Iodide excess regulates its own efflux: A possible involvement of pendrin

American Journal of Physiology - Cell Physiology

Volumn 310, Issue 7, 2016, Pages C576-C582

  Calil Silveira, Jamile ^a   Serrano Nascimento, Caroline ^a   Kopp, Peter Andreas ^b   Nunes, Maria Tereza ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Iodide efflux; Iodide excess; Pendrin; Wolff Chaikoff effect escape

Indexed keywords

BETA ACTIN; IODIDE; MESSENGER RNA; PENDRIN; BICARBONATE CHLORIDE ANTIPORTER; PENDRIN PROTEIN, RAT; SODIUM IODIDE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; THYROID FOLLICULAR CELL; ANIMAL; CELL LINE; DRUG EFFECTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; THYMOCYTE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CHLORIDE-BICARBONATE ANTIPORTERS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; RATS; REAL-TIME POLYMERASE CHAIN REACTION; SODIUM IODIDE; THYMOCYTES;

EID: 84983784459     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00210.2015     Document Type: Article

References (49)

1. Arriagada AA, Albornoz E, Opazo MC, Becerra A, Vidal G, Fardella C, Michea L, Carrasco N, Simon F, Elorza AA, Bueno SM, Kalergis AM, Riedel CA. Excess iodide induces an acute inhibition of the sodium/ iodide symporter in thyroid male rat cells by increasing reactive oxygen species. Endocrinology 156: 1540–1551, 2015.
2. Bizhanova A, Kopp P. Minireview: The sodium-iodide symporter NIS and pendrin in iodide homeostasis of the thyroid. Endocrinology 150: 1084–1090, 2009.
3. Braverman LE, Ingbar SH. Changes in thyroidal function during adaptation to large doses of iodide. J Clin Invest 42: 1216–1231, 1963.
4. Burgi H. Iodine excess. Best Pract Res Clin Endocrinol Metab 24: 107–115, 2010.
5. Burgi H, Radvila A, Kohler H, Studer H. Effects of pharmacological doses of iodide on the hyperplastic rat thyroid gland. Roles of intrathyroidal iodide, thyrotropin and thyroglobulin in the Wolff-Chaikoff phenomenon. Endocrinology 95: 388–396, 1974.
6. Calebiro D, Porazzi P, Bonomi M, Lisi S, Grindati A, De Nittis D, Fugazzola L, Marino M, Botta G, Persani L. Absence of primary hypothyroidism and goiter in Slc26a4 (-/-) mice fed on a low iodine diet. J Endocrinol Invest 34: 593–598, 2011.
7. Calil-Silveira J, Serrano-Nascimento C, Nunes MT. Iodide treatment acutely increases pendrin (SLC26A4) mRNA expression in the rat thyroid and the PCCl3 thyroid cell line by transcriptional mechanisms. Mol Cell Endocrinol 350: 118–124, 2012.
8. Dohan O, De la Vieja A, Carrasco N. Hydrocortisone and purinergic signaling stimulate sodium/iodide symporter (NIS)-mediated iodide transport in breast cancer cells. Mol Endocrinol 20: 1121–1137, 2006.
9. Dossena S, Bizhanova A, Nofziger C, Bernardinelli E, Ramsauer J, Kopp P, Paulmichl M. Identification of allelic variants of pendrin (SLC26A4) with loss and gain of function. Cell Physiol Biochem 28: 467–476, 2011.
10. Dossena S, Nofziger C, Tamma G, Bernardinelli E, Vanoni S, Nowak C, Grabmayer E, Kossler S, Stephan S, Patsch W, Paulmichl M. Molecular and functional characterization of human pendrin and its allelic variants. Cell Physiol Biochem 28: 451–466, 2011.
11. - transport activity. Cell Physiol Biochem 18: 67–74, 2006.
12. Eng PH, Cardona GR, Fang SL, Previti M, Alex S, Carrasco N, Chin WW, Braverman LE. Escape from the acute Wolff-Chaikoff effect is associated with a decrease in thyroid sodium/iodide symporter messenger ribonucleic acid and protein. Endocrinology 140: 3404–3410, 1999.
13. 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 144: 139–144, 2001.
14. Everett LA, Belyantseva IA, Noben-Trauth K, Cantos R, Chen A, Thakkar SI, Hoogstraten-Miller SL, Kachar B, Wu DK, Green ED. Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Hum Mol Genet 10: 153–161, 2001.
15. Fong P. Thyroid iodide efflux: a team effort? J Physiol 589: 5929–5939, 2011.
16. Galrao AL, Camargo RY, Friguglietti CU, Moraes L, Cerutti JM, Serrano-Nascimento C, Suzuki MF, Medeiros-Neto G, Rubio IG. Hypermethylation of a new distal sodium/iodide symporter (NIS) enhancer (NDE) is associated with reduced NIS expression in thyroid tumors. J Clin Endocrinol Metab 99: E944–E952, 2014.
17. Gillam MP, Sidhaye AR, Lee EJ, Rutishauser J, Stephan CW, Kopp P. Functional characterization of pendrin in a polarized cell system. Evidence for pendrin-mediated apical iodide efflux. J Biol Chem 279: 13004–13010, 2004.
18. Golstein P, Abramow M, Dumont JE, Beauwens R. The iodide channel of the thyroid: a plasma membrane vesicle study. Am J Physiol Cell Physiol 263: C590–C597, 1992.
19. Iosco C, Cosentino C, Sirna L, Romano R, Cursano S, Mongia A, Pompeo G, di Bernardo J, Ceccarelli C, Tallini G, Rhoden KJ. Anoctamin 1 is apically expressed on thyroid follicular cells and contributes to ATP- and calcium-activated iodide efflux. Cell Physiol Biochem 34: 966–980, 2014.
20. Iwata T, Yoshida T, Teranishi M, Murata Y, Hayashi Y, Kanou Y, Griffith AJ, Nakashima T. Influence of dietary iodine deficiency on the thyroid gland in Slc26a4-null mutant mice. Thyroid Res 4: 10, 2011.
21. Kopp P. Thyroid hormone synthesis. In: Werner and Ingbar’s The Thyroid: A Fundamental and Clinical Text, edited by Braverman LE and Cooper D. Philadelphia, PA: Lippincott-Raven, 2013, p. 48–74.
22. Kopp P, Pesce L, Solis SJ. Pendred syndrome and iodide transport in the thyroid. Trends Endocrinol Metab 19: 260–268, 2008.
23. Leoni SG, Galante PA, Ricarte-Filho JC, Kimura ET. Differential gene expression analysis of iodide-treated rat thyroid follicular cell line PCCl3. Genomics 91: 356–366, 2008.
24. 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 25: 1924–1935, 2011.
25. 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 154: 381–387, 1944.
26. Muscella A, Marsigliante S, Verri T, Urso L, Dimitri C, Botta G, Paulmichl M, Beck-Peccoz P, Fugazzola L, Storelli C. PKC-epsilondependent cytosol-to-membrane translocation of pendrin in rat thyroid PC Cl3 cells. J Cell Physiol 217: 103–112, 2008.
27. Palos F, Garcia-Rendueles ME, Araujo-Vilar D, Obregon MJ, Calvo RM, Cameselle-Teijeiro J, Bravo SB, Perez-Guerra O, Loidi L, Czarnocka B, Alvarez P, Refetoff S, Dominguez-Gerpe L, Alvarez CV, Lado-Abeal J. Pendred syndrome in two Galician families: insights into clinical phenotypes through cellular, genetic, and molecular studies. J Clin Endocrinol Metab 93: 267–277, 2008.
28. Pesce L, Bizhanova A, Caraballo JC, Westphal W, Butti ML, Comellas A, Kopp P. TSH regulates pendrin membrane abundance and enhances iodide efflux in thyroid cells. Endocrinology 153: 512–521, 2012.
29. - symporter (NIS): mechanism and medical impact. Endocr Rev 35: 106–149, 2014.
30. Pramyothin P, Leung AM, Pearce EN, Malabanan AO, Braverman LE. Clinical problem-solving. A hidden solution. N Engl J Med 365: 2123–2127, 2011.
31. Raben MS. The paradoxical effects of thiocyanate and of thyrotropin on the organic binding of iodine by the thyroid in the presence of large amounts of iodide. Endocrinology 45: 296–304, 1949.
32. Scott DA, Wang R, Kreman TM, Andrews M, McDonald JM, Bishop JR, Smith RJ, Karniski LP, Sheffield VC. Functional differences of the PDS gene product are associated with phenotypic variation in patients with Pendred syndrome and non-syndromic hearing loss (DFNB4). Hum Mol Genet 9: 1709–1715, 2000.
33. Scott DA, Wang R, Kreman TM, Sheffield VC, Karniski LP. The Pendred syndrome gene encodes a chloride-iodide transport protein. Nat Genet 21: 440–443, 1999.
34. Serrano-Nascimento C, Calil-Silveira J, Goulart-Silva F, Nunes MT. New insights about the posttranscriptional mechanisms triggered by iodide excess on sodium/iodide symporter (NIS) expression in PCCl3 cells. Mol Cell Endocrinol 349: 154–161, 2012.
35. 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 298: C893–C899, 2010.
36. Serrano-Nascimento C, da Silva Teixeira S, Nicola JP, Nachbar RT, Masini-Repiso AM, Nunes MT. The acute inhibitory effect of iodide excess on sodium/iodide symporter expression and activity involves the PI3K/Akt signaling pathway. Endocrinology 155: 1145–1156, 2014.
37. - and (formula presented) secretion and in regulation of CFTR in the parotid duct. J Physiol 586: 3813–3824, 2008.
38. Taylor JP, Metcalfe RA, Watson PF, Weetman AP, Trembath RC. Mutations of the PDS gene, encoding pendrin, are associated with protein mislocalization and loss of iodide efflux: implications for thyroid dysfunction in Pendred syndrome. J Clin Endocrinol Metab 87: 1778–1784, 2002.
39. Twyffels L, Strickaert A, Virreira M, Massart C, Van Sande J, Wauquier C, Beauwens R, Dumont JE, Galietta LJ, Boom A, Kruys V. Anoctamin-1/TMEM16A is the major apical iodide channel of the thyrocyte. Am J Physiol Cell Physiol 307: C1102–C1112, 2014.
40. - symporter mRNAs in dog thyroid. Mol Cell Endocrinol 131: 195–203, 1997.
41. van den Hove MF, Croizet-Berger K, Jouret F, Guggino SE, Guggino WB, Devuyst O, Courtoy PJ. The loss of the chloride channel, ClC-5, delays apical iodide efflux and induces a euthyroid goiter in the mouse thyroid gland. Endocrinology 147: 1287–1296, 2006.
42. Velez ML, Costamagna E, Kimura ET, Fozzatti L, Pellizas CG, Montesinos MM, Lucero AM, Coleoni AH, Santisteban P, Masini-Repiso AM. Bacterial lipopolysaccharide stimulates the thyrotropin-dependent thyroglobulin gene expression at the transcriptional level by involving the transcription factors thyroid transcription factor-1 and paired box domain transcription factor 8. Endocrinology 147: 3260–3275, 2006.
43. 2+. Endocrinology 114: 1108–1113, 1984.
44. Wolff J. What is the role of pendrin? Thyroid 15: 346–348, 2005.
45. Wolff J, Chaikoff IL. Plasma inorganic iodide as a homeostatic regulator of thyroid function. J Biol Chem 174: 555–564, 1948.
46. Wolff J, Chaikoff IL, Goldberg RC, Meier JR. The temporary nature of the inhibitory action of excess iodine on organic iodine synthesis in the normal thyroid. Endocrinology 45: 504–513, 1949.
47. Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev 81: 1097–1142, 2001.
48. Yoshida A, Hisatome I, Taniguchi S, Sasaki N, Yamamoto Y, Miake J, Fukui H, Shimizu H, Okamura T, Okura T, Igawa O, Shigemasa C, Green ED, Kohn LD, Suzuki K. Mechanism of iodide/chloride exchange by pendrin. Endocrinology 145: 4301–4308, 2004.
49. Yoshida A, Taniguchi S, Hisatome I, Royaux IE, Green ED, Kohn LD, Suzuki K. Pendrin is an iodide-specific apical porter responsible for iodide efflux from thyroid cells. J Clin Endocrinol Metab 87: 3356–3361, 2002.