Acute changes in maternal thyroid hormone induce rapid and transient changes in gene expression in fetal rat brain

Journal of Neuroscience

Volumn 20, Issue 6, 2000, Pages 2255-2265

  Dowling, Amy L S ^a   Martz, Gabriel U ^a   Leonard, Jack L ^b   Zoeller, R Thomas ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Brain development; Cerebral cortex; Congenital hypothyroidism; Differential display; Neuroendocrine specific protein; NSP; Oct 1; POU domain; Thyroid hormone

Indexed keywords

NEUROENDOCRINE SPECIFIC PROTEIN; THYROID HORMONE; THYROID HORMONE RECEPTOR; THYROXINE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN DEVELOPMENT; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THYROID FUNCTION;

EID: 0034653383     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-06-02255.2000     Document Type: Article

References (58)

1. Altman J, Bayer SA (1995) Atlas of prenatal rat brain development. Boca Raton, FL: CRC.
2. Baka I, Ninkina N, Pinon L, Adu J, Davies A, Georgiev G, Buchman V (1996) Intracellular compartmentalization of s-rex/NSP mRNAs in neurons. Mol Cell Neurosci 7:289-303.
3. Bernal J, Pekonen F (1984) Ontogenesis of the nuclear 3,5,3'-triiodothyronine receptor in the human fetal brain. Endocrinology 114:677-679.
4. Boulder Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257-262.
5. Bradley DJ, Young WS, Weinberger C (1989) Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary. Proc Natl Acad Sci USA 86:7250-7254.
6. Bradley DJ, Towle HC, Young WS (1992) 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 12:2288-2302.
7. Calvo R, Obregon MJ, Ruiz de Ona C, Escobar del Rey F, Morreale de Escobar G (1990) Congenital hypothyroidism, as studied in rats. J Clin Invest 86:889-899.
8. Cao XY, Jiang XM, Dou ZH, Murdon AR, Zhang ML, O'Donnell K, Ma T, Kareem A, DeLong N, Delong GR (1994) Timing of vulnerability of the brain to iodine deficiency in endemic cretinism. N Engl J Med 331:1739.
9. Caviness VS, Takahashi T, Nowakowski RS (1995) Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci 18:379-383.
10. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
11. Chopra IJ (1996) Nature, source, and relative significance of circulating thyroid hormones. In: Werner and Ingbar's the thyroid, Ed 7 (Braverman LE, Utiger RD, eds), pp 111-124. Philadelphia: Lippincott-Raven.
12. 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. J Clin Endocrinol Metab 77:1719-1722.
13. DeChiara TM, Brosius J (1987) Neural BC1 RNA: cDNA clones reveal nonrepetitive sequence content. Proc Natl Acad Sci USA 84:2624-2628.
14. Dussault JH, Ruel J (1987) Thyroid hormones and brain development. Annu Rev Physiol 49:321-334.
15. Dyess EM, Segerson TP, Liposits Z, Paull WK, Kaplan MM, Wu P, Jackson IMD, Lechan RM (1988) Triiodothyronine exerts direct cell-specific regulation of thyrotropin-releasing hormone gene expression in the hypothalamic paraventricular nucleus. Endocrinology 123:2291-2297.
16. Everts ME, Docter R, Moerings EPCM, van Koetsveld PM, Visser TJ, de Jong M, Krenning EP, Hennemann G (1994a) Uptake of thyroxine in cultured anterior pituitary cells of euthyroid rats. Endocrinology 134:2490-2497.
17. Everts ME, Visser TJ, Moerings EP, Docter R, van Toor H, Tempelaars AM, de Jong M, Krenning EP, Hennemann G (1994b) Uptake of triiodothyroacetic acid and its effect on thyrotropin secretion in cultured anterior pituitary cells. Endocrinology 135:2700-2707.
18. Everts ME, Visser TJ, Moerings EPCM, Tempelaars AMP, van Toor H, Doctor R, de Jong M, Krenning EP, Hennemann G (1995) Uptake of 3,5',5,5'-tetraiodothyroacetic acid and 3,3',5'-triiodothyronine in cultured rat anterior pituitary cells and their effects on thyrotropin secretion. Endocrinology 136:4454-4461.
19. 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. Eur J Endocrinol 130:97-106.
20. Ferreiro B, Bernai J, Goodyer CG, Branchard CL (1988) Estimation of nuclear thyroid hormone receptor saturation in human fetal brain and lung during early gestation. J Clin Endocrinol Metab 67:853-856.
21. Fisher D, Dussault J, Sack J, Chopra I (1977) Ontogenesis of hypothalamic-pituitary-thyroid function and metabolism in man, sheep, rat. Recent Prog Horm Res 33:59-107.
22. Fisher DA (1999) Hypothyroxinemia in premature infants: is thyroxine treatment necessary? Thyroid 9:715-720.
23. Haddow JE, Palomaki GE, Allan WC, Williams JR, Knight GJ, Gagnon J, O'Heir CE, Mitchell ML, Hermos RJ, Waisbren SE, Fais JD, Klein RZ (1999) Maternal thyroid deficiency during pregnancy and subsequent ncuropsychological development of the child. N Engl J Med 341:549-555.
24. He X, Treacy MN, Simmons DM, Ingraham HA, Swanson LW, Rosenfeld MG (1989) Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature 340:35-42.
25. Hens J, Nuydens R, Geerts H, Senden NHM, Van de Ven WJM, Roebroek AMJ, van de Velde HJK, Ramaekers RCS, Broers JLV (1998) Neuronal differentiation is accompanied by NSP-C expression. Cell Tissue Res 292:229-237.
26. Koenig RJ (1998) Thyroid hormone receptor coactivators and corepressors. Thyroid 8:703-713.
27. Koller KJ, Wolff RS, Warden MK, Zoeller RT (1987) Thyroid hormones regulate levels of thyrotropin-releasing hormone mRNA in the paraventricular nucleus. Proc Natl Acad Sci USA 84:7329-7333.
28. Lakin ND, Palmer R, Lillycrop KA, Howard MK, Burke LC, Thomas NSB, Latchman DS (1995) Down regulation of the octamer binding protein Oct-1 during growth arrest and differentiation of a neuronal cell line. Mol Brain Res 28:47-54.
29. Lazar MA (1993) Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 14:184-193.
30. Lazar MA (1994) Thyroid hormone receptors: update 1994. Endocr Rev Monogr 3:280-283.
31. Lechan RM, Wu P, Jackson IMD, Wolfe H, Cooperman S, Mandel G, Goodman RH (1986) Thyrotropin-releasing hormone precursor: characterization in rat brain. Science 231:159-161.
32. Ledakis P, Tanimura H, Fojo T (1998) Limitations of differential display. Biochem Biophys Res Commun 251:653-656.
33. Leonard JL, Koehrle J (1996) Intracellular pathways of iodothyronine metabolism. In: Werner and Ingbar's the thyroid, Ed 7 (Braverman LE, Utiger RD, eds), pp 125-161. Philadelphia: Lippincott-Raven.
34. Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967-971.
35. Mangelsdorf DJ, Evans RM (1995) The RXR heterodimers and orphan receptors. Cell 83:841-850.
36. Moreau X, Lejeune PJ, Jeanningros R (1999) Kinetics of red blood cell T3 uptake in hypothyroidism with or without hormonal replacement, in the rat. J Endocrinol Invest 22:257-261.
37. Nagasawa T, Takeda T, Minemura K, DeGroot LJ (1997) Oct-1, silencer sequence, and GC box regulate thyroid hormone receptor beta-1 promoter. Mol Cell Endocrinol 130:153-165.
38. Ninkina NN, Baka ID, Buchman VL (1997) Rat and chicken s-rex/NSP mRNA: nuclcotide sequence of main transcripts and expression of splice variants in rat tissues. Gene 184:205-210.
39. Obregon MJ, Mallol J, Pastor R, Morreale de Escobar G, Escobar del Rey F (1984) L-thyroxine and 3,5,3-triiodo-L-thyronine in rat embryos before onset of fetal thyroid function. Endocrinology 114:305-307.
40. Oppenheimer JH, Schwartz HL (1997) Molecular basis of thyroid hormone-dependent brain development. Endocr Rev 18:462-475.
41. Paxinos G, Watson C (1986) The rat brain in stercotaxic coordinates. San Diego: Academic.
42. 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.
43. Pop VJ, Kuijpens JL, van Baar AL, Verkerk G, van Son MM, de Vijlder JJ, Vulsma T, Wiersinga WM, Drexhage HA, Vader HL (1999) Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol 50:149-155.
44. Porterficld SP, Hendrich CE (1992) Tissue iodothyronine levels in fetuses of control and hypothyroid rats at 13 and 16 days gestation. Endocrinology 131:195-200.
45. Roebroek AJM, van de Velde HJK, Van Bokhoven A, Broers JLV, Ramaekers FCS, Van de Ven WJM (1993) Cloning and expression of alternative transcripts of a novel neuroendocrine-specific gene and identification of its 135-kDa translational product. J Biol Chem 268:13439-13447.
46. Rochroek AJM, Contreras B, Pauli IGL, Van de Ven WJM (1998) cDNA cloning, genome organization, and expression of the human TRN2 gene, a member of a gene family encoding reticulons. Genomics 51:98-106.
47. Ruiz de Ona C, Obregon MJ, Escobar del Rey F, Morreale de Escobar G (1988) Developmental changes in rat brain 5'-deiodinase and thyroid hormones during the fetal period: the effects of fetal hypothyroidism and maternal thyroid hormones. Pediatr Res 24:588-594.
48. Scott HC, Sun GY, Zoeller RT (1998) Prenatal ethanol exposure selectively reduces the mRNA encoding alpha-1 thyroid hormone receptor in fetal rat brain. Alcohol Clin Exp Res 22:2111-2117.
49. Senden NH, Timmer ED, Broers JE, van de Velde HJ, Roebroek AJ (1996) Neuroendocrine-specific protein C (NSP-C): subcellular localization and differential expression in relation to NSP-A. Eur J Cell Biol 69:197-213.
50. Tanaka T, Kuwano Y, Kuzumaki T, Ishidawa K, Ogata K (1987) Nucleotide sequence of cloned cDNA specific for ral ribosomal protein L31. Eur J Biochem 162:45-48.
51. Treacy MN, Rosenfeld MG (1992) Expression of a family of POU-domain protein regulatory genes during development of the central nervous system. Annu Rev Neurosci 15:139-165.
52. van de Velde HJK, Roebroek AJM, Senden NHM, Ramaekers FCS, Van de Ven WJM (1994a) NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum. J Cell Sci 107:2403-2416.
53. van de Velde HJK, Roebroek AJM, van Leeuwen FW, Van de Ven WJM (1994b) Molecular analysis of expression in rat brain of NSP-A, a novel neuroendocrine-specific protein of the endoplasmic reticulum. Mol Brain Res 23:81-92.
54. Versloot PM, van der Heide D, Schroder-van der Elst JP, Boogerd L (1998) Maternal thyroxine and 3,5,3'-tri-iodothyronine kinetics in near-term pregnant rats at two different levels of hypothyroidism. Eur J Endocrinol 138:113-119.
55. Vulsma T, Gons MH, de Vijlder J (1989) Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect of thyroid agenesis. N Engl J Med 321:13-16.
56. Wan JS, Erlander MG (1997) Cloning differentially expressed genes by using differential display and subtractive hybridization. Methods Mol Biol 85:45-68.
57. Wieczorek DF, Hughes SR (1991) Developmentally regulated cDNA expressed exclusively in neural tissue. Mol Brain Res 10:33-41.
58. Zoeller RT, Wolff RS, Koller KJ (1988) Thyroid hormone regulation of messenger rihonuclcic acid encoding thyrotropin (TSH)-releasing hormone is independent of the pituitary gland and TSH. Mol Endocrinol 2:248-252.