Maternal thyroid hormones are transcriptionally active during embryo-foetal development: Results from a novel transgenic mouse model

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 10, 2010, Pages 2417-2435

  Nucera, Carmelo ^a   Muzzi, Patrizia ^b   Tiveron, Cecilia ^c,d   Farsetti, Antonella ^c,e   Regina, Federico La ^d   Foglio, Benedetta ^b   Shih, Shou Ching ^f   Moretti, Fabiola ^e   Pietra, Linda Della ^c   Mancini, Francesca ^c,e   Sacchi, Ada ^c   Trimarchi, Francesco ^g   Vercelli, Alessandro ^b   Pontecorvi, Alfredo ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF MESSINA   (Italy)

Author keywords

Central nervous system; Embryonic development; Maternal thyroid hormone; Reporter gene; Thyroid receptors; Thyroid responsive element; Transgenic mouse

Indexed keywords

BETA GALACTOSIDASE; THYROID HORMONE;

ANIMAL; ARTICLE; C57BL MOUSE; CENTRAL NERVOUS SYSTEM; DBA MOUSE; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; IMMUNOHISTOCHEMISTRY; LACTOSE OPERON; MALE; METABOLISM; MOUSE; PREGNANCY; PRENATAL DEVELOPMENT; PROMOTER REGION; REPORTER GENE; TRANSCRIPTION INITIATION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; BETA-GALACTOSIDASE; CENTRAL NERVOUS SYSTEM; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REPORTER; GENETIC ENGINEERING; IMMUNOHISTOCHEMISTRY; LAC OPERON; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; PREGNANCY; PROMOTER REGIONS, GENETIC; THYROID HORMONES; TRANSCRIPTIONAL ACTIVATION; TRANSGENES;

MUS; MUS MUSCULUS;

EID: 78049279356     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00947.x     Document Type: Article

References (106)

1. Oppenheimer JH, Koerner D, Schwartz HL, et al Specific nuclear triiodothyronine binding sites in rat liver and kidney. J Clin Endocrinol Metab. 1972; 35: 330-3.
2. Galton VA, Wood ET, St Germain EA, et al Thyroid hormone homeostasis and action in the type 2 deiodinase-deficient rodent brain during development. Endocrinology. 2007; 148: 3080-8.
3. Gereben B, Zavacki AM, Ribich S, et al Cellular and molecular basis of deiodinase regulated thyroid hormone signaling. Endocr Rev. 2008; 29: 898-38.
4. Visser TJ. Thyroid hormone transporters. Horm Res. 2007; 68: 28-30.
5. Dumitrescu AM, Refetoff S. Novel biological and clinical aspects of thyroid hormone metabolism. Endocr Dev. 2007; 10: 127-39.
6. Brent GA. The molecular basis of thyroid hormone action. N Engl J Med. 1994; 331: 847-53.
7. Koibuchi N, Chin WW. Thyroid hormone action and brain development. Trends Endocrinol Metab. 2000; 11: 123-8.
8. Wu Y, Koenig RJ. Gene regulation by thyroid hormone. Trends Endocrinol Metab. 2000; 11: 207-11.
9. Hu X, Lazar MA. Transcriptional repression by nuclear hormone receptors. Trends Endocrinol Metab. 2000; 11: 6-10.
10. Astapova I, Lee LJ, Morales C, et al The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo. Proc Natl Acad Sci USA. 2008; 105: 19544-9.
11. Obregon MJ, Mallol J, Pastor R, et al L-thyroxine and 3, 5, 3'-triodo-L-thyronine in rat embryos before onset of fetal thyroid function. Endocrinology. 1984; 114: 305-7.
12. Porterfield SP, Hendrich CE. Tissue iodothyronine levels in fetuses of control and hypothyroid rats at 13 and 16 days gestation. Endocrinology. 1992; 131: 195-200.
13. Contempre B, Jauniaux E, Calvo R, et al Detection of thyroid hormones in human embryonic cavities during the first trimester of pregnancy. J Clin Endocrinol Metab. 1993; 77: 1719-22.
14. Vulsma T, Gons MH, De Vijlder JJ. Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. N Engl J Med. 1989; 321: 13-6.
15. Bernal J, Pekonen F. Ontogenesis of the nuclear 3, 5, 3'-triiodothyronine receptor in the human fetal brain. Endocrinology. 1984; 114: 677-9.
16. Ferreiro B, Bernal J, Goodyer CG, Branchard CL. Estimation of nuclear thyroid hormone receptor saturation in human fetal brain and lung during early gestation. J Clin Endocrinol Metab. 1988; 67: 853-6.
17. Zhang J, Lazar MA. The mechanism of action of thyroid hormones. Annu Rev Physiol. 2000; 62: 439-66.
18. Anselmo J, Cao D, Karrison T, et al Fetal loss associated with excess thyroid hormone exposure. JAMA. 2004; 292: 691-5.
19. Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Role of thyroid hormone during early brain development. Eur J Endocrinol. 2004; 151: U25-37.
20. Oppenheimer JH, Schwartz HL. Molecular basis of thyroid hormone-dependent brain development. Endocr Rev. 1997; 18: 462-75.
21. Manzano J, Bernal J, Morte B. Influence of thyroid hormones on maturation of rat cerebellar astrocytes. Int J Dev Neurosci. 2007; 25: 171-9.
22. Dowling AL, Iannacone EA, Zoeller RT. Maternal hypothyroidism selectively affects the expression of neuroendocrine-specific protein A messenger ribonucleic acid in the proliferative zone of the fetal rat brain cortex. Endocrinology. 2001; 142: 390-9.
23. Dowling AL, Martz GU, Leonard JL, Zoeller RT. Acute changes in maternal thyroid hormone induce rapid and transient changes in gene expression in fetal rat brain. J Neurosci. 2000; 20: 2255-65.
24. Lucio RA, Garcia JV, Ramon Cerezo J, et al The development of auditory callosal connections in normal and hypothyroid rats. Cereb Cortex. 1997; 7: 303-16.
25. De Escobar GM, Obregon MJ, Del Rey FE. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab. 2004; 18: 225-48.
26. Zoeller RT. Transplacental thyroxine and fetal brain development. J Clin Invest. 2003; 111: 954-7.
27. Morreale de Escobar G, Ruiz de Ona C, Obregon MJ, et al Models of iodine deficiency. In: Delong GR, Robbins J, Condiffe PG, editors. Iodine and the brain. New York: Plenum Press; 1989. pp. 187-201.
28. Berbel P, Mestre JL, Santamaria A, et al 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. 2009; 19: 511-9.
29. Zimmermann MB. Iodine deficiency in pregnancy and the effects of maternal iodine supplementation on the offspring: a review. Am J Clin Nutr. 2009; 89668S-72S.
30. Berbel P, Obregon MJ, Bernal J, et al Iodine supplementation during pregnancy: a public health challenge. Trends Endocrinol Metab. 2007; 18: 338-43.
31. Glinoer D. Clinical and biological consequences of iodine deficiency during pregnancy. Endocr Dev. 2007; 10: 62-85.
32. Glinoer D, Delange F. The potential repercussions of maternal, fetal, and neonatal hypothyroxinemia on the progeny. Thyroid. 2000, 10: 871-87.
33. Lavado-Autric R, Auso E, Garcia-Velasco JV, et al Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest. 2003; 111: 1073-82.
34. Calvo RM, Jauniaux E, Gulbis B, et al Fetal tissues are exposed to biologically relevant free thyroxine concentrations during early phases of development. J Clin Endocrinol Metab. 2002; 87: 1768-77.
35. Kilby MD, Gittoes N, McCabe C, et al Expression of thyroid receptor isoforms in the human fetal central nervous system and the effects of intrauterine growth restriction. Clin Endocrinol. 2000; 53: 469-77.
36. Bradley DJ, Towle HC, Young WS. Spatial and temporal expression of alpha- and beta-thyroid hormone receptor mRNAs, including the beta 2-subtype, in the developing mammalian nervous system. J Neurosci. 1992; 12: 2288-302.
37. Strait KA, Schwartz HL, Perez-Castillo A, Oppenheimer JH. Relationship of c-erbA mRNA content to tissue triiodothyronine nuclear binding capacity and function in developing and adult rats. J Biol Chem. 1990; 265: 10514-21.
38. Hodin RA, Lazar MA, Chin WW. Differential and tissue-specific regulation of the multiple rat c-erbA messenger RNA species by thyroid hormone. J Clin Invest. 1990; 85: 101-5.
39. Farsetti A, Desvergne B, Hallenbeck P, et al Characterization of myelin basic protein thyroid hormone response element and its function in the context of native and heterologous promoter. J Biol Chem. 1992; 267: 15784-8.
40. Farsetti A, Mitsuhashi T, Desvergne B, et al Molecular basis of thyroid hormone regulation of myelin basic protein gene expression in rodent brain. J Biol Chem. 1991; 266: 23226-32.
41. Takahashi N, Roach A, Teplow DB, et al Cloning and characterization of the myelin basic protein gene from mouse: one gene can encode both 14 kd and 18.5 kd MBPs by alternate use of exons. Cell. 1985; 42: 139-48.
42. Desvergne B, Petty KJ, Nikodem VM. Functional characterization and receptor binding studies of the malic enzyme thyroid hormone response element. J Biol Chem. 1991; 266: 1008-13.
43. 3rd ed. Cold Spring Harbor: CSHL Press; 2003.
44. Shih SC, Smith LE. Quantitative multi-gene transcriptional profiling using real-time PCR with a master template. Exp Mol Pathol. 2005; 79: 14-22.
45. Schneider MJ, Fiering SN, Pallud SE, et al Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Mol Endocrinol. 2001; 15: 2137-48.
46. Pohlenz J, Maqueem A, Cua K, et al Improved radioimmunoassay for measurement of mouse thyrotropin in serum: strain differences in thyrotropin concentration and thyrotroph sensitivity to thyroid hormone. Thyroid. 1999; 9: 1265-71.
47. Vernet M, Bonnerot C, Briand P, Nicolas, JF. Application of LacZ gene fusions to preimplantation development. Methods Enzymol. 1993; 225: 434-51.
48. Signoretti S, Pires MM, Lindauer M, et al p63 regulates commitment to the prostate cell lineage. Proc Natl Acad Sci USA. 2005; 102: 11355-60.
49. Spergel DJ, Kruth U, Shimshek DR, et al Using reporter genes to label selected neuronal populations in transgenic mice for gene promoter, anatomical, and physiological studies. Prog Neurobiol. 2001; 63: 673-86.
50. Ausò 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: 4037-47.
51. Zappone MV, Galli R, Catena R, et al Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development. 2000; 127: 2367-82.
52. Huo B, Dozin B, Nikodem VM. Identification of a nuclear protein from rat developing brain as heterodimerization partner with thyroid hormone receptor-beta. Endocrinology. 1997; 138: 3283-89.
53. Quignodon L, Legrand C, Allioli N, et al Thyroid hormone signaling is highly heterogeneous during pre- and postnatal brain development. J Mol Endocrinol. 2004; 33: 467-76.
54. Pombero A, Valdes L, Vieira C, Martinez S. Developmental mechanisms and experimental models to understand forebrain malformative diseases. Genes Brain Behav. 2007; 6: 45-52.
55. Chan SY, Franklyn JA, Pemberton HN, et al Monocarboxylate transporter 8 expression in the human placenta: the effects of severe intrauterine growth restriction. J Endocrinol. 2006; 189: 465-71.
56. Mortimer RH, Galligan JP, Cannell GR, et al Maternal to fetal thyroxine transmission in the human term placenta is limited by inner ring deiodination. J Clin Endocrinol Metab. 1996; 81: 2247-9.
57. Huang SA, Dorfman DM, Genest DR, et al Type 3 iodothyronine deiodinase is highly expressed in the human uteroplacental unit and in fetal epithelium. J Clin Endocrinol Metab. 2003; 88: 1384-8.
58. St Germain DL, Galton VA, Hernandez A. Minireview: defining the roles of the iodothyronine deiodinases: current concepts and challenges. Endocrinology. 2009; 150: 1097-107.
59. Chan S, Kachilele S, Hobbs E, et al Placental iodothyronine deiodinase expression in normal and growth-restricted human pregnancies. J Clin Endocrinol Metab. 2003; 88: 4488-95.
60. Friesema EC, Ganguly S, Abdalla A, et al Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J Biol Chem. 2003; 278: 40128-35.
61. Koopdonk-Kool JM, De Vijlder JJ, Veenboer GJ, et al Type II and type III deiodinase activity in human placenta as a function of gestational age. J Clin Endocrinol Metab. 1996; 81: 2154-8.
62. Bernal J. Thyroid hormones and brain development. Vitam Horm. 2005; 71: 95-122.
63. Bernal J. Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab. 2007; 3: 249-59.
64. Siegfried Z, Eden S, Mendelsohn M, et al DNA methylation represses transcription in vivo. Nat Genet. 1999; 22: 203-6.
65. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet. 2009; 10: 295-304.
66. Palmiter RD, Brinster RL. Germ-line transformation of mice. Annu Rev Genet. 1986; 20: 465-99.
67. Obregon MJ, Calvo RM, Del Rey FE, De Escobar GM. Ontogenesis of thyroid function and interactions with maternal function. Endocr Dev. 2007; 10: 86-98.
68. Forrest D. The developing brain and maternal thyroid hormone: finding the links. Endocrinology. 2004; 145: 4034-6.
69. Yeh KY, Moog M. Influence of the thyroid and adrenal glands on the growth of the intestine of the suckling rat, and on the development of intestinal alkaline phosphatase and disaccharidase activities. J Exp Zool. 1977; 2000: 337-47.
70. Wall AJ, Middleton WR, Pearse AG, Booth CC. Intestinal mucosal hyperplasia following induced hyperthyroidism in the rat. Virchows Arch B Cell Pathol. 1970; 6: 79-87.
71. Leblond CP, Carriere R. The effect of growth hormone and thyroxine on the mitotic rate of the intestinal mucosa of the rat. Endocrinology. 1955; 56: 261-6.
72. Tutton PJ. The influence of thyroidectomy and of triiodothyronine administration on epithelial cell proliferation in the jejunum of rat. Virchows Arch B Cell Pathol. 1976; 20: 139-42.
73. Malo MS, Zhang W, Alkhoury F, et al Thyroid hormone positively regulates the enterocyte differentiation marker intestinal alkaline phosphatase gene via an atypical response element. Mol Endocrinol. 2004; 18: 1941-62.
74. Plateroti M, Chassande O, Fraichard A, et al Involvement of T3Ralpha- and beta-receptor subtypes in mediation of T3 functions during postnatal murine intestinal development. Gastroenterology. 1999; 116: 1367-78.
75. Gauthier K, Chassande O, Plateroti M, et al Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J. 1999; 18: 623-31.
76. Plateroti M, Gauthier K, Domon-Dell C, et al Functional interference between thyroid hormone receptor alpha (TRalpha) and natural truncated TRDeltaalpha isoforms in the control of intestine development. Mol Cell Biol. 2001; 21: 4761-72.
77. Fraichard A, Chassande O, Plateroti M, et al The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J. 1997; 16: 4412-20.
78. Kress E, Rezza A, Nadjar J, et al The frizzled-related sFRP2 gene is a target of thyroid hormone receptor alpha1 and activates beta-catenin signaling in mouse intestine. J Biol Chem. 2009; 284: 1234-41.
79. Plateroti M, Kress E, Mori JI, et al Thyroid hormone receptor alpha1 directly controls transcription of the beta-catenin gene in intestinal epithelial cells. Mol Cell Biol. 2006; 26: 3204-14.
80. Nagasawa T, Suzuki S, Takeda T, et al Thyroid hormone receptor beta 1 expression in developing mouse limbs and face. Endocrinology. 1997; 138: 1276-81.
81. Crenshaw EB 3rd, Russo AF, Swanson LW, et al Neuron-specific alternative RNA processing in transgenic mice expressing a metallothionein-calcitonin fusion gene. Cell. 1987; 49: 389-98.
82. Heuer H, Visser TJ. Minireview: pathophysiological importance of thyroid hormone transporters. Endocrinology. 2009; 150: 1078-83.
83. Dumitrescu A, Liao, XH, Weiss RE, et al Tissue-specific thyroid hormone deprivation and excess in monocarboxylate transporter (mct) 8-deficient mice. Endocrinology. 2006; 147: 4036-43.
84. Heuer H, Maier MK, Iden S, et al The monocarboxylate transporter 8 linked to human psychomotor retardation is highly expressed in thyroid hormone-sensitive neuron populations. Endocrinology. 2005; 146: 1701-6.
85. Friesema EC, Grueters A, Biebermann H, et al Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet. 2004; 364: 1435-7.
86. Köhrle J. The deiodinase family: selenoenzymes regulating thyroid hormone availability and action. Cell Mol Life Sci. 2000; 57: 1853-63.
87. Ceballos A, Belinchon MM, Sanchez-Mendoza E, et al Importance of monocarboxylate transporter 8 for the blood-brain barrier-dependent availability of 3, 5, 3'-triiodo-L-thyronine. Endocrinology. 2009; 150: 2491-6.
88. Oetting A, Yen PM. New insights into thyroid hormone action. Best Pract Res Clin Endocrinol Metab. 2007; 21: 193-208.
89. Koibuchi N. The role of thyroid hormone on cerebellar development. Cerebellum. 2008; 7: 530-3.
90. Lazar MA. Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev. 1993; 14: 184-93.
91. Iskaros J, Pickard M, Evans I, et al Thyroid hormone receptor gene expression in first trimester human fetal brain. J Clin Endocrinol Metab. 2000; 85: 2620-3.
92. Jones I, Srinivas M, Ng L, et al The thyroid hormone receptor beta gene: structure and functions in the brain and sensory systems. Thyroid. 2003; 13: 1057-68.
93. Forrest D, Erway LC, Ng L, et al Thyroid hormone receptor beta is essential for development of auditory function. Nat Genet. 1996; 13: 354-7.
94. Rusch A, Erway LC, Oliver D, et al Thyroid hormone receptor beta-dependent expression of a potassium conductance in inner hair cells at the onset of hearing. Proc Natl Acad Sci USA. 1998; 95: 15758-62.
95. Rusch A, Ng L, Goodyear R, et al Retardation of cochlear maturation and impaired hair cell function caused by deletion of all known thyroid hormone receptors. J Neurosci. 2001; 21: 9792-800.
96. Ng L, Hurley JB, Dierks B, et al A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet. 2001; 27: 94-8.
97. Forrest D, Reh TA, Rusch A. Neurodevelopmental control by thyroid hormone receptors. Curr Opin Neurobiol. 2002; 12: 49-56.
98. Baas D, Legrand C, Samarut J, et al Persistence of oligodendrocyte precursor cells and altered myelination in optic nerve associated to retina degeneration in mice devoid of all thyroid hormone receptors. Proc Natl Acad Sci USA. 2002; 99: 2907-11.
99. Gothe S, Wang Z, Ng L, et al Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev. 1999; 13: 1329-41.
100. Forrest D, Sjoberg M, Vennstrom B. Contrasting developmental and tissue-specific expression of alpha and beta thyroid hormone receptor genes. EMBO J. 1990; 9: 1519-28.
101. Sap J, Munoz A, Schmitt J, et al Repression of transcription mediated at a thyroid hormone response element by the v-erb-A oncogene product. Nature. 1989; 340: 242-4.
102. Mai W, Janier, MF, Allioli N, et al Thyroid hormone receptor alpha is a molecular switch of cardiac function between fetal and postnatal life. Proc Natl Acad Sci USA. 2004; 101: 10332-7
103. Morte B, Manzano J, Scanlan T, et al Deletion of the thyroid hormone receptor alpha 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc Natl Acad Sci USA. 2002; 99: 3985-9.
104. Koenig RJ, Lazar MA, Hodin, RA, et al Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing. Nature. 1989; 337: 659-61.
105. Lazar MA, Hodin RA, Chin WW. Human carboxyl-terminal variant of alpha-type c-erbA inhibits trans-activation by thyroid hormone receptors without binding thyroid hormone. Proc Natl Acad Sci USA. 1989; 86: 7771-4.
106. Farsetti A, Lazar J, Phyillaier M, et al Active repression by thyroid hormone receptor splicing variant alpha2 requires specific regulatory elements in the context of native triiodothyronine-regulated gene promoters. Endocrinology. 1997; 138: 4705-12.