Thyroid transcription factor 1 is calcium modulated and coordinately regulates genes involved in calcium homeostasis in C cells

Molecular and Cellular Biology

Volumn 18, Issue 12, 1998, Pages 7410-7422

  Suzuki, Koichi ^a,b   Lavaroni, Stefano ^a   Mori, Atsumi ^a   Okajima, Fumikazu ^a,c   Kimura, Shioko ^d   Katoh, Ryohei ^b   Kawaoi, Akira ^a,b   Kohn, Leonard D ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c GUNMA UNIVERSITY   (Japan)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIMYCIN; CALCITONIN; CALCIUM; CALMODULIN; CYCLIC AMP; HOMEODOMAIN PROTEIN; THYROID PEROXIDASE; THYROTROPIN RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; DNA FLANKING REGION; DNA PROTEIN COMPLEX; GENE CONTROL; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; ORGANOGENESIS; PARATHYROID CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; THYROID PARAFOLLICULAR CELL; TISSUE DISTRIBUTION; TISSUE LEVEL; TRANSCRIPTION REGULATION;

EID: 0031724219     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.12.7410     Document Type: Article

References (68)

1. Ajlouni, K., and M. El Khateeb. 1981. The effect of acute hypercalcemia on prolactin release in man. Horm. Metab. Res. 13:282-284.
2. 2) receptor-operated calcium entry into rat thyroid cells. Biochem. Biophys. Res. Commun. 195:1-7.
3. Ambesi-Impiombato, F. S., and H. G. Coon. 1979. Thyroid cells in culture. Int. Rev. Cytol. 1(Suppl.):163-172.
4. Arnone, M. I., M. Zannini, and R. Di Lauro. 1995. The DNA binding activity and the dimerization ability of the thyroid transcription factor I are redox regulated. J. Biol. Chem. 270:12048-12055.
5. Aurbach, G. D., S. J. Marx, and A. M. Spiegel. 1992. Parathyroid hormone, calcitonin, and the calciferols, p. 1397-1476. In J. D. Wilson and D. W. Foster (ed.), Williams textbook of endocrinology, 8th ed. The W. B. Saunders Co., Philadelphia, Pa.
6. Behrens, J., O. Lowrick, L. Klein-Hitpass, and W. Birchmeier. 1991. The E-cadherin promoter: functional analysis of a G-C-rich region and an epithelial cell-specific palindromic regulatory element. Proc. Natl. Acad. Sci. USA 88:11495-11499.
7. Besnard, P., V. Jousset, and J.-M. Garel. 1989. Additive effects of dexamethasone and calcium on the calcitonin mRNA level in adrenalectomized rats. FEBS Lett. 258:293-296.
8. Bikle, D. D., A. Ratnam, T. Mauro, J. Harris, and S. Pillai. 1996. Changes in calcium responsiveness and handling during keratinocyte differentiation. Potential role of the calcium receptor. J. Clin. Investig. 97:1085-1093.
9. Bizzarri, C., and D. Corda. 1994. Norepinephrine, unlike ATP, induces all-or-none increase in cytosolic calcium in thyroid cells. The role of inositol-trisphosphate-sensitive stores and calcium channels. Eur. J. Biochem. 219: 837-844.
10. Brown, E. M., C. J. Chen, M. S. Leboff, O. Kifor, and G. El-Hajj. 1989. Mechanisms underlying the inverse control of parathyroid hormone secretion by calcium, p. 252-268. In G. Oxford and C. M. Armstrong (ed.), Secretion and its control. Rockefeller University Press, New York, N.Y.
11. 2+-sensing receptor from bovine parathyroid. Nature 366:575-580.
12. Bruno, M. D., R. J. Bohinski, K. M. Huelsman, J. A. Whitsett, and T. R. Korfhagen. 1995. Lung cell-specific expression of the murine surfactant protein A (SP-A) gene is mediated by interactions between the SP-A promoter and thyroid transcription factor-1. J. Biol. Chem. 270:6531-6536. (Erratum, 270:16482.)
13. Chattopadhyay, N., G. Legradi, M. Bai, O. Kifor, C. Ye, P. M. Vassilev, E. M. Brown, and R. M. Lechan. 1997. Calcium-sensing receptor in the rat hippocampus: a developmental study. Dev. Brain Res. 100:13-21.
14. Civitareale, D., M. P. Castelli, P. Falasca, and A. Saiardi. 1993. Thyroid transcription factor 1 activates the promoter of the thyrotropin receptor gene. Mol. Endocrinol. 7:1589-1595.
15. 1 adrenergic receptors in cultured rat thyroid cells. J. Biol. Chem. 260:9230-9236.
16. Don, R. H., P. T. Cox, B. J. Wainwright, K. Baker, and J. S. Mattick. 1991. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 19:4008.
17. 1 receptor activation. J. Neurosci. 17:9545-9553.
18. Emanuel, R. L., G. K. Adler, O. Kifor, S. J. Quinn, F. Fuller, K. Krapcho, and E. M. Brown. 1996. Calcium-sensing receptor expression and regulation by extracellular calcium in the AtT-20 pituitary cell line. Mol. Endocrinol. 10: 555-565.
19. - symporter activity. Mol. Endocrinol. 11:1747-1755.
20. Esbenshade, T. A., T. L. Theroux, and K. P. Minneman. 1994. Increased voltage-dependent calcium influx produced by alpha 1B-adrenergic receptor activation in rat medullary thyroid carcinoma 6-23 cells. Mol. Pharmacol. 45: 591-598.
21. Francis-Lang, H., M. Price, M. Polycarpou-Schwarz, and R. Di Lauro. 1992. Cell-type-specific expression of the rat thyroperoxidase promoter indicates common mechanisms for thyroid-specific gene expression. Mol. Cell. Biol. 12:576-588.
22. Freichel, M., A. Zink-Lorenz, A. Holloschi, M. Hafner, V. Flockerzi, and F. Raue. 1996. Expression of a calcium-sensing receptor in a human medullary thyroid carcinoma cell line and its contribution to calcitonin secretion. Endocrinology 137:3842-3848.
23. Fuleihan, G. E., E. M. Brown, R. Gleason, J. Scott, and G. K. Adler. 1996. Calcium modulation of adrenocorticotropin levels in women - a clinical research center study. J. Clin. Endocrinol. Metab. 81:932-936.
24. Guazzi, S., M. Price, M. De Felice, G. Damante, M. G. Mattei, and R. Di Lauro. 1990. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J. 9:3631-3639.
25. Hishikawa, R., M. Fukase, T. Yamatani, S. Kadowaki, and T. Fujita. 1985. Phorbol ester stimulates calcitonin secretion synergistically with A23187, and additively with dibutyryl cyclic AMP, in a rat C-cell line. Biochem. Biophys. Res. Commun. 132:424-429.
26. Ikuyama, S., H. Shimura, J. P. Hoeffler, and L. D. Kohn. 1992. Role of the cyclic adenosine 3′,5′-monophosphate response element in efficient expression of the rat thyrotropin receptor promoter. Mol. Endocrinol. 6:1701-1715.
27. Isozaki, O., N. Emoto, T. Tsushima, Y. Sato, K. Shizume, H. Demura, T. Akamizu, and L. D. Kohn. 1992. Opposite regulation of deoxyribonucleic acid synthesis and iodide uptake in rat thyroid cells by basic fibroblast growth factor: correlation with opposite regulation of c-fos and thyrotropin receptor gene expression. Endocrinology 131:2723-2732.
28. Kikkawa, F., F. J. Gonzalez, and S. Kimura. 1990. Characterization of a thyroid-specific enhancer located 5.5 kilobase pairs upstream of the human thyroid peroxidase gene. Mol. Cell. Biol. 10:6216-6224.
29. Kimura, S., Y. Hara, T. Pineau, P. Fernandez-Salguero, C. H. Fox, J. M. Ward, and F. J. Gonzalez. 1996. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev. 10:60-69.
30. Kohn, L. D., C. Giuliani, V. Montani, G. Napolitano, M. Ohmori, M. Ohta, M. Saji, F. Schuppert, M. Shong, K. Suzuki, S.-I. Taniguchi, K. Yano, and D. S. Singer. 1995. Antireceptor immunity, p. 115-170. In D. Rayner and B. Champion (ed.), Thyroid immunity. RG Landes Biomedical Publishers, Austin, Tex.
31. Kohn, L. D., H. Shimura, Y. Shimura, A. Hidaka, C. Giuliani, G. Napolitano, M. Ohmori, G. Laglia, and M. Saji. 1995. The thyrotropin receptor. Vitam. Horm. 50:287-384.
32. Kohn, L. D., W. A. Valente, E. F. Grollman, S. M. Aloj, and P. Vitti. September 1986. U.S. patent 4,609,622.
33. 2 receptor-channel activation and desensitization. Mol. Endocrinol. 12:901-913.
34. Lazzaro, D., M. Price, M. de Felice, and R. Di Lauro. 1991. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093-1104.
35. Levine, M., and J. L. Manley. 1989. Transcriptional repression of eukaryotic promoters. Cell 59:405-408.
36. Lillie, J. H., D. K. MacCallum, and A. Jepsen. 1988. Growth of stratified squamous epithelium on reconstituted extracellular matrices: long-term culture. J. Investig. Dermatol. 90:100-109.
37. MacIntyre, I. 1995. Calcitonin: physiology, biosynthesis, secretion, metabolism, and mode of action, p. 978-989. In L. J. DeGroot (ed.), Endocrinology, 3rd ed. The W. B. Saunders Co., Philadelphia, Pa.
38. Maenhaut, C., G. Brabant, G. Vassart, and J. E. Dumont. 1992. In vitro and in vivo regulation of thyrotropin receptor mRNA levels in dog and human thyroid cells. J. Biol. Chem. 267:3000-3007.
39. Matsuo, K., G. H. Amplalavanar, H. Nojima, and T. Takano. 1991. GenBank accession no. D90397.
40. 2+ receptor-stimulated hormone release from sheep thyroid parafollicular cells. J. Physiol. (London) 502:31-44.
41. Mizuno, K., F. J. Gonzalez, and S. Kimura. 1991. Thyroid-specific enhancer-binding protein (T/EBP): cDNA cloning, functional characterization, and structural identity with thyroid transcription factor TTF-1. Mol. Cell. Biol. 11:4927-4933.
42. Musti, A. M., V. M. Ursini, E. V. Avvedimento, V. Zimarino, and R. Di Lauro. 1987. A cell type specific factor recognizes the rat thyroglobulin promoter. Nucleic Acids Res. 15:8149-8166.
43. Naor, Z., A. M. Leifer, and K. J. Catt. 1980. Calcium-dependent actions of gonadotropin-releasing hormone on pituitary guanosine 3′,5′-monophosphate production and gonadotropin release. Endocrinology 107:1438-1445.
44. Nojima, H. 1989. Structural organization of multiple rat calmodulin genes. J. Mol. Biol. 208:269-282.
45. Ohmori, M., H. Shimura, Y. Shimura, S. Ikuyama, and L. D. Kohn. 1995. Characterization of an up-stream thyroid transcription factor-1-binding site in the thyrotropin receptor promoter. Endocrinology 136:269-282.
46. 2+-dependent manner in FRTL-5 thyroid cell membranes. FEBS Lett. 253:132-136.
47. 2-purinergic stimulation of phosphoinositide turnover and arachidonate release in FRTL-5 thyroid cells. Cooperative mechanism of signal transduction systems. J. Biol. Chem. 264: 13029-13037.
48. 2-purinergic receptor-mediated iodide efflux and phosphoinositide turnover in FRTL-5 cells. Endocrinology 123:1035-1043.
49. 2+-sensing receptor gene cause familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism. Cell 75:1297-1303.
50. Potts, J. T. J., F. R. Bringhurst, T. Gardella, S. Nussbaum, G. Segre, and H. Kronenberg. 1995. Parathyroid hormone: physiology, chemistry, biosynthesis, secretion, metabolism, and mode of action, p. 920-966. In L. J. DeGroot (ed.), Endocrinology, 3rd ed. The W. B. Saunders Co., Philadelphia, Pa.
51. Rheinwald, J. G., and H. Green. 1975. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6:331-343.
52. Riccardi, D., J. Park, W. S. Lee, G. Gamba, E. M. Brown, and S. C. Hebert. 1995. Cloning and functional expression of a rat kidney extracellular calcium/ polyvalent cation-sensing receptor. Proc. Natl. Acad. Sci. USA 92:131-135.
53. ++ down regulate thyrotropin receptor gene expression by a mechanism different from the cAMP signal. Biochem. Biophys. Res. Commun. 176:94-101.
54. Saji, M., M. Shong, G. Napolitano, L. A. Palmer, S. I. Taniguchi, M. Ohmori, M. Ohta, K. Suzuki, S. L. Kirshner, C. Giuliani, D. S. Singer, and L. D. Kohn. 1997. Regulation of major histocompatibility complex class I gene expression in thyroid cells. Role of the cAMP response element-like sequence. J. Biol. Chem. 272:20096-20107.
55. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
56. Santisteban, P., A. Acebron, M. Polycarpou-Schwarz, and R. Di Lauro. 1992. Insulin and insulin-like growth factor I regulate a thyroid-specific nuclear protein that binds to the thyroglobulin promoter. Mol. Endocrinol. 6:1310-1317.
57. Shimura, H., F. Okajima, S. Ikuyama, Y. Shimura, S. Kimura, M. Saji, and L. D. Kohn. 1994. Thyroid-specific expression and cyclic adenosine 3′,5′-monophosphate autoregulation of the thyrotropin receptor gene involve thyroid transcription factor-1. Mol. Endocrinol. 8:1049-1069.
58. Stolarsky-Fredman, L., S. E. Leff, E. S. Klein, E. B. D. Crenshaw, J. Yeakley, and M. G. Rosenfeld. 1990. A tissue-specific enhancer in the rat-calcitonin/ CGRP gene is active in both neural and endocrine cell types. Mol. Endocrinol. 4:497-504.
59. Suzuki, K., A. Lavaroni, A. Mori, E. Miyagi, R. Katoh, L. D. Kohn, and A. Kawaoi. In vivo expression of thyroid transcription factor (TTF-1) RNA and its relation to thyroid function: identification of follicular thyroglobulin (TG) as a feedback suppressor of TTF-1 RNA levels and TG synthesis. Thyroid, in press.
60. Suzuki, K., A. Lavaroni, A. Mori, M. Ohta, J. Saito, M. Pietrarelli, D. S. Singer, S. Kimura, R. Katoh, L. D. Kohn, and A. Kawaoi. 1998. Autoregulation of thyroid-specific gene transcription by thyroglobulin. Proc. Natl. Acad. Sci. USA 95:8251-8256.
61. Suzuki, K., Y. Kobayashi, R. Katoh, L. D. Kohn, and A. Kawaoi. 1998. Identification of thyroid transcription factor-1 in C cells and parathyroid cells. Endocrinology 139:3014-3017.
62. Thiagalingam, A., A. de Bustros, M. Borges, R. Jasti, D. Compton, L. Diamond, M. Mabry, D. W. Ball, S. B. Baylin, and B. D. Nelkin. 1996. RREB-1, a novel zinc finger protein, is involved in the differentiation response to Ras in human medullary thyroid carcinomas. Mol. Cell. Biol. 16:5335-5345.
63. 2+ stores in rat thyroid FRTL-5 cells. J. Cell. Physiol. 149:485-491.
64. Van Renterghem, P., S. Dremier, G. Vassart, and D. Christophe. 1995. Study of TTF-1 gene expression in dog thyrocytes in primary culture. Mol. Cell. Endocrinol. 112:83-93.
65. Veldhuis, J. D., J. L. Borges, C. R. Drake, and A. D. Rogol. 1984. Divergent influences of calcium ions on releasing factor-stimulated anterior pituitary hormone secretion in normal man. J. Clin. Endocrinol. Metab. 59:56-61.
66. Won, J. G., and D. N. Orth. 1990. Roles of intracellular and extracellular calcium in the kinetic profile of adrenocorticotropin secretion by perfused rat anterior pituitary cells. I. Corticotropin-releasing factor stimulation. Endocrinology 126:849-857.
67. Yan, C., Z. Sever, and J. A. Whitsett. 1995. Upstream enhancer activity in the human surfactant protein B gene is mediated by thyroid transcription factor 1. J. Biol. Chem. 270:24852-24857.
68. Zeytin, F. N., S. Rusk, and S. E. Leff. 1987. Calcium, dexamethasone, and the antiglucocorticoid RU-486 differentially regulate neuropeptide synthesis in a rat C cell line. Endocrinology 121:361-370.