Expression of sodium-iodide symporter mRNA in the thyroid gland of Xenopus laevis tadpoles: Developmental expression, effects of antithyroidal compounds, and regulation by TSH

Journal of Endocrinology

Volumn 190, Issue 1, 2006, Pages 157-170

  Opitz, Robert ^a   Trubiroha, Achim ^a   Lorenz, Claudia ^a   Lutz, Ilka ^a   Hatmann, Sabine ^b   Blank, Tobias ^b   Braunbeck, Thomas ^b   Kloas, Werner ^c  

^a LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 IMIDAZOLIDINETHIONE; ANTITHYROID AGENT; BUCLADESINE; CYCLIC AMP; FORSKOLIN; MESSENGER RNA; SODIUM IODIDE SYMPORTER; SODIUM PERCHLORATE; THYROTROPIN; THYROTROPIN BETA SUBUNIT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2.1; TRANSCRIPTION FACTOR PAX8; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; EX VIVO STUDY; FEEDBACK SYSTEM; GOITER; HISTOLOGY; HORMONE SYNTHESIS; HYPOPHYSIS THYROID SYSTEM; INTRACELLULAR SPACE; METAMORPHOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TADPOLE; THYROID FOLLICLE CELL; THYROID GLAND; THYROID HYPERPLASIA; TISSUE CULTURE; XENOPUS LAEVIS;

ANIMALS; ANTITHYROID AGENTS; CATTLE; ETHYLENETHIOUREA; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; METAMORPHOSIS, BIOLOGICAL; NUCLEAR PROTEINS; ORGAN CULTURE TECHNIQUES; PAIRED BOX TRANSCRIPTION FACTORS; PERCHLORIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM COMPOUNDS; SYMPORTERS; THYROID GLAND; THYROTROPIN; THYROTROPIN, BETA SUBUNIT; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 33746714936     PISSN: 00220795     EISSN: None     Source Type: Journal    
DOI: 10.1677/joe.1.06606     Document Type: Article

References (64)

1. Alexander WD & Wolff J 1966 Thyroidal iodide transport: relation between transport, goitrogenic and antigoitrogenic properties of certain anions. Endocrinology 78 581-590.
2. Altmann A, Schulz RB, Glensch G, Eskerski H, Zitzmann S, Eisenhut M & Haberkorn U 2005 Effects of Pax8 and TTF-1 thyroid transcription factor gene transfer in hepatoma cells: imaging of functional protein-protein interaction and iodide uptake. Journal of Nuclear Medicine 46 831-839.
3. Bidey SP, Marshall NJ & Ekins RP 1981 Characterisation of the cyclic AMP response to thyrotrophin in monolayer cultures of normal human thyroid cells. Acta Endocrinologica 98 370-376.
4. Bruno R, Giannasio P, Ronga G, Baudin E, Travagh JP, Russo D, Filetti S & Schlumberger M 2004 Sodium iodide symporter expression and radio-iodine distribution in extrathyroidal tissues. Journal of Endocrinological Investigation 27 1010-1014.
5. Carr DL, Laharrague F, Kahn B, Pressley TA & Carr JA 2003 Molecular characterization of a putative sodium/iodide symporter in the South African clawed frog, Xenopus laevis (abstract). Annals of the New York Acadamy of Sciences 986 711-712.
6. Dai G, Levy O & Carrasco N 1996 Cloning and characterization of the thyroid iodide transporter. Nature 379 458-460.
7. Damante G, Tell G & Di Lauro R 2001 A unique combination of transcription factors controls differentiation of thyroid cells. Progress in Nucleic Acid Research and Molecular Biology 66 307-356.
8. De La Vieja A, Dohan O, Levy O & Carrasco N 2000 Molecular analysis of the sodium/iodide symporter: impact on thyroid and extrathyroid pathophysiology. Physiological Reviews 80 1083-1105.
9. Denver RJ 1988 Several hypothalamic peptides stimulate in vitro thyrotropin secretion by pituitaries of anuran amphibians. General and Comparative Endocrinology 72 383-393.
10. Doerge DR & Takazawa RS 1990 Mechanism of thyroid peroxidase inhibition by ethylenethiourea. Chemical Research in Toxicology 3 98-101.
11. Dohan O, De la Vieja A, Paroder V, Riedel C, Attain M, Reed M, Ginter CS & Carrasco N 2003 The sodium/iodide symporter (NIS): characterization, regulation, and medical significance. Endocrine Reviews 24 48-77.
12. Elsalini OA, von Gartzen J, Cramer M & Rohr KB 2003 Zebrafish hhex, nk2.1a, and pax2.1 regulate thyroid growth and differentiation downstream of Nodal-dependent transcription factors. Developmental Biology 263 67-80.
13. - symporter gene. Molecular Endocrinology 11 1747-1755.
14. Fabbro D, Pellizzari L, Mercuri F, Tell G & Damante G 1998 Pax-8 protein levels regulate thyroglobulin gene expression. Journal of Molecular Endocrinology 21 347-354.
15. Goleman WL, Carr JA & Anderson TA 2002 Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis. Environmental Toxicology and Chemistry 21 590-597.
16. Heller N & Brändli AW 1999 Xenopus Pax-2/5/8 orthologues: novel insights into Pax gene evolution and identification of Pax-8 as the earliest marker for otic and pronephric cell lineages. Developmental Genetics 24 208-219.
17. Hollemann T & Pieler T 2000 Xnkx-2.1: a homeobox gene expressed during early forebrain, lung and thyroid development in Xenopus laevis. Development Genes and Evolution 210 579-581.
18. Hourdry J & Regard E 1975 Quantitative measurement of colloidal iodine in thyroid follicles of Xenopus larva by x-ray spectrometry: effects of hypophysectomy and the administration of TSH. General and Comparative Endocrinology 27 277-288.
19. Kalisnik M 1972 A histometric thyroid gland activation index. Journal of Microscopy 95 345-348.
20. Kimura T, Van Keymeulen A, Golstein J, Fusco A, Dumont JE & Roger PP 2001 Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocrine Revievs 22 631-656.
21. Klein SL, Strausberg RL, Wagner L, Pontius J, Clifton SW & Richardson P 2002 Genetic and genomic tools for Xenopus research: the NIH Xenopus initiative. Developmental Dynamics 225 384-391.
22. Kloas W 2002 Amphibians as model for the study of endocrine disruptors. International Review of Cytology 216 1-57.
23. Kogai T, Endo T, Saito T, Miyazaki A, Kawaguchi A & Onaya T 1997 Regulation by thyroid-stimulating hormone of sodium/iodide symporter gene expression and protein levels in FRTL-5 cells. Endocrinology 138 2227-2232.
24. Krain LP & Denver RJ 2004 Developmental expression and hormonal regulation of glucocorticoid and thyroid hormone receptors during metamorphosis in Xenopus laevis. Journal of Endocrinology 181 91-104.
25. Leloup J & Buscaglia M 1977 La triiodothyronine, hormone de la metamorphose des amphibiens. Comptes Rendus de l'Academie des Sciences 284 2261-2263.
26. - symporter with an anti-COOH terminus antibody. PNAS 94 5568-5573.
27. Liou HH, Lin W, Liou HC, Huang TF & Fu WM 2001 Modulation of protein kinase A activation by fibronectin matrix proteins at developing neuromuscular synapses in Xenopus laevis cell cultures. Molecular Pharmacology 60 348-354.
28. Lynn WG & Dent JN 1960 The action of various goitrogens in inhibiting localization of radioiodine in the thyroid and thymus glands of larval tree frogs. Biological Bulletin 118 430-438.
29. Lynn WG & Dent JN 1961 A comparison of the responses of Triturus and Desmognathus to TSH administration. Biological Bulletin 120 54-61.
30. Marians RC, Ng L, Blair HC, Unger P, Graves PN & Davies TF 2002 Defining thyrotropin-dependent and -independent steps of thyroid hormone synthesis by using thyrotropin receptor-null mice. PNAS 99 15776-15781.
31. Mascia A, Nitsch L, Di Lauro R & Zannini M 2002 Hormonal control of the transcription factor Pax8 and its role in the regulation of thyroglobulin gene expression in thyroid cells. Journal of Endocrinology 172 163-176.
32. Medina DL, Suzuki K, Pietrarelli M, Okajima F, Kohn LD & Santisteban P 2000 Role of insulin and serum on thyrotropin regulation of thyroid transcription factor-1 and pax-8 genes expression in FRTL-5 thyroid cells. Thyroid 10 295-303.
33. Nieuwkoop PD & Faber J 1994 Normal Table of Xenopus laevis (Daudin). New York, NY, USA: Garland.
34. Norris DO & Platt JE 1973 Effects of pituitary hormones, melatonin, and thyroidal inhibitors on radioiodide uptake by the thyroid glands of larval and adult tiger salamanders, Ambystoma tigrinum (Amphibia: Caudata). General and Comparative Endocrinology 21 368-376.
35. Ohno M, Zannini M, Levy O, Carrasco N & di Lauro R 1999 The paired-domain transcription factor Pax8 binds to the upstream enhancer of the rat sodium/iodide symporter gene and participates in both thyroid-specific and cyclic-AMP-dependent transcription. Molecular and Cellular Biology 19 2051-2060.
36. Opitz R, Braunbeck T, Bögi C, Pickford DB, Nentwig G, Oehlmann J, Tooi O, Lutz I & Kloas W 2005 Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds. Environmental Toxicology and Chemistry 24 653-664.
37. Opitz R, Hartmann S, Blank T, Braunbeck T, Lutz I & Kloas W 2006a Evaluation of histological and molecular endpoints for enhanced detection of thyroid system disruption in Xenopus laevis tadpoles. Toxicological Sciences 90 337-348.
38. Opitz R, Lutz I, Nguyen NG, Scanlan TS & Kloas W 2006b Analysis of thyroid hormone receptor βA mRNA expression in Xenopus laevis tadpoles as a means to detect agonism and antagonism of thyroid hormone action. Toxicology and Applied Pharmacology 212 1-13.
39. + ATPase in pig thyroid cells in primary culture: modulation by thyrotropin and thyroid hormones. Molecular and Cellullar Endocrinology 146 93-101.
40. Perron B, Rodriguez AM, Leblanc G & Pourcher T 2001 Cloning of the mouse sodium iodide symporter and its expression in the mammary gland and other tissues Journal of Endocrinology 170 185-196.
41. Pohlenz J & Refetoff S 1999 Mutations in the sodium/iodide symporter (NIS) gene as a cause for iodide transport defects and congenital hypothyroidism. Biochimie 81 469-476.
42. Regard E 1978 Cytophysiology of the amphibian thyroid gland through larval development and metamorphosis. International Review of Cytology 52 81-118.
43. - symporter in cultured human thyroid cells exposed to thyrotropin and in Graves'thyroid tissue. Journal of Clinical Endocrinology and Metabolism 82 3331-3336.
44. Saito T, Endo T, Nakazato M, Kogai T & Onaya T 1997b Thyroid-stimulating hormone-induced clown-regulation of thyroid transcription factor 1 in rat thyroid FRTL-5 cells. Endocrinology 138 602-606.
45. Sakai M, Hanaoka Y, Tanaka S, Hayashi H & Kikuyama S 1991 Thyrotropic activity of various adenohypophyseal hormones of the bullfrog. Zoological Science 8 929-934.
46. Saxen L, Saxen E, Toivonen S & Salimaki K 1957 Quantitative investigation on the anterior pituitary-thyroid mechanism during frog metamorphosis. Endocrinology 61 35-44.
47. Selmi-Ruby S, Witrin C, Trouttet-Masson S, Bernier-Valentin F, Flachon V, Munari-Silem Y & Rousset B 2003 The porcine sodium/iodide symporter gene exhibits an uncommon expression pattern related to the use of alternative splice sites not present in the human or murine species. Endocrinology 144 1074-1085.
48. Shi YB 1999 Amphibian Metamorphosis. From Morphology to Molecular Biology. New York, NY, USA: Wiley-Liss.
49. Small EM, Vokes SA, Garriock RJ, Li D & Krieg PA 2000 Developmental expression of the Xenopus Nkx2-1 and Nkx2-4 genes. Mechanisms of Development 96 259-262.
50. Spitzweg C, Dutton CM, Castro MR, Bergert ER, Goellner JR, Heufelder AE & Morris JC 2001 Expression ofthe sodium iodide symporter in human kidney. Kidney International 39 1013-1023.
51. Suzuki K, Mori A, Lavarom S, Miyagi E, Ulianich L, Katoh R, Kawaoi A & Kohn LD 1999 In vivo expression of thyroid transcription factor-1 RNA and its relation to thyroid function and follicular heterogeneity: idenfification of follicular thyroglobulin as a feedback suppressor for thyroid transcription factor-1 RNA levels and thyroglobulin synthesis. Thyroid 9 319-331.
52. Taki K, Kogai T, Kanamoto Y, Hershman JM & Brent GA 2002 A thyroid-specific far-upstream enhancer in the human sodium/iodide symporter gene requires Pax-8 binding and cyclic adenosine 3′,5′-monophosphate response element-like sequence binding proteins for full activity and is differentially regulated in normal and thyroid cancer cells. Molecular Endocrinology 16 2266-2282.
53. Tietge JE, Holcombe GW, Flynn KM, Kosian PA, Korte JJ, Anderson LE, Wolf DC & Degitz SJ 2005 Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology. Environmental Toxicology and Chemistry 24 926-933.
54. Tonacchera M, Pinchera A, Dimida A, Ferrarini E, Agretti P Vitti P, Santini F, Crump K & Gibbs J 2004 Relative potencies and additivity of perchlorate, thiocyanate, nitrate, and iodide on the inhibition of radioactive iodide uptake by the human sodium iodide symporter. Thyroid 14 1012-1019.
55. Trapasso F, Iuliano R, Chiefari E, Arturi F, Stella A, Filetti S, Fusco A & Russo D 1999 Iodide symporter gene expression in normal and transformed rat thyroid cells. European Journal of Endocrinology 140 447-451.
56. - symporter mRNAs in dog thyroid. Molecular and Cellular Endocrinology 131 195-203.
57. Vassart G & Dumont JE 1992 The thyrotropin receptor and the regulation of thyrocyte function and growth. Endocrine Reviews 13 596-611.
58. Viglietto G, Romano A, Manzo G, Chiappetta G, Paoletti I, Califano D, Galati MG, Mauriello V, Bruni P, Lago CT et al. 1997 Upregulation of the angiogenic factors PIGF, VEGF and their receptors (Flt-1, Flk-l/KDR) by TSH in cultured thyrocytes and in the thyroid gland of thiouracil-fed rats suggest a TSH-dependent paracrine mechanism for goiter hypervascularization. Oncogene 15 2687-2698.
59. Wagner S, Aust G, Schott M, Scherbaum WA, Feldkamp J & Seissler J 2002 Regulation of sodium-iodide-symporter gene expression in human thyrocytes measured by real-time polymerase chain reaction. Experimental and Clinical Endocrinology and Diabetes 110 398-402.
60. Wendl T, Lun K, Mione M, Favor J, Brand M, Wilson SW & Rohr KB 2002 pax2.1 is required for the development of thyroid follicles in zebrafish. Development 129 3751-3760.
61. Wolff J 1998 Perchlorate and the thyroid gland. Pharmacological Reviews 50 89-105.
62. Wright ML, Blanchard LS, Pikula A & Labieniec KE 1995 Circadian rhythms of thyroid secretion, morphometry, and cell division in prometamorphic and climax Rana tadpoles. General and Comparative Endocrinology 99 75-84.
63. Yamazaki K, Yamada E, Kanaji Y, Yanagisawa T, Kato Y, Takano K, Obara T & Sato K 2003 Genes regulated by thyrotropin and iodide in cultured human thyroid follicles: analysis by cDNA microarray. Thyroid 13 149-158.
64. Yen PM 2001 Physiological and molecular basis of thyroid hormone action. Physiological Reviews 81 1097-1142.