T3 differentially regulates TRH expression in developing hypothalamic neurons in vitro

Brain Research

Volumn 1305, Issue , 2009, Pages 20-30

  Carreón Rodríguez, Alfonso ^a   Charli, Jean Louis ^a   Pérez Martínez, Leonor ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Development; Gene expression; Hypothalamus; Neuronal differentiation; TRH

Indexed keywords

LIOTHYRONINE; MESSENGER RNA; PROTIRELIN; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA;

AGE; ANIMAL; ARTICLE; CELL CULTURE; DRUG EFFECT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HYPOTHALAMUS; MALE; METABOLISM; NERVE CELL; NONPARAMETRIC TEST; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; UPREGULATION; WESTERN BLOTTING; WISTAR RAT;

AGE FACTORS; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOTHALAMUS; MALE; NEURONS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STATISTICS, NONPARAMETRIC; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA; THYROTROPIN-RELEASING HORMONE; TIME FACTORS; TRIIODOTHYRONINE; UP-REGULATION;

EID: 73949103268     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.09.042     Document Type: Article

References (65)

1. Al-Bader, M.D., Al-Sarraf, H.A., 2005. Housekeeping gene expression during fetal brain development in the rat-validation by semi-quantitative RT-PCR. Brain Res. Dev. Brain Res. 156, 38-45. (Pubitemid 40603279)
2. Baram, T.Z., Lerner, S.P., 1991. Ontogeny of corticotropin releasing hormone gene expression in rat hypothalamus - comparison with somatostatin. Int. J. Dev. Neurosci. 9, 473-478.
3. Bergh, J.J., Lin, H.Y., Lansing, L., Mohamed, S.N., Davis, F.B., Mousa, S., Davis, P.J., 2005. Integrin avb3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 146, 2864-2871. (Pubitemid 41002793)
4. Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein - dye binding. Anal. Biochem. 72, 248-254.
5. Bradley, D.J., Towle, H.C., Young 3rd, W.S., 1992. Spatial and temporal expression of alpha- and beta-thyroid hormone receptormRNAs, including the beta 2-subtype, in the developing mammalian nervous system. J. Neurosci. 12, 2288-2302.
6. Burgunder, J.M., Taylor, T., 1989. Ontogeny of thyrotropin-releasing hormone gene expression in the rat diencephalon. Neuroendocrinology 49, 631-640. (Pubitemid 19154616)
7. Buzzard, J.J., Morrison, J.R., O', bryan, M.K., Song, Q., Wreford, N.G., 2000. Developmental expression of thyroid hormone receptors in the rat testis. Biol. Reprod. 62, 664-669. (Pubitemid 30118307)
8. Calza, L., Forrest, D., Vennstrom, B., Hökfelt, T., 2000. Expression of peptides and other neurochemical markers in hypothalamus and olfactory bulb of mice devoid of all known thyroid hormone receptors. Neuroscience 101, 1001-1012.
9. Clerget-Froidevaux, M.S., Seugnet, I., Demeneix, B.A., 2004. Thyroid status co-regulates thyroid hormone receptor and co-modulator genes specifically in the hypothalamus. FEBS Lett. 569, 341-345. (Pubitemid 38844642)
10. Cote-Velez, A., Perez-Martinez, L., Charli, J.L., Joseph-Bravo, P., 2008. The PKC and ERK/MAPK pathways regulate glucocorticoid action on TRH transcription. Neurochem. Res. 33, 1582-1591.
11. Chan, S., Kilby, M.D., 2000. Thyroid hormone and central nervous system development. J. Endocrinol. 165, 1-8. (Pubitemid 30210560)
12. Danielson, P.E., Forss-Petter, S., Brow, M.A., Calavetta, L., Douglass, J., Milner, R.J., Sutcliffe, J.G., 1988. p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7, 261-267.
13. Davis, P.J., Shih, A., Lin, H.Y., Martino, L.J., Davis, F.B., 2000. Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J. Biol. Chem. 275, 38032-38039. (Pubitemid 32004926)
14. Davis, P.J., Davis, F.B., Cody, V., 2005. Membrane receptors mediating thyroid hormone action. Trends Endocrinol. Metab. 16, 419-435.
15. Davis, P.J., Leonard, J.L., Davis, F.B., 2008. Mechanisms of nongenomic actions of thyroid hormone. Front. Neuroendocrinol. 29, 211-218. (Pubitemid 351467119)
16. Dias, A.C., Modulo, C.M., Jorge, A.G., Braz, A.M., Jordao Jr., A.A., Filho, R.B., De Paula, J.S., Rocha, E.M., 2007. Influence of thyroid hormone on thyroid hormone receptor beta-1 expression and lacrimal gland and ocular surface morphology. Invest. Ophthalmol. Vis. Sci. 48, 3038-3042. (Pubitemid 351261145)
17. Dupre, S.M., Guissouma, H., Flamant, F., Seugnet, I., Scanlan, T.S., Baxter, J.D., Samarut, J., Demeneix, B.A., Becker, N., 2004. Both thyroid hormone receptor (TR)beta 1 and TR beta 2 isoforms contribute to the regulation of hypothalamic thyrotropin-releasing hormone. Endocrinology 145, 2337-2345. (Pubitemid 38535063)
18. Forrest, D., Reh, T.A., Rusch, A., 2002. Neurodevelopmental control by thyroid hormone receptors. Curr. Opin. Neurobiol. 12, 49-56. (Pubitemid 34175274)
19. Friedrichsen, S., Christ, S., Heuer, H., Schafer, M.K., Mansouri, A., Bauer, K., Visser, T.J., 2003. Regulation of iodothyronine deiodinases in the Pax8-/- mouse model of congenital hypothyroidism. Endocrinology 144, 777-784. (Pubitemid 36262844)
20. Gahr, M., 2004. Hormone-dependent neural plasticity in the juvenile and adult song system: what makes a successful male? Ann. N. Y. Acad. Sci. 1016, 684-703. (Pubitemid 38951491)
21. Garza, R., Puymirat, J., Dussault, J.H., 1990. Influence of soluble environmental factors on the development of fetal brain acetylcholinesterase- positive neurons cultured in a chemically defined medium: comparison with the effects of L-triiodothyronine (L-T3). Brain Res. Dev. Brain Res. 56, 160-168. (Pubitemid 20364124)
22. Glass, C.K., Rosenfeld, M.G., 2000. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14, 121-141. (Pubitemid 30070977)
23. Guerra-Crespo, M., Ubieta, R., Joseph-Bravo, P., Charli, J.L., Perez-Martinez, L., 2001. BDNF increases the early expression of TRH mRNA in fetal TrkB+ hypothalamic neurons in primary culture. Eur. J. Neurosci. 14, 483-494. (Pubitemid 34203456)
24. Hong, S.H., Wong, C.W., Privalsky, M.L., 1998. Signaling by tyrosine kinases negatively regulates the interaction between transcription factors and SMRT (silencing mediator of retinoic acid and thyroid hormone receptor) corepressor. Mol. Endocrinol. 12, 1161-1171. (Pubitemid 30659043)
25. Ishii, S., Yamada, M., Satoh, T., Monden, T., Hashimoto, K., Shibusawa, N., Onigata, K., Morikawa, A., Mori, M., 2004. Aberrant dynamics of histone deacetylation at the thyrotropin-releasing hormone gene in resistance to thyroid hormone. Mol. Endocrinol. 18, 1708-1720. (Pubitemid 38859578)
26. Jingami, H., Mizuno, N., Takahashi, H., Shibahara, S., Furutani, Y., Imura, H., Numa, S., 1985. Cloning and sequence analysis of cDNA for rat corticotropin-releasing factor precursor. FEBS Lett. 191, 63-66. (Pubitemid 16234144)
27. Joseph-Bravo, P., Perez-Martinez, L., Lezama, L., Morales-Chapa, C., Charli, J.L., 2002. An improved method for the expression of TRH in serum-supplemented primary cultures of fetal hypothalamic cells. Brain Res. Brain Res. Protoc. 9, 93-104. (Pubitemid 34595441)
28. Kalb, R.G., Hockfield, S., 1992. Activity-dependent development of spinal cord motor neurons. Brain Res. Brain Res. Rev. 17, 283-289.
29. Karolyi, I.J., Dootz, G.A., Halsey, K., Beyer, L., Probst, F.J., Johnson, K.R., Parlow, A.F., Raphael, Y., Dolan, D.F., Camper, S.A., 2007. Dietary thyroid hormone replacement ameliorates hearing deficits in hypothyroid mice. Mamm. Genome 18, 596-608. (Pubitemid 47497925)
30. Koenig, R.J., Warne, R.L., Brent, G.A., Harney, J.W., Larsen, P.R., Moore, D.D., 1988. Isolation of a cDNA clone encoding a biologically active thyroid hormone receptor. Proc. Natl. Acad. Sci. U. S. A. 85, 5031-5035.
31. Koibuchi, N., Iwasaki, T., 2006. Regulation of brain development by thyroid hormone and its modulation by environmental chemicals. Endocr. J. 53, 295-303. (Pubitemid 43988157)
32. Koibuchi, N., Jingu, H., Iwasaki, T., Chin, W.W., 2003. Current perspectives on the role of thyroid hormone in growth and development of cerebellum. Cerebellum 2, 279-289. (Pubitemid 38280285)
33. Koller, K.J., Wolff, R.S., Warden, M.K., Zoeller, R.T., 1987. Thyroid hormones regulate levels of thyrotropin-releasing-hormone mRNA in the paraventricular nucleus. Proc. Natl. Acad. Sci. U. S. A. 84, 7329-7333. (Pubitemid 18017339)
34. Langlois, M.F., Zanger, K., Monden, T., Safer, J.D., Hollenberg, A.N., Wondisford, F.E., 1997. A unique role of the beta-2 thyroid hormone receptor isoform in negative regulation by thyroid hormone. Mapping of a novel amino-terminal domain i mportant for ligand-independent activation. J. Biol. Chem. 272, 24927-24933. (Pubitemid 27415668)
35. Leader, J.E., Wang, C., Fu, M., Pestell, R.G., 2006. Epigenetic regulation of nuclear steroid receptors. Biochem. Pharmacol. 72, 1589-1596. (Pubitemid 44666731)
36. Lechan, R.M., Wu, P., Jackson, I.M., Wolf, H., Cooperman, S., Mandel, G., Goodman, R.H., 1986. Thyrotropin-releasing hormone precursor: characterization in rat brain. Science 231, 159-161. (Pubitemid 16154707)
37. Lemkine, G.F., Raj, A., Alfama, G., Turque, N., Hassani, Z., Alegria-Prevot, O., Samarut, J., Levi, G., Demeneix, B.A., 2005. Adult neural stem cell cycling in vivo requires thyroid hormone and its alpha receptor. FASEB J. 19, 863-865. (Pubitemid 40617410)
38. Lezoualc'h, F., Hassan, A., Abdel-Tawab, H., Puymirat, J., Demeneix, B.A., 1994. Precocious auto-induction of thyroid hormone receptors in embryonic chick hypothalamic neurons. Neurosci. Lett. 180, 197-202. (Pubitemid 24333902)
39. Loudes, C., Faivre-Bauman, A., Barret, A., Grouselle, D., Puymirat, J., Tixier-Vidal, A., 1983. Release of immunoreactive TRH in serum-free cultures of mouse hypothalamic cells. Dev. Brain Res. 9, 231-234.
40. Markakis, E.A., 2002. Development of the neuroendocrine hypothalamus. Front. Neuroendocrinol. 23, 257-291. (Pubitemid 34856515)
41. Mitsuhashi, T., Tennyson, G., Nikodem, V., 1988. Nucleotide sequence of novel cDNAs generated by alternative splicing of a rat thyroid hormone receptor gene transcript. Nucleic Acids Res. 16, 5697.
42. Munoz, A., Wrighton, C., Seliger, B., Bernal, J., Beug, H., 1993. Thyroid hormone receptor/c-erbA: control of commitment and differentiation in the neuronal/chromaffin progenitor line PC12. J. Cell Biol. 121, 423-438. (Pubitemid 23110885)
43. Niquet, J., Perez-Martinez, L., Guerra, M., Grouselle, D., Joseph-Bravo, P., Charli, J., 2000. Extracellular matrix proteins increase the expression of pro-TRH and pro-protein convertase PC1 in fetal hypothalamic neurons in vitro. Brain Res. Dev. Brain Res. 120, 49-56. (Pubitemid 30155865)
44. Obregon, M.J., 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. (Pubitemid 14221908)
45. Perez-Martinez, L., Jaworski, D.M., 2005. Tissue inhibitor of metalloproteinase-2 promotes neuronal differentiation by acting as an anti-mitogenic signal. J. Neurosci. 25, 4917-4929. (Pubitemid 40712835)
46. Perez-Martinez, L., Charli, J.L., Joseph-Bravo, P., 2001. Development of pro-TRH gene expression in primary cultures of fetal hypothalamic cells. Brain Res. Dev. Brain Res. 130, 73-81. (Pubitemid 32830974)
47. Porterfield, S.P., Hendrich, C.E., 1992. Tissue iodothyronine levels in fetuses of control and hypothyroid rats at 13 and 16 days gestation. Endocrinology 131, 195-200.
48. Puymirat, J., Barret, A., Picart, R., Vigny, A., Loudes, C., Faivre-Bauman, A., Tixier-Vidal, A., 1983. Triiodothyronine enhances the morphological maturation of dopaminergic neurons from fetal mouse hypothalamus cultured in serum-free medium. Neuroscience 10, 801-810. (Pubitemid 14097186)
49. Qiu, P., Feng, X.H., Li, L., 2003. Interaction of Smad3 and SRF-associated complex mediates TGF-beta1 signals to regulateSM22 transcription duringmyofibroblast differentiation. J. Mol. Cell Cardiol. 35, 1407-1420. (Pubitemid 37491184)
50. Reinehr, T., Isa, A., De Sousa, G., Dieffenbach, R., Andler, W., 2008. Thyroid hormones and their relation to weight status. Horm. Res. 70, 51-57. (Pubitemid 351919802)
51. Sakurai, A., Miyamoto, T., Degroot, L.J., 1992. Cloning and characterization of the human thyroid hormone receptor beta 1 gene promoter. Biochem. Biophys. Res. Commun. 185, 78-84.
52. Santisteban, P., Bernal, J., 2005. Thyroid development and effect on the nervous system. Rev. Endocr. Metab. Disord. 6, 217-228. (Pubitemid 41285599)
53. Segerson, T.P., Kauer, J., Wolfe, H.C., Mobtaker, H., Wu, P., Jackson, I.M., Lechan, R.M., 1987. Thyroid hormone regulates TRH biosynthesis in the paraventricular nucleus of the rat hypothalamus. Science 238, 78-80. (Pubitemid 17150486)
54. Siesser, W.B., Cheng, S.Y., Mcdonald, M.P., 2005. Hyperactivity, impaired learning on a vigilance task, and a differential response to methylphenidate in the TRbetaPV knock-in mouse. Psychopharmacology (Berl) 181, 653-663. (Pubitemid 41400751)
55. Siesser, W.B., Zhao, J., Miller, L.R., Cheng, S.Y., Mcdonald, M.P., 2006. Transgenic mice expressing a human mutant beta1 thyroid receptor are hyperactive, impulsive, and inattentive. Genes Brain Behav. 5, 282-297.
56. Suen, C.H., Yen, P.M., Chin, W.W., 1994. In vitro transcriptional studies of the roles of the thyroid hormone (T3) response elements and minimal promoters in T3-stimulated gene transcription. J. Biol. Chem. 269, 1314-1322. (Pubitemid 24032525)
57. Suzuki, S., Miyamoto, T., Opsahl, A., Sakurai, A., Degroot, L.J., 1994. Two thyroid hormone response elements are present in the promoter of human thyroid hormone receptor beta 1. Mol. Endocrinol. 8, 305-314. (Pubitemid 24108358)
58. Tang, H.Y., Lin, H.Y., Zhang, S., Davis, F.B., Davis, P.J., 2004. Thyroid hormone causes mitogen-activated protein kinase-dependent phosphorylation of the nuclear estrogen receptor. Endocrinology 145, 3265-3272. (Pubitemid 38829999)
59. Taylor, T., Gyves, P., Burgunder, J.M., 1990a. Thyroid hormone regulation of TRH mRNA levels in rat paraventricular nucleus of the hypothalamus changes during ontogeny. Neuroendocrinology 52, 262-267. (Pubitemid 20260128)
60. Taylor, T., Wondisford, F.E., Blaine, T., Weintraub, B.D., 1990b. The paraventricular nucleus of the hypothalamus has a major role in thyroid hormone feedback regulation of thyrotropin synthesis and secretion. Endocrinology 126, 317-324. (Pubitemid 20037159)
61. Thompson, C.C., Weinberger, C., Lebo, R., Evans, R.M., 1987. Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system. Science 237, 1610-1614. (Pubitemid 17134886)
62. Ubieta, R., Uribe, R.M., Gonzalez, J.A., Garcia-Vazquez, A., Perez-Monter, C., Perez-Martinez, L., Joseph-Bravo, P., Charli, J.L., 2007. BDNF up-regulates pre-pro-TRH mRNA expression in the fetal/neonatal paraventricular nucleus of the hypothalamus. Properties of the transduction pathway. Brain Res. 1174, 28-38. (Pubitemid 47451363)
63. Yen, P.M., 2001. Physiological and molecular basis of thyroid hormone action. Physiol. Rev. 81, 1097-1142. (Pubitemid 32606667)
64. Zhang, J., Lazar, M.A., 2000. The mechanism of action of thyroid hormones. Annu. Rev. Physiol. 62, 439-466. (Pubitemid 30618270)
65. Zoeller, R.T., Dowling, A.L., Vas, A.A., 2000. Developmental exposure to polychlorinated biphenyls exerts thyroid hormone-like effects on the expression of RC3/neurogranin and myelin basic protein messenger ribonucleic acids in the developing rat brain. Endocrinology 141, 181-189. (Pubitemid 32260358)