretin and the human placenta. Placenta 34 513-517. (doi:10.1016/j.placenta. 2013.04.013)
91. Lanham SA, Fowden AL, Roberts C, Cooper C, Oreffo RO & Forhead AJ 2011 Effects of hypothyroidism on the structure and mechanical properties of bone in the ovine fetus. Journal of Endocrinology 210 189-198. (doi:10.1530/JOE-11-0138)
92. Latimer AM, Hausman GJ, McCusker RH & Buonomo FC 1993 The effects of thyroxine on serum and tissue concentrations on insulin-like growth factors (IGF-I and IGF-II) and IGF binding proteins in the fetal pig. Endocrinology 133 1312-1319.
93. Li H, Patel J, Mortimer RH & Richard K 2012 Ontogenic changes in human placental sodium iodide symporter expression. Placenta 33 946-948. (doi:10.1016/j.placenta.2012.08.002)
94. Liu J, Chen K, Valego NK, Carey LC & Rose JC 2005 Ontogeny and effects of thyroid hormone on b-1-adrenergic receptor mRNA expression in ovine fetal kidney cortex. Journal of the Society for Gynecologic Investigation 12 563-569. (doi:10.1016/j.jsgi.2005.08.007)
95. Lorijn RHW & Longo LD 1980 Clinical and physiological implications of increased fetal oxygen consumption. American Journal of Obstetrics and Gynecology 136 451-457.
96. Lorijn RHW, Nelson JC & Longo LD 1980 Induced fetal hyperthyroidism:cardiac output and oxygen consumption. American Journal of Physiology 239 H302-H307.
97. Loubiere LS, Vasilopoulou E, Bulmer JN, Taylor PM, Stieger B, Verrey F, McCabe CJ, Franklyn JA, Kilby MD & Chan SY 2010 Expression of thyroid hormone transporters in the human placenta and changes associated with intrauterine growth retardation. Placenta 31 295-304. (doi:10.1016/j.placenta.2010.01.013)
98. Loubiere LS, Vasilopoulou E, Glazier JD, Taylor PM, Franklyn JA, Kilby MD & Chan SY 2012 Expression and function of thyroid hormone transporters in the microvillous plasma membrane of human term placental syncytiotrophoblast. Endocrinology 153 6126-6135. (doi:10.1210/en.2012-1753)
99. Mai W, Janier MF, Allioli N, Quignodon L, Chuzel T, Flamart F & Samarut J 2004 Thyroid hormone receptor a is a molecular switch of cardiac function between fetal and postnatal life. PNAS 101 10332-10337. (doi:10.1073/pnas.0401843101)
100. Medina MC, Molina J, Gadea Y, Fachado A, Murillo M, Simovic G, Pileggi A, Hernandez A, Edlind H & Bianco AC 2011 The thyroid hormoneinactivating type III deiodinase is expressed in mouse and human b cells and its targeted inactivation impairs insulin secretion. Endocrinology 152 3717-3727. (doi:10.1210/en.2011-1210)
101. Mendelson CR & Boggaram V 1991 Hormonal control of the surfactant system in fetal lung. Annual Review of Physiology 53 415-440. (doi:10.1146/annurev.ph.53.030191.002215)
102. Mesiano S, Young IR, Baxter RC, Hintz RL, Browne CA & Thorburn GD 1987 Effect of hypophysectomy with and without thyroxine replacement on growth and circulating concentrations of insulin-like growth factors I and II in the fetal lamb. Endocrinology 120 1821-1830. (doi:10.1210/endo-120-5-1821)
103. Metz LD, Seidler FJ, McCook EC & Slotkin TA 1996 Cardiac a-adrenergic receptor expression is regulated by thyroid hormones during a critical developmental period. Journal of Molecular and Cellular Cardiology 28 1033-1044. (doi:10.1006/jmcc.1996.0096)
104. Morreale de Escobar G, Calvo R, Obregon MJ & Escobar Del Rey F 1990 Contribution ofmaternal thyroxine to fetal thyroxine pools in normal rats near term. Endocrinology 126 2765-2767. (doi:10.1210/endo-126-5-2765)
105. Mostyn A, Pearce S, Budge H, Elmes M, Forhead AJ, Fowden AL, Stephenson T & Symonds ME 2003 Influence of cortisol on adipose tissue development in the fetal sheep during late gestation. Journal of Endocrinology 176 23-30. (doi:10.1677/joe.0.1760023)
106. Nagasawa T, Suzuki S, Takeda T & DeGroot LJ 1997 Thyroid hormone receptor b1 expression in developing mouse limbs and face. Endocrinology 138 1276-1281.
107. Ng L, Lybarsky A, Nikonov SS, Ma M, Srinivas M, Kefas B, St Germain DL, Hernandez A, Pugh EN & Forrest D 2010 Type 3 deiodinase, a thyroidhormone-inactivating enzyme, controls survival and maturation of cone photoreceptors. Journal of Neuroscience 30 3347-3357. (doi:10.1523/JNEUROSCI.5267-09.2010)
108. Obregon MJ, Calvo RM, del Ray FE & De Escobar GM 2007 Ontogenesis of thyroid function and interactions with maternal function. In Thyroid gland development and function, Vol 10, pp 86-98. Eds G Van Vliet & M Polak. Endocrine Development. Basal, Switzerland: Karger. (doi:10.1159/000106821)
109. O'Connor DM, Blanche D, Hoggard N, Brookes E, Wooding FB, Fowden AL & Forhead AJ 2007 Developmental control of plasma leptin and adipose leptin mRNA in the ovine fetus during late gestation: role of glucocorticoids and thyroid hormones. Endocrinology 148 3750-3757. (doi:10.1210/en.2007-0310)
110. Olver RE, Schneeberger EE & Walters DV 1981 Epithelial solute permeability, ion transport and tight junction morphology in the developing lung of the fetal lamb. Journal of Physiology 315 395-412.
111. Patel J, Landers K, Li H, Mortimer RH & Richard K 2011 Thyroid hormones and fetal neurological development. Journal of Endocrinology 209 1-8. (doi:10.1530/JOE-10-0444)
112. Pereira DN & Procianoy RS 2003 Effect of perinatal asphyxia on thyroidstimulating hormone and thyroid hormone levels. Acta Paediatrica 92 339-345. (doi:10.1111/j.1651-2227.2003.tb00556.x)
113. 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)
114. Piosik PA, van Groenigen M, van Doorn J, Baas F & Vijlder JJ 1997 Effects of maternal thyroid status on thyroid hormones and growth in congenitally hypothyroid goat fetuses during the second half of gestation. Endocrinology 138 5-11.
115. Polk DH 1995 Thyroid hormone metabolism during development. Reproduction, Fertility, and Development 7 469-477. (doi:10.1071/RD9950469)
116. Polk DH, Callegari CC, Newnham J, Padbury JF, Reviczky A, Fisher DA & Klein AH 1987 Effect of fetal thyroidectomy on newborn thermogenesis in lambs. Pediatric Research 21 453-457. (doi:10.1203/00006450-198705000-00006)
117. Polk DH, Wu S-Y, Wright C, Reviczky AL & Fisher DA 1988 Ontogeny of thyroid hormone effect on tissue 50-monodeiodinase activity in fetal sheep. American Journal of Physiology 254 E337-E341.
118. Polk D, Cheromcha D, Reviczky A & Fisher DA 1989 Nuclear thyroid hormone receptors: ontogeny and thyroid hormone effects in sheep. American Journal of Physiology 256 E543-E549.
119. Polk DH, Reviczky A, Lam RW & Fisher DA 1991 Thyrotropin-releasing hormone in the ovine fetus: ontogeny and effect of thyroid hormone. American Journal of Physiology 260 E53-E58.
120. 3 or norepinephrine stimulate brown adipose tissue thermogenesis in the fetal sheep. Journal of Developmental Physiology 11 171-177.
121. Puig-Domingo M & Vila L 2013 The implications of iodine and its supplementation during pregnancy in fetal brain development. Current Clinical Pharmacology 8 97-109. (doi:10.2174/1574884711308020002)
122. Rae MT, Rhind SM, Kyle CE, Miller DW & Brooks AN 2002 Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. Journal of Endocrinology 173 449-455. (doi:10.1677/joe.0.1730449)
123. Rakover Y, Weiner E, Mosh N & Shalev E 1999 Fetal pituitary negative feedback at early gestational age. Clinical Endocrinology 50 809-814. (doi:10.1046/j.1365-2265.1999.00767.x)
124. Ramminger SJ, Inglis SK, Olver RE & Wilson SM 2002 Hormonal modulation of Na(C) transport in rat fetal distal lung epithelial cells. Journal of Physiology 544 567-577. (doi:10.1113/jphysiol.2002.022459)
125. Richard K, Hume R, Kaptein E, Stanley EL, Visser TJ & Coughtrie MW 2001 Sulfation of thyroid hormone and dopamine during human development:ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain. Journal of Clinical Endocrinology and Metabolism 86 2734-2742.
126. Richards GE, Morrow DA, Thominet JL, Silverman BL & Gluckman PD 1993 The effect of thyroidectomy on growth hormone regulation in the ovine fetus. Journal of Developmental Physiology 19 165-169.
127. Romaguera J, Ramirez M & Adamsons K 1993 Intra-amniotic thyroxine to accelerate fetal maturation. Seminars in Perinatology 17 260-266.
128. 4 transfer does not suffice to prevent the effects of in utero hypothyroidism. Hormone Research 39 1-7. (doi:10.1159/000182686)
129. Santisteban P 2013 Development and anatomy of the hypothalamic-pituitary-thyroid axis. In Werner & Ingbar's The Thyroid: A fundamental and Clinical Text, 10th edn, pp 4-23. Eds LE Braverman & DS Cooper. Lippincott, Williams & Wilkins.
130. Schermer SJ, Bird JA, Lomax MA, Shepherd DA & Symonds ME 1996 Effect of fetal thyroidectomy on brown adipose tissue and thermoregulation in newborn lambs. Reproduction, Fertility, and Development 8 995-1002. (doi:10.1071/RD9960995)
131. Schroder HJ, Huneke B, Klug A, Stegner H, Carstensen M & Leichtweiss HP 1987 Fetal sheep temperatures in utero during cooling and application of triiodothyronine, norepinephrine, propranolol and suxamethonium. Pflügers Archiv 410 376-384. (doi:10.1007/BF00586514)
132. Segar JL, Volk KA, Lipman MH & Scholz TD 2013 Thyroid hormone is required for growth adaptation to pressure load in the ovine fetal heart. Experimental Physiology 98 722-733. (doi:10.1113/expphysiol.2012. 069435)
133. Sferruzzi-Perri AN, Vaughan OR, Forhead AJ & Fowden AL 2013 Hormonal and nutritional drivers of intrauterine growth. Current Opinion in Clinical Nutrition and Metabolic Care 16 298-309. (doi:10.1097/MCO.0b013e32835e3643)
134. Shields BM, Knight BA, Hill A, Hattersley AT & Vaidya B 2011 Fetal thyroid hormone level at birth is associated with fetal growth. Journal of Clinical Endocrinology and Metabolism 96 E934-E938. (doi:10.1210/jc.2010-2814)
135. Silva JE 2011 Physiological importance and control of non-shivering facultative thermogenesis. Frontiers in Bioscience 3 352-371. (doi:10.2741/s156)
136. Spencer GS, Hallett KG, Beerman U & Macdonald AA 1989 Changes in the levels of growth hormone, insulin, cortisol, thyroxine and somatomedin-C/IGF-I with increasing gestational age in the fetal pig and the effects of thyroidectomy in utero. Comparative Biochemistry and Physiology. A, Comparative Physiology 93 467-472. (doi:10.1016/0300-9629(89)90068-6)
137. Stenzel D & Huttner WB 2013 Role of maternal thyroid hormones in the developing neocortex and during human evolution. Frontiers in Neuroanatomy 7 19. (doi:10.3389/fnana.2013.00019)
138. Symonds ME, Mostyn A, Pearce S, Budge H & Stephenson T 2003 Endocrine and nutritional regulation of fetal adipose tissue development. Journal of Endocrinology 179 293-299. (doi:10.1677/joe.0.1790293)
139. Thorburn GD & Hopkins PS 1973 Thyroid function in the foetal lamb. In Foetal and Neonatal Physiology, pp 488-507. Eds RS Comline, KW Cross, GS Dawes & PW Nathanielsz. Cambrige University Press.
140. Thornburg K, Jonker S, O'Tierney P, Chattergoon N, Louey S, Faber J & Giraud G 2011 Regulation of the cardiomyocyte population in the developing heart. Progress in Biophysics and Molecular Biology 106 289-299. (doi:10.1016/j.pbiomolbio.2010.11.010)
141. Thorpe-Beeston JG, Nicolaides KH, Felton CV, Butler J & McGregor AM 1991a 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)
142. Thorpe-Beeston JG, Nicolaides KH, Snijders RJ, Felton CV & McGregor AM 1991b Thyroid function in small for gestational age fetuses. Obstetrics and Gynecology 77 701-706.
143. Torday JS & Dow KE 1984 Synergistic effect of triiodothyronine and dexamethasone on male and female fetal rat lung surfactant synthesis. Developmental Pharmacology and Therapeutics 7 133-139.
144. Tsai C-E, Lin S-P, Ito M, Takagi N, Takada S & Ferguson-Smith AC 2002 Genomic imprinting contributes to thyroid hormone metabolism in the mouse embryo. Current Biology 12 1221-1226. (doi:10.1016/S0960-9822(02)00951-X)
145. van Tuyl M, Blommaart PE, Boer PAJ,Wert SE, Ruijter JM, Islam S, Schnitzer J, Ellison AR, Tibboel D, Moorman AF et al. 2004 Prenatal exposure to thyroid hormones is necessary for normal postnatal development of murine heart and lungs. Developmental Biology 272 103-117. (doi:10.1016/j.ydbio.2004.03.042)
146. Ueta CB, Oskouei BN, Olivares EL, Pinto JR, Correa MM, Simovic G, Simonides WS, Hare JM & Bianco AC 2012 Absence of myocardial thyroid hormone inactivating deiodinase results in restrictive cardiomyopathy in mice. Molecular Endocrinology 26 809-818. (doi:10.1210/me.2011-1325)
147. Vega-Nunez E, Menendez-Hurtado A, Garesse R, Santos A & Perez-Castillo A 1995 Thyroid hormones-regulated brain mitochondrial genes revealed by differential cDNAcloning. Journal of Clinical Investigation 96 893-899. (doi:10.1172/JCI118136)
148. Visser WE, Friesema ECH, Jansen J & Visser TJ 2008 Thyroid hormone transport in and out of cells. Trends in Endocrinology and Metabolism 19 50-56. (doi:10.1016/j.tem.2007.11.003)
149. Vulsma T, Gins MH & de Vijlder JJ 1989 Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to total organification defect or thyroid agenesis. New England Journal of Medicine 321 13-16. (doi:10.1056/NEJM198907063210103)
150. Walker DW & Schuijers JA 1989 Effect of thyroidectomy on cardiovascular responses to hypoxia and tyramine infusion in fetal sheep. Journal of Developmental Physiology 12 337-345.
151. Warburton D, Parton L, Buckley S, Cosico L, Enns G & Saluna T 1988 Combined effects of corticosteroid, thyroid hormones and b-agonists on surfactant, pulmonary mechanics and b-receptor binding in fetal lamb lung. Pediatric Research 24 166-170. (doi:10.1203/00006450-198808000-00005)
152. White P, Burton KA, Fowden AL & Dauncey MJ 2001 Developmental expression analysis of thyroid hormone receptor isoforms reveals new insights into their essential functions in cardiac and skeletal muscles. FASEB Journal 15 1367-1376. (doi:10.1096/fj.00-0725com)
153. Wilson SM, Olver RE & Walters DV 2007 Developmental regulation of luminal lung liquid and electrolyte transport. Respiratory Physiology & Neurobiology 159 247-255. (doi:10.1016/j.resp.2007.10.004)
154. Wrutniak C & Cabello G 1983 Changes in the concentration of thyroxine in the plasma of rat fetuses during late gestation: influence of ligation of the maternal uterine vein and artery. Journal of Endocrinology 99 233-238. (doi:10.1677/joe.0.0990233)
155. 3 mitochondrial pathway. Annals of the New York Academy of Sciences 839 93-100. (doi:10.1111/j.1749-6632. 1998.tb10738.x)
156. Wu S, Polk D, Wong S, Reviczky A, Vu R & Fisher DA 1992 Thyroxine sulphate is a major thyroid hormone metabolite and a potential intermediate in the monodeiodination pathways in fetal sheep. Endocrinology 131 1751-1756.
157. Wu SY, Polk DH, Huang WS, Reviczky A,Wang K & Fisher DA 1993 Sulfate conjugates of iodothyronines in developing sheep: effect of fetal hypothyroidism. American Journal of Physiology 265 E115-E120.
158. Yasuda T, Ohnishi H, Wataki K, Minagawa M, Minamitani K & Niimi H 1999 Outcome of a baby born of a mother with acquired juvenile hypothyroidism having undetectable thyroid hormone concentrations. Journal of Clinical Endocrinology and Metabolism 84 2630-2632.