Thyroid hormone-dependent transcriptional repression of neural cell adhesion molecule during brain maturation

EMBO Journal

Volumn 15, Issue 16, 1996, Pages 4307-4316

  Iglesias, Teresa ^a,c,d   Caubín, Julio ^b   Stunnenberg, Hendrik G ^c   Zaballos, Angel ^b   Bernal, Juan ^a   Muñoz, Alberto ^a  

^a CSIC   (Spain)

^b Departamento de Investigación   (Spain)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Brain; erbA; NCAM; Neural cell adhesion molecule; Thyroid hormone

Indexed keywords

ALPHA TUBULIN; NERVE CELL ADHESION MOLECULE; THYROID HORMONE;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EXON; HYPOTHYROIDISM; IN SITU HYBRIDIZATION; INTRON; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; RAT; REPORTER GENE; TRANSCRIPTION REGULATION;

EID: 0029738028     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00805.x     Document Type: Article

References (81)

1. Alvarez-Dolado, M., Iglesias, T., Rodríguez-Peña, A., Bernal, J. and Muñoz, A. (1994) Expression of neurotrophins and the trk family of neurotrophin receptors in normal and hypothyroid rat brain. Mol. Brain Res., 27, 249-257.
2. Aniello, F., Couchie, D., Gripois, D. and Nunez, J. (1991) Regulation of five tubulin isotypes by thyroid hormone during brain development. J. Neurochem., 57, 1781-1786.
3. Atashi, J.R., Klinz, S.G., Ingraham, C.A., Matten, W.T., Schachner, M. and Maness, P.F. (1992) Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron, 8, 831-842.
4. Baniahmad, A., Ha, I., Reinberg, D., Tsai, S., Tsai, M.-J. and O'Malley, B.W. (1993) Interaction of human thyroid hormone receptor β with transcription factor TFIIB may mediate target gene derepression and activation by thyroid hormone. Proc. Natl Acad. Sci. USA, 90, 8832-8836.
5. Becker, C.G., Becker, T., Schmidt, A. and Roth, G. (1994) Polysialic acid expression in the salamander retina is inducible by thyroxine. Dev. Brain Res., 79, 140-146.
6. Bigler, J. and Eisenman, R.N. (1994) Isolation of a thyroid hormone-responsive gene by immunoprecipitation of thyroid hormone receptor-DNA complexes. Mol. Cell. Biol., 14, 7621-7632.
7. Bigler, J. and Eisenman, R.N. (1995) Novel location and function of a thyroid hormone response element. EMBO J., 14, 5710-5723.
8. Bradley, D.J., Young, W.S. III and Weinberger, C. (1989) Differential expression of a and β thyroid hormone receptor thyroid hormone receptor genes in rat brain and pituitary. Proc. Natl Acad Sci. USA, 86, 7250-7254.
9. Caubín, J., Iglesias, T., Bernal, J., Muñoz, A., Márquez, G., Barbero, J.L. and Zaballos, A. (1994) Isolation of genomic DNA fragments corresponding to genes modulated in vivo by a transcription factor. Nucleic Acids Res., 22, 4132-4138.
10. Chen, J.D. and Evans, R.M. (1995) A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature, 377, 454-457.
11. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform-extraction. Anal. Biochem., 162, 156-159.
12. Church, G.M. and Gilbert, W. (1984) Genome sequencing. Proc. Natl Acad. Sci. USA, 81, 1991-1995.
13. Clos, J. and Legrand, Ch. (1990) An interaction between thyroid hormone and nerve growth factor promotes the development of hippocampus, olfactory bulbs and cerebellum: a comparative biochemical study of normal and hypothyroid rats. Growth Factors, 3, 205-220.
14. Costa-Giomi, M.P., Gaub, M.-P., Chambon, P. and Abarzua, P. (1992) Characterization of a retinoic acid responsive element isolated by whole genomic PCR. Nucleic Acids Res., 20, 3223-3232.
15. Cunningham, B.A. (1995) Cell adhesion molecules as morphoregulators. Curr. Opin. Cell Biol., 7, 628-633.
16. DeLong, G.R. (1990) The effect of iodine deficiency on neuromuscular development. IDD Newsletter, 6, 1-9.
17. Dussault, J.H. and Ruel, J. (1987) Thyroid hormones and brain development. Annu. Rev. Physiol., 49, 321-334.
18. Edelman, G.M. and Crossin, K.L. (1991) Cell adhesion molecules: implications for a molecular histology. Annu. Rev. Biochem., 60, 155-190.
19. El-Deiry, W.S., Kern, S.E., Pietenpol, J.A., Kinzler, K.W. and Vogelstein, B. (1992) Definition of a consensus binding site for p53. Nature Genet., 1, 45-49.
20. Farsetti, A., Mitsuhashi, T., Desvergne, B., Robbins, J. and Nikodem, V (1991) Molecular basis of thyroid hormone regulation of myelin basic protein gene expression in rodent brain. J. Biol. Chem., 266, 23226-23232.
21. Feinberg, P.A. and Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 137, 266-267.
22. Figueiredo, B.C., Almazan, G., Ma, Y., Tetzlaff, W., Miller, F.D. and Cuello, A.C. (1992) Gene expression in the developing cerebellum during perinatal hypo- and hyperthyroidism. Mol. Brain Res., 17, 258-268.
23. Figueiredo, B.C., Otten, U., Strauss, S., Volk, B. and Maysinger, D. (1993) Effects of perinatal hypo- and hyperthyroidism on the levels of nerve growth factor and its low-affinity receptor in cerebellum. Dev. Brain Res., 72, 237-244.
24. Fondell, J.D., Roy, A.L. and Roeder, R.G. (1993) Unliganded thyroid hormone receptor inhibits formation of a functional preinitiation complex: implications for active repression. Genes Dev., 7, 1400-1410.
25. Forrest, D. (1992) The erbA/thyroid hormone receptor genes in development of the central nervous system. Semin. Cancer Biol., 5, 167-176.
26. Forrest, D., Hallböök, F., Persson, H. and Vennström, B. (1991) Distinct functions for thyroid hormone receptors a and β in brain development indicated by differential expression of receptor genes. EMBO J., 10, 269-275.
27. García-Fernández, L.F., Iñiguez, M.A., Rodríguez-Peña, A., Muñoz, A. and Bernal, J. (1993) Brain-specific prostaglandin D2 synthetase mRNA is dependent on thyroid hormone during rat brain development. Biochem. Biophys. Res. Commun., 196, 396-401.
28. Gegelashvili, G., Andersson, A.-M., Schousboe, A. and Bock, E. (1993) Cyclic AMP regulates NCAM expression and phosphorylation in cultured mouse astrocytes. Eur. J. Cell Biol., 62, 343-351.
29. Gennarini, G., Hirsch, M.-R., He, H.-T., Hirn, M., Finne, J. and Goridis, C. (1986) Differential expression of mouse neural cell adhesion molecule (N-CAM) mRNA species during brain development and in neural cell lines. J. Neurosci., 6, 1983-1990.
30. Goridis, C. and Brunet, J.-F. (1992) NCAM: structural diversity, function and regulation of expression. Semin. Cell Biol., 3, 189-197.
31. Goridis, C., Hirn, M., Santoni, M.-J., Gennarini, G., Deagostini-Bazin, H., Jordan, B.R., Kiefer, M. and Steinmetz, M. (1985) Isolation of mouse N-CAM-related cDNA: detection and cloning using monoclonal antibodies. EMBO J., 4, 631-635.
32. Hörlein, A.J. et al. (1995) Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature, 377, 397-404.
33. Husmann, M., Görgen, I., Weisgerber, C. and Bitter-Suermann, D. (1989) Up-regulation of embryonic NCAM in an EC cell line by retinoic acid. Dev. Biol., 136, 194-200.
34. Iglesias, T., Caubín, J., Zaballos, A., Bernal, J. and Muñoz, A. (1995) Identification of the mitochondrial NADH dehydrogenase subunit 3 (ND3) as a thyroid hormone regulated gene by whole genome PCR analysis. Biochem. Biophys. Res. Commun., 210, 995-1000.
35. Iñiguez, M.A., Rodríguez-Peña, A., Ibarrola, N., Morreale de Escobar, G. and Bernal, J. (1992) Adult rat brain is sensitive to thyroid hormone. J. Clin. Invest., 90, 554-558.
36. Iñiguez, M.A., Rodríguez-Peña, A., Ibarrola, N., Aguilera, M., Muñoz, A. and Bernal, J. (1993) Thyroid hormone regulation of RC3, a brain-specific gene encoding a protein kinase-C substrate. Endocrinology, 133, 467-473.
37. Iñiguez, M.A., de Lecea, L., Guadaño, A., Morte, B., Gerendasy, D., Sutcliffe, J.G. and Bernal, J. (1996) Cell-specific effects of thyroid hormone on RC3/neurogranin expression in rat brain. Endocrinology, 137, 1032-1041.
38. Inoue, S., Kondo, S., Hashimoto, M., Kondo, T. and Muramatsu, M. (1991) Isolation of estrogen receptor-binding sites in human genomic DNA. Nucleic Acids Res., 19, 4091-4096.
39. Kato, S., Sasaki, H., Suzawa, M., Masushige, S., Tora, L., Chambon, P. and Gronemeyer, H. (1995) Widely spaced, directly repeated PuGGTCA elements act as promiscuous enhancers for different classes of nuclear receptors. Mol. Cell. Biol., 15, 5858-5867.
40. Kinzler, K.W. and Vogelstein, B. (1989) Whole genome PCR: application to the identification of sequences bound by gene regulatory proteins. Nucleic Acids Res., 17, 3645-3653.
41. Lazar, M.A. (1994) Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr. Rev., 14, 184-193.
42. Lee, J.W., Ryan, F., Swaffield, J.C., Johnston, S.A. and Moore, D. (1995) Interaction of thyroid hormone receptor with a conserved transcriptional mediator. Nature, 374, 91-94.
43. Legrand, J. (1984) Effects of thyroid hormones on central nervous system. In Yanai, J. (ed.), Neurobehavioural Teratology. Elsevier, Amsterdam, The Netherlands, pp. 331-363.
44. Leonard, J.L., Kaplan, M.M., Visser, T.J., Silva, J.E. and Larsen, P.R. (1981) Cerebral cortex responds rapidly to thyroid hormones. Science, 214, 571-573.
45. Levi, G., Broders, F., Dunon, D., Edelman, G.M. and Thiery, J.P. (1990) Thyroxine-dependent modulations of the expression of the neural cell adhesion molecule N-CAM during Xenopus laevis metamorphosis. Development, 109, 681-692.
46. Lindholm, D., Castrén, E., Tsoulfas, P., Kolbeck, R., da Penha Berzaghi, M., Leingärtner, A., Heisenberg, C.-P., Tesarollo, L., Parada, L. and Thoenen, H. (1993) Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J. Cell Biol., 122, 443-450.
47. Linial, M., Gunderson, N. and Groudine, M. (1985) Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science, 230, 1126-1132.
48. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Mellström, B., Naranjo, J.R., Santos, A., González, A.M. and Bernal, J. (1991) Independent expression of the α and β c-erbA genes in developing rat brain. Mol. Endocrinol., 5, 1339-1350.
50. Miller, P.D., Chung, W.-W., Lagenaur, C.F. and DeKosky, S.T. (1993) Regional distribution of neural cell adhesion molecule (N-CAM) and L1 in human and rodent hippocampus. J. Comp. Neurol., 327, 341-349.
51. Montag, D. et al. (1994) Mice deficient for the myelin-associated glycoprotein show subtle abnormalities in myelin. Neuron, 13, 229-246.
52. Müller, U. and Kypta, R. (1995) Molecular genetics of neuronal adhesion. Curr. Opin. Neurobiol., 5, 36-41.
53. Muñoz, A., Rodriguez-Peña, A., Pérez-Castillo, A., Ferreiro, B., Sutcliffe, J.G. and Bernal, J. (1991) Effects of neonatal hypothyroidism on rat brain gene expression. Mol. Endocrinol., 5, 273-280.
54. Näthke, I.S., Hinck, L.E. and Nelson, W.J. (1993) Epithelial cell adhesion and development of cell surface polarity: possible mechanisms for modulation of cadherin function, organization and distribution. J. Cell Sci., suppl. 17, 139-145.
55. Owens, G.C., Edelman, G.M. and Cunningham, B.A. (1987) Organization of the neural cell adhesion molecule (N-CAM) gene: alternative exon usage as the basis for different membrane-associated domains. Proc. Natl Acad. Sci. USA, 84, 294-298.
56. Pérez-Castillo, A., Bernal, J., Ferreiro, B. and Pans, T. (1985) The early ontogenesis of thyroid hormone receptor in the rat fetus. Endocrinology, 117, 2457-2461.
57. Pipaón, C., Santos, A. and Pérez-Castillo, A. (1992) Thyroid hormone up-regulates NGFI-A gene expression in rat brain during development. J. Biol. Chem., 267, 21-23.
58. Porterfield, S.P. and Hendrich, C.E. (1993) The role of thyroid hormones in prenatal and neonatal neurological development - current perspectives. Endocr. Rev., 14, 94-106.
59. Rabié, A., Pastel, A.J., Clavel, M.C. and Legrand, J. (1979) Effect of thyroid deficiency on the growth of the hippocampus in the rat. Dev. Neurosci., 2, 183-194.
60. Reyes, A.A., Schulte, S.V., Small, S. and Akeson, R. (1993) Distinct NCAM splicing events are differentially regulated during rat brain development. Mol. Brain Res., 17, 201-211.
61. Rodríguez-Peña, A., Ibarrola, N., Iñiguez, M.A., Muñoz, A. and Bernal, J. (1993) Neonatal hypothyroidism affects the timely expression of myelin-associated glycoprotein in the rat brain. J. Clin. Invest., 91, 812-818.
62. Rosales, C., O'Brien, V., Kornberg, L. and Juliano, R. (1995) Signal transduction by cell adhesion receptors. Biochim. Biophys. Acta, 1242, 77-98.
63. Rudert, F. and Gronemeyer, H. (1993) Retinoic acid-response elements with a highly repetitive structure isolated by immuno-selection from genomic DNA. J. Steroid Biochem. Mol. Biol., 46, 121-133.
64. Rutishauser, U. (1993) Adhesion molecules of the nervous system. Curr. Opin. Neurobiol., 3, 709-715.
65. Samuels, H.H., Stanley, F. and Casanova, J. (1978) Depletion of L-3,5,3′-triiodothyronine and L-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. J. Endocrinol., 105, 80-85.
66. Sandaltzopoulos, R. and Becker, P.B. (1994) Solid phase DNase I footprinting: quick and versatile. Nucleic Acids Res., 8, 1511-1512.
67. Sanger, F., Nicklen, S. and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
68. Sap, J., Muñoz, A., Damm, K., Goldberg, I., Ghysdael, J., Leutz, A., Beug, H. and Vennström, B. (1986) The c-erbA protein is a high affinity receptor for thyroid hormone. Nature, 324, 635-640.
69. Sap, J., Muñoz, A., Schmitt, J., Stunnenberg, H.G. and Vennström, B. (1989) Repression of transcription mediated at a thyroid hormone response element by the v-erbA oncogene product. Nature, 340, 242-244.
70. Sap, J., de Magistris, L., Stunnenberg, H.G. and Vennström, B. (1990) A major thyroid hormone response element in the third intron of the rat growth hormone gene. EMBO J., 9, 887-896.
71. Seelig, S., Liaw, C., Towle, H.C. and Oppenheimer, J.H. (1981) Thyroid hormone attenuates and augments hepatic gene expression at a pretranslational level. Proc. Natl Acad. Sci. USA, 78, 4733-4737.
72. Small, S.J., Shull, G.E., Santoni, M.-J. and Akeson, R. (1987) Identification of a cDNA clone that contains the complete coding sequence for a 140-kD rat NCAM polypeptide. J. Cell Biol., 105, 2335-2345.
73. Thompson, J., Moore, S.E. and Walsh, F.S. (1987) Thyroid hormones regulate expression of the neural cell adhesion molecule in adult skeletal muscle. FEBS Lett., 219, 135-138.
74. Tosic, M., Torch, S., Comte, V., Dolivo, M., Honegger, P. and Matthieu, J.-M. (1992) Triiodothyronine has diverse and multiple stimulating effects on expression of the major myelin protein genes. J. Neurochem., 59, 1770-1777.
75. Valcárcel, R., Holz, H., García Jiménez, C., Barettino, D. and Stunnenberg, H.G. (1994) Retinoid-dependent in vitro transcription mediated by the RXR/RAR heterodimer. Genes Dev., 8, 3068-3079.
76. Vega-Núñez, E., Menéndez-Hurtado, A., Garesse, R., Santos, A. and Pérez-Castillo, A. (1995) Thyroid hormone-regulated brain mitochondrial genes revealed by differential cDNA cloning. J. Clin. Invest., 96, 893-899.
77. Vennström, B. and Bishop, J.M. (1982) Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus. Cell, 28, 135-143.
78. Weinberger, C., Thompson, C.C., Ong, E.S., Lebo, R., Gruol, D.J. and Evans, R.M. (1986) The c-erbA encodes a thyroid hormone receptor. Nature, 324, 640-646.
79. Yen, P.M. and Chin, W.W. (1994) New advances in understanding the molecular mechanisms of thyroid hormone action. Trends Endocrinol. Metab., 5, 65-72.
80. Zhang, W., Brooks, R.L., Silversides, D.W., West, B.L., Leidig, F., Baxter, J.D. and Eberhadt, N.L. (1992) Negative thyroid hormone control of human growth hormone gene expression is mediated by 3′-untranslated/3′-flanking DNA. J. Biol. Chem., 267, 15056-15063.
81. Zou, L., Hagen, S.G. and Strait, K.A. (1994) Identification of thyroid hormone response elements in rodent Pcp-2, a developmentally regulated gene of cerebellar Purkinje cells. J. Biol. Chem., 269, 13346-13352.