Regulation of thyroid oxidative state by thioredoxin reductase has a crucial role in thyroid responses to iodide excess

Molecular Endocrinology

Volumn 25, Issue 11, 2011, Pages 1924-1935

  Leoni, Suzana G ^a   Kimura, Edna T ^b   Santisteban, Pilar ^a   de la Vieja, Antonio ^c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; IODIDE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SELENOPROTEIN; SODIUM IODIDE SYMPORTER; THIOREDOXIN REDUCTASE; THYROID HORMONE; TRANSCRIPTION FACTOR PAX8;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOREGULATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; GENE EXPRESSION; MALE; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THYROID GLAND; THYROID HORMONE RELEASE;

ANIMALS; BLOTTING, WESTERN; CELL LINE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; IODIDES; MALE; OXIDATION-REDUCTION; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; SYMPORTERS; THIOREDOXIN-DISULFIDE REDUCTASE; THYROID GLAND;

RATTUS;

EID: 80054966987     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-0038     Document Type: Article

References (70)

1. Ingbar SH 1972 Autoregulation of the thyroid. Response to iodide excess and depletion. Mayo Clin Proc 47:814-823
2. Greenspan F 1997 The thyroid gland. In: Greenspan F, Strewler G, eds. Basic and clinical endocrinology. 5th ed. London: Prentice-Hall International; 193-262
3. Morton ME 1944 Inhibiting effect of inorganic iodide on the formation in vitro of thyroxine and diiodotyrosine by surviving thyroid tissue. J Biol Chem 154:381-387
4. Wolff J, Chaikoff IL 1948 Plasma inorganic iodide, a chemical regulator of normal thyroid function. Endocrinology 42:468-471
5. Wolff J, Chaikoff IL, Goldberg RC, Meier JR 1949 The temporary nature of the inhibitory action of excess iodine on organic iodine synthesis in the normal thyroid. Endocrinology 45:504-513
6. Dai G, Levy O, Carrasco N 1996 Cloning and characterization of the thyroid iodide transporter. Nature 379:458-460
7. De La Vieja A, Dohan O, Levy O, Carrasco N 2000 Molecular analysis of the sodium/iodide symporter: impact on thyroid and extrathyroid pathophysiology. Physiol Rev 80:1083-1105
8. Braverman LE, Ingbar SH 1963 Changes in thyroidal function during adaptation to large doses of iodide. J Clin Invest 42:1216-1231
9. Spitzweg C, Joba W, Morris JC, Heufelder AE 1999 Regulation of sodium iodide symporter gene expression in FRTL-5 rat thyroid cells. Thyroid 9:821-830
10. Schmutzler C, Mentrup B, Schomburg L, Hoang-Vu C, Herzog V, Kohrle J 2007 Selenoproteins of the thyroid gland: expression, localization and possible function of glutathione peroxidase 3. Biol Chem 388:1053-1059
11. Schweizer U, Chiu J, Kohrle J 2008 Peroxides and peroxide-degrading enzymes in the thyroid. Antioxid Redox Signal 10:1577-1592
12. Kohrle J 2005 Selenium and the control of thyroid hormone metabolism. Thyroid 15:841-853
13. Vitale M, Di Matola T, D'Ascoli F, Salzano S, Bogazzi F, Fenzi G, Martino E, Rossi G 2000 Iodide excess induces apoptosis in thyroid cells through a p53-independent mechanism involving oxidative stress. Endocrinology 141:598-605
14. Golstein J, Dumont JE 1996 Cytotoxic effects of iodide on thyroid cells: difference between rat thyroid FRTL-5 cell and primary dog thyrocyte responsiveness. J Endocrinol Invest 19:119-126
15. Many MC, Mestdagh C, van den Hove MF, Denef JF 1992 In vitro study of acute toxic effects of high iodide doses in human thyroid follicles. Endocrinology 131:621-630
16. Leoni SG, Galante PA, Ricarte-Filho JC, Kimura ET 2008 Differential gene expression analysis of iodide-treated rat thyroid follic-ular cell line PCCl3. Genomics 91:356-366
17. Sen CK, Packer L 1996 Antioxidant and redox regulation of gene transcription. FASEB J 10:709-720
18. Degroot LJ, Greer MA 1956 The effect of stable iodide on thyroid secretion in man. Metabolism 5:682-696
19. Yamamoto K, Onaya T, Yamada T, Kotani M 1972 Inhibitory effect of excess iodide on thyroid hormone release as measured by intracellular colloid droplets. Endocrinology 90:986-991
20. Otake M, Sato A, Onaya TT, Yamada T 1973 Effect of repeated administration of excess iodide on thyroid hormone secretion in rats, with special reference to the escape from the iodide effect. Endocrinology 93:343-347
21. Eng PH, Cardona GR, Fang SL, Previti M, Alex S, Carrasco N, Chin WW, Braverman LE 1999 Escape from the acute Wolff-Chaikoff effect is associated with a decrease in thyroid sodium/iodide sym-porter messenger ribonucleic acid and protein. Endocrinology 140: 3404-3410
22. Eng PH, Cardona GR, Previti MC, Chin WW, Braverman LE 2001 Regulation of the sodium iodide symporter by iodide in FRTL-5 cells. Eur J Endocrinol 144:139-144
23. Serrano-Nascimento C, Calil-Silveira J, Nunes MT 2010 Posttran-scriptional regulation of sodium-iodide symporter mRNA expression in the rat thyroid gland by acute iodide administration. Am J Physiol Cell Physiol 298:C893-C899
24. 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. Mol Cell Biol 19:2051-2060
25. García B, Santisteban P 2002 PI3K is involved in the IGF-I inhibition of TSH-induced sodium/iodide symporter gene expression. Mol Endocrinol 16:342-352
26. Riedel C, Levy O, Carrasco N 2001 Post-transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem 276: 21458-21463
27. de la Vieja A, Ginter CS, Carrasco N 2004 The Q267E mutation in the sodium/iodide symporter (NIS) causes congenital iodide transport defect (ITD) by decreasing the NIS turnover number. J Cell Sci 117:677-687
28. Poncin S, Colin IM, Gerard AC 2009 Minimal oxidative load: a prerequisite for thyroid cell function. J Endocrinol 201:161-167
29. Lewin MH, Arthur JR, Riemersma RA, Nicol F, Walker SW, Millar EM, Howie AF, Beckett GJ 2002 Selenium supplementation acting through the induction of thioredoxin reductase and glutathione peroxidase protects the human endothelial cell line EAhy926 from damage by lipid hydroperoxides. Biochim Biophys Acta 1593: 85-92
30. Omata Y, Folan M, Shaw M, Messer RL, Lockwood PE, Hobbs D, Bouillaguet S, Sano H, Lewis JB, Wataha JC 2006 Sublethal concentrations of diverse gold compounds inhibit mammalian cytoso-lic thioredoxin reductase (TrxR1). Toxicol In Vitro 20:882-890
31. Otake M, Onaya T, Sato A, Yamada T 1973 Studies on the mechanism of inhibitory action of excess iodide on thyroid hormone secretion. Proc Soc Exp Biol Med 144:538-543
32. Suzuki K, Kimura H, Wu H, Kudo N, Kim WB, Suzuki S, Yoshida A, Caturegli P, Kohn LD 2010 Excess iodide decreases transcription of NIS and VEGF genes in rat FRTL-5 thyroid cells. Biochem Biophys Res Commun 393:286-290
33. Thomasz L, Oglio R, Dagrosa MA, Krawiec L, Pisarev MA, Juvenal GJ 2010 6 Iodo-delta-lactone reproduces many but not all the effects of iodide. Mol Cell Endocrinol 323:161-166
34. Ferre F, Clote P 2006 DiANNA 1.1: an extension of the DiANNA web server for ternary cysteine classification. Nucleic Acids Res 34:W182-W185
35. Cheng J, Randall AZ, Sweredoski MJ, Baldi P 2005 SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res 33:W72-W76
36. Fariselli P, Riccobelli P, Casadio R 1999 Role of evolutionary information in predicting the disulfide-bonding state of cysteine in proteins. Proteins 36:340-346
37. Spitzweg C, Morris JC 2010 Genetics and phenomics of hypothyroidism and goiter due to NIS mutations. Mol Cell Endocrinol 322:56-63
38. - symporter. Mechanism, stoichiometry, and specificity. J Biol Chem 272:27230-27238
39. Huc-Brandt S, Marcellin D, Graslin F, Averseng O, Bellanger L, Hivin P, Quemeneur E, Basquin C, Navarro V, Pourcher T, Dar-rouzet E 2011 Characterisation of the purified human sodium/ iodide symporter reveals that the protein is mainly present in a dimeric form and permits the detailed study of a native C-termi-nal fragment. Biochim Biophys Acta 1808:65-77
40. Landriscina M, Maddalena F, Laudiero G, Esposito F 2009 Adaptation to oxidative stress, chemoresistance, and cell survival. Anti-oxid Redox Signal 11:2701-2716
41. Schreck R, Baeuerle PA 1991 A role for oxygen radicals as second messengers. Trends Cell Biol 1:39-42
42. Maier J, van Steeg H, van Oostrom C, Paschke R, Weiss RE, Krohn K 2007 Iodine deficiency activates antioxidant genes and causes DNA damage in the thyroid gland of rats and mice. Biochim Biophys Acta 1773:990-999
43. Touyz RM, Schiffrin EL 2004 Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 122: 339-352
44. Chazenbalk GD, Valsecchi RM, Krawiec L, Burton G, Juvenal GJ, Monteagudo E, Chester HA, Pisarev MA 1988 Thyroid autoregu-lation. Inhibitory effects of iodinated derivatives of arachidonic acid on iodine metabolism. Prostaglandins 36:163-172
45. Panneels V, Macours P, Van den Bergen H, Braekman JC, Van Sande J, Boeynaems JM 1996 Biosynthesis and metabolism of 2-io-dohexadecanal in cultured dog thyroid cells. J Biol Chem 271: 23006-23014
46. Corvilain B, Collyn L, van Sande J, Dumont JE 2000 Stimulation by iodide of H2O2 generation in thyroid slices from several species. Am J Physiol Endocrinol Metab 278:E692-E699
47. Esposito F, Chirico G, Montesano Gesualdi N, Posadas I, Ammen-dola R, Russo T, Cirino G, Cimino F 2003 Protein kinase B activation by reactive oxygen species is independent of tyrosine kinase receptor phosphorylation and requires SRC activity. J Biol Chem 278:20828-20834
48. Giannoni E, Buricchi F, Grimaldi G, Parri M, Cialdai F, Taddei ML, Raugei G, Ramponi G, Chiarugi P 2008 Redox regulation of anoikis: reactive oxygen species as essential mediators of cell survival. Cell Death Differ 15:867-878
49. Esposito F, Ammendola R, Faraonio R, Russo T, Cimino F 2004 Redox control of signal transduction, gene expression and cellular senescence. Neurochem Res 29:617-628
50. Gruffat D, Venot N, Marriq C, Chabaud O 1992 Thyroid hormone synthesis in thyroglobulin secreted by porcine thyroid cells cultured on porous bottom chambers. Effect of iodide. Endocrinology 131: 2921-2927
51. Arner ES, Holmgren A 2000 Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102-6109
52. Holmgren A, Bjornstedt M 1995 Thioredoxin and thioredoxin reductase. Methods Enzymol 252:199-208
53. Gladyshev VN, Hatfield DL 1999 Selenocysteine-containing proteins in mammals. J Biomed Sci 6:151-160
54. Chen ZH, Saito Y, Yoshida Y, Sekine A, Noguchi N, Niki E 2005 4-Hydroxynonenal induces adaptive response and enhances PC12 cell tolerance primarily through induction of thioredoxin reductase 1 via activation of Nrf2. J Biol Chem 280:41921-41927
55. Steinbrenner H, Sies H 2009 Protection against reactive oxygen species by selenoproteins. Biochim Biophys Acta 1790:1478-1485
56. Voudouri AE, Chadio SE, Menegatos JG, Zervas GP, Nicol F, Arthur JR 2003 Selenoenzyme activities in selenium- and iodine-deficient sheep. Biol Trace Elem Res 94:213-224
57. Kohrle J, Gartner R 2009 Selenium and thyroid. Best Pract Res Clin Endocrinol Metab 23:815-827
58. Ueno H, Kajihara H, Nakamura H, Yodoi J, Nakamuro K 2007 Contribution of thioredoxin reductase to T-cell mitogenesis and NF-kB DNA-binding promoted by selenite. Antioxid Redox Signal 9:115-121
59. Mostert V, Hill KE, Burk RF 2003 Loss of activity of the selenoenzyme thioredoxin reductase causes induction of hepatic heme oxy-genase-1. FEBS Lett 541:85-88
60. Smith AD, Guidry CA, Morris VC, Levander OA 1999 Aurothio-glucose inhibits murine thioredoxin reductase activity in vivo. J Nutr 129:194-198
61. Bernier-Valentin F, Trouttet-Masson S, Rabilloud R, Selmi-Ruby S, Rousset B 2006 Three-dimensional organization of thyroid cells into follicle structures is a pivotal factor in the control of sodium/ iodide symporter expression. Endocrinology 147:2035-2042
62. Knight SA, Sunde RA 1987 The effect of progressive selenium deficiency on anti-glutathione peroxidase antibody reactive protein in rat liver. J Nutr 117:732-738
63. Smerdely P, Pitsiavas V, Boyages SC 1993 Methimazole inhibits FRTL5 thyroid cell proliferation by inducing S-phase arrest of the cell cycle. Endocrinology 133:2403-2406
64. Andrews NC, Faller DV 1991 A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 19:2499
65. Zaballos MA, Garcia B, Santisteban P 2008 Gfiy dimers released in response to thyrotropin activate phosphoinositide 3-kinase and regulate gene expression in thyroid cells. Mol Endocrinol 22:1183-1199
66. - symporter. Mol Endocrinol 19: 2847-2858
67. Karbowski M, Kurono C, Wozniak M, Ostrowski M, Teranishi M, Nishizawa Y, Usukura J, Soji T, Wakabayashi T 1999 Free radical-induced megamitochondria formation and apoptosis. Free Radic Biol Med 26:396-409
68. Riou C, Remy C, Rabilloud R, Rousset B, Fonlupt P 1998 H2O2 induces apoptosis of pig thyrocytes in culture. J Endocrinol 156: 315-322
69. Arner ES, Bjornstedt M, Holmgren A 1995 1-Chloro-2,4-dinitro-benzene is an irreversible inhibitor of human thioredoxin reductase. Loss of thioredoxin disulfide reductase activity is accompanied by a large increase in NADPH oxidase activity. J Biol Chem 270:3479-3482
70. Lawrence RA, Burk RF 1976 Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952-958