Excess iodide induces an acute inhibition of the sodium/iodide symporter in thyroid male rat cells by increasing reactive oxygen species

Endocrinology (United States)

Volumn 156, Issue 4, 2015, Pages 1540-1551

  Arriagada, Alejandro A ^a,b   Albornoz, Eduardo ^a,b   Opazo, Ma Cecilia ^a,b   Becerra, Alvaro ^a,b   Vidal, Gonzalo ^a,b   Fardella, Carlos ^b   Michea, Luis ^b,d   Carrasco, Nancy ^e   Simon, Felipe ^a,b   Elorza, Alvaro A ^a,b   Bueno, Susan M ^b,c,f   Kalergis, Alexis M ^b,c,f   Riedel, Claudia A ^a,b,f  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d UNIVERSITY OF CHILE   (Chile)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; IODIDE; IODINE 125; REACTIVE OXYGEN METABOLITE; SODIUM IODIDE SYMPORTER; THYROID HORMONE; THYROTROPIN; COTRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; INCUBATION TIME; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; THYROID CELL; ANIMAL; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; THYROID GLAND;

ANIMALS; CELL SURVIVAL; HYDROGEN PEROXIDE; IODIDES; MALE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SYMPORTERS; THYROID GLAND;

EID: 84926433830     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1371     Document Type: Article

References (56)

1. th ed. Philadelphia: Williams & Wilkins; 2000.
2. Dohan O, Carrasco N. Advances in Na(+)/I(-) symporter (NIS) research in the thyroid and beyond. Mol Cell Endocrinol. 2003;213:59-70.
3. Dohan O, De la Vieja A, Paroder V, et al. The sodium/iodide symporter (NIS): characterization, regulation, and medical significance. Endocr Rev. 2003;24:48-77.
4. Riedel C, Levy O, Carrasco N. Post-transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem. 2001;276:21458-21463.
5. Eng PH, Cardona GR, Fang SL, et al. Escape from the acute Wolff-Chaikoff effect is associated with a decrease in thyroid sodium/iodide symporter messenger ribonucleic acid and protein. Endocrinology. 1999;140:3404-3410.
6. Eng PH, Cardona GR, Previti MC, Chin WW, Braverman, LE. Regulation of the sodium iodide symporter by iodide in FRTL-5 cells. Eur J Endocrinol. 2001;144:139-144.
7. Leoni SG, Kimura ET, Santisteban P, De la Vieja A. Regulation of thyroid oxidative state by thioredoxin reductase has a crucial role in thyroid responses to iodide excess. Mol Endocrinol (Baltimore, Md). 2011;25:1924-1935.
8. Wolff J, Chaikoff IL. Plasma inorganic iodide as a homeostatic regulator of thyroid function. J Biol Chem. 1948;174:555-564.
9. Wolff J, Chaikoff IL, Goldberg RC, Meier JR. The temporary nature of the inhibitory action of excess iodide on organic iodine synthesis in the normal thyroid. Endocrinology. 1949;45:504-513.
10. Socolow EL, Dunlap D, Sobel RA, Ingbar SH. A correlative study of the effect of iodide administration in the rat on thyroidal iodide transport and organic iodine content. Endocrinology. 1968;83:737-743.
11. Dai G, Levy O, Carrasco N. Cloning and characterization of the thyroid iodide transporter. Nature. 1996;379:458-460.
12. Grollman EF, Smolar A, Ommaya A, Tombaccini D, Santisteban P. Iodine suppression of iodide uptake in FRTL-5 thyroid cells. Endocrinology. 1986;118:2477-2482.
13. Serrano-Nascimento C, Calil-Silveira J, Nunes MT. Posttranscriptional regulation of sodium-iodide symporter mRNA expression in the rat thyroid gland by acute iodide administration. Am J Physiol Cell Physiol. 2010;298:C893-C899.
14. Corvilain B, Van Sande J, Dumont JE. Inhibition by iodide of iodide binding to proteins: the "Wolff-Chaikoff" effect is caused by inhibition of H2O2 generation. Biochem Biophys Res Commun. 1988;154:1287-1292.
15. Corvilain B, Collyn L, Van Sande J, Dumont JE. Stimulation by iodide of H(2)O(2) generation in thyroid slices from several species. Am J Physiol Endocrinol Metab. 2000;278:E692-E699.
16. D'Autreaux BIT, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol. 2007;8:813-824.
17. Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47-95.
18. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science (New York, NY). 2006;312:1882-1883.
19. Foreman J, Demidchik V, Bothwell JHF, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422:442-446.
20. Fukayama H, Murakami S, Nasu M, Sugawara M. Hydrogen peroxide inhibits iodide uptake and iodine organification in cultured porcine thyroid follicles. Thyroid. 1991;1:267-271.
21. Nadolnik LI, Niatsetskaya ZV, Lupachyk SV. Effect of oxidative stress on rat thyrocyte iodide metabolism. Cell Biochem Funct. 2008;26:366-373.
22. Sugawara M, Yamaguchi DT, Lee HY, et al. Hydrogen peroxide inhibits iodide influx and enhances iodide efflux in cultured FRTL-5 rat thyroid cells. Eur J Endocrinol. 1990;122:610-616.
23. Ferreira ACF, Lima LIVP, Araujo RL, et al. Rapid regulation of thyroid sodium-iodide symporter activity by thyrotrophin and iodine. J Endocrinol. 2005;184:69-76.
24. Bürgi H. Iodine excess. Best Pract Res Clin Endocrinol. 2010;24(1):107-115.
25. Levy O, Dai G, Riedel C, et al. Characterization of the thyroid Na+/I- symporter with an anti-COOH terminus antibody. Proc Natl Acad Sci USA. 1997;94:5568-5573.
26. Ambesi-Impiombato FS, inventor. Living, fast-growing thyroid cell strain, FRTL-5. US Patent US4608341A. 1983.
27. Kaminsky SM, Levy O, Salvador C, Dai G, Carrasco N. Na(+)-I- symport activity is present in membrane vesicles from thyrotropin-deprived non-I(-)-transporting cultured thyroid cells. Proc Natl Acad Sci USA. 1994;91:3789-3793.
28. Nunez-Villena F, Becerra A, Echeverria C, et al. Increased expression of the transient receptor potential melastatin 7 channel is critically involved in lipopolysaccharide-induced reactive oxygen species-mediated neuronal death. Antioxid Redox Signal. 2011;15:2425-2438.
29. Becerra A, Echeverra C, Varela D, et al. Transient receptor potential melastatin 4 inhibition prevents lipopolysaccharide-induced endothelial cell death. Cardiovasc Res. 2011;91:677-684.
30. Simon F, Fernandez R. Early lipopolysaccharide-induced reactive oxygen species production evokes necrotic cell death in human umbilical vein endothelial cells. J Hypertens. 2009;27:1202-1216.
31. Albornoz EA, Carreño LJ, Cortés C, et al. Gestational hypothyroidism increases the severity of experimental autoimmune encephalomyelitis in adult offspring. Thyroid. 2013;23:1627-1637.
32. th ed. New York: Academic Press; 1986:499.
33. Muzzo S, Ramírez I, Carvajal F, Biolley E, Leiva L. Iodine nutrition in school children of four areas of Chile during the year 2001. Rev Med Chil. 2003;131:1391-1398.
34. Mussig K. Iodine-induced toxic effects due to seaweed consumption. In: Comprehensive Handbook of Iodine. New York: Academic Press; 2009:897-908.
35. Su L, Wang M, Yin S-T, et al. The interaction of selenium and mercury in the accumulations and oxidative stress of rat tissues. Ecotoxicol Environ Saf. 2008;70:483-489.
36. Chiu-Ugalde J, Theilig F, Behrends T, et al. Mutation of megalin leads to urinary loss of selenoprotein P and selenium deficiency in serum, liver, kidneys and brain. Biochem J. 2010;431:103-111.
37. Zhou X, Smith AM, Failla ML, Hill KE, Yu Z. Estrogen status alters tissue distribution and metabolism of selenium in female rats. J Nutr Biochem. 2012;23:532-538.
38. Hill KE, Zhou J, McMahan WJ, Motley AK. Deletion of selenoprotein P alters distribution of selenium in the mouse. J Biol Chem. 2003;278:13640-13646.
39. Levy O, De la Vieja A, Ginter CS, Riedel C, Dai G, Carrasco N. N-linked glycosylation of the thyroid Na+/I- symporter (NIS). Implications for its secondary structure model. J Biol Chem. 1998;273:22657-22663.
40. Song Y, Driessens N, Costa M, et al. Review: roles of hydrogen peroxide in thyroid physiology and disease. J Clin Endocrinol Metab. 2007;92:3764-3773.
41. Suzuki K, Kimura H, Wu H, et al. Excess iodide decreases transcription of NIS and VEGF genes in rat FRTL-5 thyroid cells. Biochem Biophys Res Commun. 2010;393:286-290.
42. Vitale M, Di Matola TD, D'Ascoli F, et al. Iodide excess induces apoptosis in thyroid cells through a p53-independent mechanism involving oxidative stress. Endocrinology. 2000;141:598-605.
43. Dupuy C, Virion A, Ohayon R, Kaniewski J, Deme D, Pommier J. Mechanism of hydrogen peroxide formation catalyzed by NADPH oxidase in thyroid plasma membrane. J Biol Chem. 1991;266, 3739-3743.
44. Taiwo FA. Mechanism of tiron as scavenger of superoxide ions and free electrons. Spectroscopy. 2008;22:491-498.
45. Li Y, Trush MA. Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem Biophys Res Commun. 1998;253:295-299.
46. Dröse S, Hanley PJ, Brandt U. Ambivalent effects of diazoxide on mitochondrial ROS production at respiratory chain complexes I and III. Biochim Biophys Acta. 2009;1790(6):558-565.
47. Perez-Gonzalez A, Galano A. OH radical scavenging activity of Edaravone: mechanism and kinetics. J Phys Chem B. 2011;115:1306-1314.
48. Yao X, Li M, He J, et al. Effect of early acute high concentrations of iodide exposure on mitochondrial superoxide production in FRTL cells. Free Radic Biol Med. 2012;52:1343-1352.
49. Bocanera LV, Krawiec L, Silberschmidt D, et al. Role of cyclic 3″5″ guanosine monophosphate and nitric oxide in the regulation of iodide uptake in calf thyroid cells. J Endocrinol. 1997;155:451-457.
50. Simon F, Stutzin A. Protein kinase C-mediated phosphorylation of p47 phox modulates platelet-derived growth factor-induced H2O2 generation and cell proliferation in human umbilical vein endothelial cells. Endothelium. 2008;15:175-188.
51. Simon F, Leiva-Salcedo E, Armisén R, et al. Hydrogen peroxide removes TRPM4 current desensitization conferring increased vulnerability to necrotic cell death. J Biol Chem. 2010;285:37150-37158.
52. Poole LB, Nelson KJ. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol. 2008;12:18-24.
53. Vadysirisack DD, Chen ESW, Zhang Z, Tsai MD, Chang GD, Jhiang SM. Identification of in vivo phosphorylation sites and their functional significance in the sodium iodide symporter. J BiolChem. 2007;282:36820-36828.
54. Thomasz L, Oglio R, Dagrosa MIAA, Krawiec LON, Pisarev MA, Juvenal GJ. 6 Iodo-δ-lactone reproduces many but not all the effects of iodide. Mol Cell Endocrinol. 2010;323:161-166.
55. Dugrillon A. Iodolactones and iodoaldehydes-mediators of iodine in thyroid autoregulation. Exp Clin Endocrinol Diabetes. 1996;104(suppl 4):41-45.
56. Kim H, Lee TH, Hwang YS, et al. Methimazole as an antioxidant and immunomodulator in thyroid cells: mechanisms involving in-terferon-γ signaling and H(2)O(2) scavenging. Mol Pharmacol. 2001;60:972-980.