The acute inhibitory effect of iodide excess on sodium/iodide symporter expression and activity involves the PI3K/Akt signaling pathway

Endocrinology

Volumn 155, Issue 3, 2014, Pages 1145-1156

  Serrano Nascimento, Caroline ^a   Teixeira, Silvania Da Silva ^a   Nicola, Juan Pablo ^b   Nachbar, Renato Tadeu ^a   Masini Repiso, Ana Maria ^b   Nunes, Maria Tereza ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2 PHENYL 1,2 BENZISOXAZOL 3(2H) ONE; ACETYLCYSTEINE; HYDROETHIDINE; INSULIN; IODIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SODIUM IODIDE SYMPORTER; SUPEROXIDE; THYROTROPIN; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; INHIBITION KINETICS; MITOCHONDRION; NONHUMAN; OSMOLARITY; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; THYROID CELL;

ANIMALS; ANIONS; BIOTINYLATION; CELL LINE; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; INSULIN; IODIDES; MITOCHONDRIA; OXYGEN; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDES; SYMPORTERS; THYROID GLAND;

EID: 84896878820     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1665     Document Type: Article

References (74)

1. Carrasco N. Iodide transport in the thyroid gland. Biochem Biophys Acta. 1993;1154:65-82. (Pubitemid 23171390)
2. Dohán 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. (Pubitemid 36223279)
3. Ciullo I, Diez-Roux G, Di Domenico M, Migliaccio A, Avvedimento EV. cAMP signaling selectively influences Ras effectors pathways. Oncogene. 2001;20:1186-1192. (Pubitemid 32226244)
4. Coulonval K, Vandeput F, Stein RC, Kozma SC, Lamy F, Dumont JE. Phosphatidylinositol 3-kinase, protein kinase B and ribosomal S6 kinases in the stimulation of thyroid epithelial cell proliferation by cAMP and growth factors in the presence of insulin. Biochem J. 2000;348:351-358. (Pubitemid 30345208)
5. Kimura T, Van Keymeulen A, Golstein J, Fusco A, Dumont JE, Roger PP. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr Rev. 2001;22:631-656. (Pubitemid 32955247)
6. Suh JM, Song JH, Kim DW, et al. Regulation of the phosphatidylinositol 3-kinase, Akt/protein kinase B, FRAP/mammalian target of rapamycin, and ribosomal S6 kinase 1 signaling pathways by thyroid-stimulating hormone (TSH) and stimulating type TSH receptor antibodies in the thyroid gland. J Biol Chem. 2003;278:21960-21971. (Pubitemid 36792604)
7. Kogai T, Sajid-Crockett S, Newmarch LS, Liu YY, Brent GA. Phosphoinositide-3-kinase (PI3K) inhibition induces sodium/iodide symporter expression (NIS) in rat thyroid cells and human pappilary cancer cells. J Endocrinol. 2008;199:243-252.
8. Liu YY, Zhang X, Ringel MD, Jhiang SM. Modulation of sodium iodide symporter expression and function by LY294002, Akti1/2 and rapamycin in thyroid cells. Endocr Relat Cancer. 2012;19:291-304.
9. Garcia B, Santisteban P. PI3K is involved in the IGF-I inhibition of TSH-induced sodium/iodide symporter gene expression. Mol Endocrinol. 2002;16:342-352. (Pubitemid 34131229)
10. Saji M, Kohn LD. Insulin and insulin-like growth factor-I inhibit thyrotropin-increased iodide transport in serum-depleted FRTL-5 rat thyroid cells: modulation of adenosine 3′,5′-monophosphate signal action. Endocrinology. 1991;128:1136-1143.
11. Zaballos MA, Garcia B, Santisteban P. Gβγ dimers released in response to thyrotropin activate phosphoinositide 3-kinase and regulate gene expression in thyroid cells. Mol Endocrinol. 2008;22:1183-1199. (Pubitemid 351629618)
12. de Souza EC, Padrón AS, Braga WM, et al. mTOR downregulates iodide uptake in thyrocytes. J Endocrinol. 2010;206:113-120.
13. Hou P, Bojdani E, Xing M. Induction of thyroid gene expression and radioiodine uptake in thyroid cancer cells by targeting major signaling pathways. J Clin Endocrinol Metab. 2010;95:820-828.
14. Morton ME, Chaikoff IL, Rosenfeld S. Inhibiting effect of inorganic iodide on the formation in vitro of thyroxine and diiodotyrosine by surviving thyroid tissue. J Biol Chem. 1944;154:381-387.
15. Wolff J, Chaikoff IL. Plasma inorganic iodide as a homeostatic regulator of thyroid function. J Biol Chem. 1948;174:555-564.
16. Wolff J, Chaikoff IL, Goldberg RC, Meier JR. The temporary nature of the innibitory action of excess iodide on organic iodine synthesis in the normal thyroid. Endocrinology. 1949;45:504-513.
17. Raben MS. The paradoxical effect of thiocyanate and of thyrotropin on the organic binding of iodine by the thyroid in the presence of large amounts of iodide. Endocrinology. 1949;45:296-304.
18. Braverman LE, Ingbar SH. Changes in thyroidal function during adaptation to large doses of iodide. J Clin Invest. 1963;42:1216-1231.
19. 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. (Pubitemid 16058422)
20. Spitzweg C, Joba W, Morris JC, Heufelder AE. Regulation of sodium iodide symporter gene expression in FRTL-5 rat thyroid cells. Thyroid. 1999;9:821-830. (Pubitemid 29409667)
21. Uyttersprot N, Pelgrims N, Carrasco N, et al. Moderate doses of iodide in vivo inhibit cell proliferation and the expression of thyroperoxidase and Na+/I- symporter mRNAs in dog thyroid. Mol Cell Endocrinol. 1997;131:195-203. (Pubitemid 27384896)
22. 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. (Pubitemid 30645394)
23. 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. (Pubitemid 32181684)
24. Ferreira AC, Lima LP, Araújo RL, et al. Rapid regulation of thyroid sodium-iodide symporter activity by thyrotrophin and iodine. J Endocrinol. 2005;184:69-76. (Pubitemid 40207562)
25. Leoni SG, Galante PA, Ricarte-Filho JC, Kimura ET. Differential gene expression analysis of iodide-treated rat thyroid follicular cell line PCCl3. Genomics. 2008;91:356-366.
26. 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. 2011;25:1924-1935.
27. 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.
28. Serrano-Nascimento C, Calil-Silveira J, Goulart-Silva F, Nunes MT. Newinsights about the posttranscriptional mechanisms triggered by iodide excess on sodium/iodide symporter (NIS) expression in PCCl3 cells. Mol Cell Endocrinol. 2012;349:154-161.
29. Poncin S, Gérard AC, Boucquey M, et al. 2008 Oxidative stress in the thyroid gland: from harmlessness to hazard depending on the iodine content. Endocrinology. 2008;149:424-433.
30. Poncin S, Colin IM, Gérard AC. Minimal oxidative load: a prerequisite for thyroid cell function. J Endocrinol. 2009;201:161-167.
31. Vitale M, Di Matola T, 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. (Pubitemid 32250483)
32. 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.
33. Many MC, Mestdagh C, van den Hove MF, Denef JF. In vitro study of acute toxic effects of high iodide doses in human thyroid follicles. Endocrinology. 1992;131:621-630.
34. Golstein J, Dumont JE. Cytotoxic effects of iodide on thyroid cells: difference between rat thyroid FRTL-5 cell and primary dog thyrocyte responsiveness. J Endocrinol Invest. 1996;19:119-126.
35. Chen L, Xu B, Liu L, et al. Cadmium induction of reactive oxygen species activates the mTOR pathway, leading to neuronal cell death. Free Radic Biol Med Mar. 2011;50:624-632.
36. Ushio-Fukai M, Alexander RW, Akers M, et al. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II invascular smooth muscle cells. J Biol Chem. 1999;274:22699-22704.
37. Son YO, Wang L, Poyil P, et al. Cadmium induces carcinogenesis in BEAS-2B cells through ROS-dependent activation of PI3K/AKT/GSK-3β/β-catenin signaling. Toxicol Appl Pharmacol. 2012;264:153-160.
38. Sadidi M, Lentz SI, Feldman EL. Hydrogen peroxide-induced Akt phosphorylation regulates Bax activation. Biochimie. 2009;91:577-585.
39. Dong-Yun S, Yu-Ru D, Shan-Lin L, Ya-Dong Z, Lian W. Redox stress regulates cell proliferation and apoptosis of human hepatoma through Akt protein phosphorylation. FEBS Lett. 2003;542:60-64.
40. 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. (Pubitemid 27241810)
41. Nicola JP, Nazar M, Mascanfroni ID, Pellizas CG, Masini-Repiso AM. NF-κB p65 subunit mediates lipopolysaccharide-induced Na(+)/I(-) symporter gene expression by involving functional interaction with the paired domain transcription factor Pax8. Mol Endocrinol. 2010;24:1846-1862.
42. Sue M, Akama T, Kawashima A, et al. Propylthiouracil increases sodium/iodide symporter gene expression and iodide uptake in rat thyroid cells in the absence of TSH. Thyroid. 2012;22:844-852.
43. Wolff J. Perchlorate and the thyroid gland. Pharmacol Rev. 1998;50:89-115.
44. Dohán O, Portulano C, Basquin C, Reyna-Neyra A, Amzel LM, Carrasco N. The Na+/I symporter (NIS) mediates electroneutral active transport of the environmental pollutant perchlorate. Proc Natl Acad Sci USA. 2007;104:20250-20255.
45. Paroder-Belenitsky M, Maestas MJ, Dohán O, et al. Mechanism of anion selectivity and stoichiometry of the Na+/I- symporter (NIS). Proc Natl Acad Sci USA. 2011;108:17933-17938.
46. Zuo L, Christofi FL, Wright VP, et al. Intra- and extracellular measurement of reactive oxygen species produced during heat stress in diaphragm muscle. Am J Physiol Cell Physiol. 2000;279:C1058-C1066.
47. Cotgreave IA. N-acetylcysteine: pharmacological considerations and experimental and clinical applications. Adv Pharmacol. 1997;38:205-227.
48. Sies H. Ebselen, a selenoorganic compound as glutathione peroxidase mimic. Free Radic Biol Med. 1993;14:313-323. (Pubitemid 23066372)
49. Graciano MF, Valle MM, Curi R, Carpinelli AR. Evidence for the involvement of GPR40 and NADPH oxidase in palmitic acid-induced superoxide production and insulin secretion. Islets. 2013;5(4):139-148.
50. Nicola JP, Nazar M, Serrano-Nascimento C, et al. Iodide transport defect: functional characterization of a novel mutation in the Na+/I-symporter 5′-untranslated region in a patient with congenital hypothyroidism. J Clin Endocrinol Metab. 2011;96:E1100-E1107.
51. Riedel C, Levy O, Carrasco N. Post-transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem. 2001;276:21458-21463.
52. Cheng JQ, Lindsley CW, Cheng GZ, Yang H, Nicosia SV. The Akt/PKB pathway: molecular target for cancer drug discovery. Oncogene. 2005;24:7482-7492. (Pubitemid 41637988)
53. Fayard E, Tintignac LA, Baudry A, Hemmings BA. Protein kinase B/Akt at a glance. J Cell Sci. 2005;118:5675-5678. (Pubitemid 43079259)
54. Dohán O, Dela Vieja A, Carrasco N. Hydrocortisone and purinergic signaling stimulate sodium/iodide symporter (NIS)-mediated iodide transport in breast cancer cells. Mol Endocrinol. 2006;20:1121-1137.
55. 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.
56. Nicola JP, Reyna-Neyra A, Carrasco N, Masini-Repiso AM. Dietary iodide controls its own absorption through post-transcriptional regulation of the intestinal Na+/I- symporter. J Physiol. 2012;590:6013-6026.
57. Cass LA, Summers SA, Prendegast GV, Backer JM, Birnbaum MJ, Meinkoth JL. Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol Cell Biol. 1999;19:5882-5891. (Pubitemid 29399293)
58. Dugrillon A. Iodolactones and iodoaldehydes-mediators of iodine in thyroid autoregulation. Exp Clin Endocrinol Diabetes. 1996;104:41-45. (Pubitemid 26418398)
59. Ringel MD, Hayre N, Saito J, et al. Overexpression and overactivation of AKT in thyroid carcinoma. Cancer Res. 2001;61:6105-6111. (Pubitemid 32762546)
60. Saji M, Ringel MD. The PI3K-Akt-mTOR pathway in initiation and progression of thyroid tumors. Mol Cell Endocrinol. 2010;321:20-28.
61. Xing M. Genetic alterations in PI3K/Akt pathway in thyroid cancer. Thyroid. 2010;20:697-706.
62. Botelho RJ, Tapper H, Furuya W, Mojdami D, Grinstein S. Fc γR-mediated phagocytosis stimulates localized pinocytosis in human neutrophils. J Immunol. 2002;69:4423-4429. (Pubitemid 35178217)
63. Uriarte SM, Jog NR, Luerman GC, Bhimani S, Ward RA, Mcleish KR. Counterregulation of clathrin-mediated endocytosis by the actin and microtubular cytoskeleton in human neutrophils. Am J Physiol Cell Physiol. 2009;96:C857-C867.
64. Knostman KA, McCubrey JA, Morrison CD, Zhang Z, Capen CC, Jhiang SM. PI3K activation is associated with intracellular sodium/iodide symporter protein expression in breast cancer. BMC Cancer. 2007;7:137.
65. 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.
66. Song Y, Driessens N, Costa M, et al. Roles of hydrogen peroxide in thyroid physiology and disease. J Clin Endocrinol Metab. 2007;92:3764-3773. (Pubitemid 47607620)
67. Haughland R. Eugene, OR. Molecular Probes. Handbook of Fluorescent Probes and Research Chemicals. 11th ed. Eugene, OR: Catalogue of Molecular Probes, Inc; 2009.
68. Denu JM, Tanner KG. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry. 1998;37:5633-5642. (Pubitemid 28241948)
69. Lee SR, Kwon KS, Kim SR, Rhee SG. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem. 1998;273:15366-15372. (Pubitemid 28298140)
70. Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell. 2002;9:387-399. (Pubitemid 34195563)
71. Downes CP, Walker S, McConnachie G, Lindsay Y, Batty IH, Leslie NR. Acute regulation of the tumour suppressor phosphatase, PTEN, by anionic lipids and reactive oxygen species. Biochem Soc Trans. 2004;32:338-342. (Pubitemid 38582123)
72. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem. 1998;273:13375-13378. (Pubitemid 28268370)
73. Lee SR, Yang KS, Kwon J, Lee C, Jeong W, Rhee SG. Reversible inactivation of the tumor suppressor PTEN by H2O2. J Biol Chem. 2002;277:20336-20342. (Pubitemid 34967328)
74. Leslie NR, Bennett D, Lindsay YE, Stewart H, Gray A, Downes CP. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 2003;22:5501-5510. (Pubitemid 37279959)