Iodine mediated mechanisms and thyroid carcinoma

Critical Reviews in Clinical Laboratory Sciences

Volumn 46, Issue 5-6, 2009, Pages 302-318

  Liu, Xiao Hong ^a   Chen, George G ^a   Vlantis, Alexander C ^a   Van Hasselt, C Andrew ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Anti tumor treatment; Apoptosis; Carcinogenesis; Cell death; Iodine; Iodine transporters; Prevention; Proliferation; Thyroid cancer

Indexed keywords

AMIODARONE; CARRIER PROTEIN; CHORIONIC GONADOTROPIN; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; IODINE; PENDRIN; RADIOACTIVE IODINE; RETINOIC ACID; ROMIDEPSIN; SODIUM IODIDE; THYROGLOBULIN; THYROTROPIN; TRANSFORMING GROWTH FACTOR BETA1; TRICHOSTATIN A; VALPROIC ACID;

ADJUVANT THERAPY; APOPTOSIS; CANCER ADJUVANT THERAPY; CANCER EPIDEMIOLOGY; CANCER PREVENTION; CANCER RADIOTHERAPY; CANCER SURGERY; CARCINOGENESIS; CELL CYCLE ARREST; CELL PROLIFERATION; HISTOPATHOLOGY; HUMAN; IONIZING RADIATION; IRON DEFICIENCY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; SODIUM TRANSPORT; THYROID CARCINOMA; THYROID FOLLICLE CELL; THYROID FOLLICULAR CARCINOMA;

ADENOCARCINOMA; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IODINE; SYMPORTERS; THYROID GLAND; THYROID NEOPLASMS;

EID: 71849115908     PISSN: 10408363     EISSN: 1549781X     Source Type: Journal    
DOI: 10.3109/10408360903306384     Document Type: Review

References (237)

1. Bizhanova A, Kopp P. The sodium-iodide symporter NIS and pendrin in iodide homeostasis of the thyroid. Endocrinology 2009;150: 1084-1090.
2. Dohan O, De la Vieja A, Paroder V, Riedel C, Artani M, Reed M, Ginter CS, Carrasco N. Te sodium/iodide sym-porter (NIS): characterization, regulation, and medical sig-nifcance. Endocr Rev 2003; 24: 48-77.
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Tun MJ. Cancer statistics, 2008. CA Cancer J Clin 2008; 58: 71-96.
4. Nef RL, Farrar WB, Kloos RT, Burman KD. Anaplastic thyroid cancer. Endocrinol Metab Clin North Am 2008; 37: 525-538.
5. Toniato A, Boschin I, Casara D, Mazzarotto R, Rubello D, Pelizzo M. Papillary thyroid carcinoma: factors infuenc-ing recurrence and survival. Ann Surg Oncol 2008; 15: 1518-1522.
6. Maier J, van Steeg H, van Oostrom C, Paschke R, Weiss RE, Krohn K. Iodine defciency activates antioxidant genes and causes DNA damage in the thyroid gland of rats and mice. Biochim Biophys Acta 2007; 1773: 990-999.
7. Krohn K, Maier J, Paschke R. Mechanisms of disease: hydrogen peroxide, DNA damage and mutagenesis in the development of thyroid tumors. Nat Clin Pract Endocrinol Metab 2007; 3: 713-720.
8. Dal Maso L, Bosetti C, La Vecchia C, Franceschi S. Risk factors for thyroid cancer: an epidemiological review focused on nutritional factors. Cancer Causes Control 2009; 20: 75-86.
9. Dijkstra B, Prichard RS, Lee A, Kelly LM, Smyth PP, Crotty T, McDermott EW, Hill AD, O'Higgins N. Changing patterns of thyroid carcinoma. Ir J Med Sci 2007; 176: 87-90.
10. Farahati J, Geling M, Mader U, Mortl M, Luster M, Muller JG, Flentje M, Reiners C. Changing trends of incidence and prognosis of thyroid carcinoma in lower Franconia, Germany, from 1981-1995. Tyroid 2004; 14: 141-147.
11. Vitale M, Di Matola T, D'Ascoli F, Salzano S, Bogazzi F, Fenzi G, Martino E, Rossi G. Iodide excess induces apop-tosis in thyroid cells through a p53-independent mechanism involving oxidative stress. Endocrinology 2000; 141: 598-605.
12. Gimm O. Tyroid cancer. Cancer Lett 2001; 163: 143-156.
13. Kuo SF, Chao TC, Chang HY, Hsueh C, Chang YC, Yang CH, Lin JD. Te role of radioactive iodine therapy in young patients with papillary thyroid cancer. Clin Nucl Med 2009; 34: 4-6.
14. Kebebew E, Greenspan FS, Clark OH, Woeber KA, McMillan A. Anaplastic thyroid carcinoma. Treatment outcome and prognostic factors. Cancer 2005; 103: 1330-1335.
15. Smallridge RC, Marlow LA, Copland JA. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr Relat Cancer 2009; 16: 17-44.
16. Hunt JL, Tometsko M, LiVolsi VA, Swalsky P, Finkelstein SD, Barnes EL. Molecular evidence of anaplastic transformation in coexisting well-diferentiated and anaplastic carcinomas of the thyroid. Am J Surg Pathol 2003; 27: 1559-1564.
17. Nikiforov YE. Genetic alterations involved in the transition from well-diferentiated to poorly diferentiated and ana-plastic thyroid carcinomas. Endocr Pathol 2004; 15: 319-327.
18. Kloos RT. Papillary thyroid cancer: medical management and follow-up. Curr Treat Options Oncol 2005; 6: 323-338.
19. Chiacchio S, Lorenzoni A, Boni G, Rubello D, Elisei R, Mariani G. Anaplastic thyroid cancer: prevalence, diagnosis and treatment. Minerva Endocrinol 2008; 33: 341-357.
20. Richardson DB. Exposure to ionizing radiation in adulthood and thyroid cancer incidence. Epidemiology 2009; 20: 181-187.
21. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature 2001; 411: 342-348.
22. Baverstock K, Eglof B, Pinchera A, Ruchti C, Williams D. Tyroid cancer after Chernobyl. Nature 1992; 359: 21-22.
23. Williams D. Cancer after nuclear fallout: lessons from the Chernobyl accident. Nat Rev Cancer 2002; 2: 543-549.
24. Belfore A, Russo D, Vigneri R, Filetti S. Graves' disease, thyroid nodules and thyroid cancer. Clin Endocrinol (Oxf) 2001; 55: 711-718.
25. Schaller RT, Jr, Stevenson JK. Development of carcinoma of the thyroid in iodine-defcient mice. Cancer 1966; 19: 1063-1080.
26. Fortner JG, George PA, Sternberg SS. Induced and spontaneous thyroid cancer in the Syrian (golden) hamster. Endocrinology 1960; 6: 364-376.
27. Boltze C, Brabant G, Dralle H, Gerlach R, Roessner A, Hoang-Vu C. Radiation-induced thyroid carcinogenesis as a function of time and dietary iodine supply: an in vivo model of tumorigenesis in the rat. Endocrinology 2002; 143: 2584-2592.
28. Kanno J, Onodera H, Furuta K, Maekawa A, Kasuga T, Hayashi Y. Tumor-promoting efects of both iodine def-ciency and iodine excess in the rat thyroid. Toxicol Pathol 1992; 20: 226-235.
29. Nishikawa A, Ikeda T, Son HY, Okazaki K, Imazawa T, Umemura T, Kimura S, Hirose M. Pronounced synergis-tic promotion of N-bis(2-hydroxypropyl) nitrosamine-initiated thyroid tumorigenesis in rats treated with excess soybean and iodine-defcient diets. Toxicol Sci 2005; 86: 258-263.
30. Williams ED, Abrosimov A, Bogdanova T, Demidchik EP, Ito M, LiVolsi V, Lushnikov E, Rosai J, Tronko MD, Tsyb AF, Vowler SL, Tomas GA. Morphologic characteristics of Chernobyl-related childhood papillary thyroid carcinomas are independent of radiation exposure but vary with iodine intake. Tyroid 2008; 18: 847-852.
31. Song Y, Driessens N, Costa M, De Deken X, Detours V, Corvilain B, Maenhaut C, Miot F, Van Sande J, Many MC, Dumont JE. Roles of hydrogen peroxide in thyroid physiology and disease. J Clin Endocrinol Metab 2007; 92: 3764-3773.
32. De Deken X, Wang D, Dumont JE, Miot F. Characterization of TOX proteins as components of the thyroid H O-22 generating system. Exp Cell Res 2002; 273: 187-196.
33. 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.
34. Venturi S, Donati FM, Venturi A, Venturi M, Grossi L, Guidi A. Role of iodine in evolution and carcinogenesis of thyroid, breast and stomach. Adv Clin Path 2000; 4: 11-17.
35. Smyth PP. Role of iodine in antioxidant defence in thyroid and breast disease. Biofactors 2003; 19: 121-130.
36. Ohayon R, Boeynaems JM, Braekman JC, Van den Bergen H, Gorin Y, Virion A. Inhibition of thyroid NADPH-oxidase by 2-iodohexadecanal in a cell-free system. Mol Cell Endocrinol 1994; 99: 133-141.
37. Cardoso LC, Martins DC, Figueiredo MD, Rosenthal D, Vaisman M, Violante AH, Carvalho DP. Ca2+/ nicotinamide adenine dinucleotide phosphate-dependent H2O2 generation is inhibited by iodide in human thyroids. J Clin Endocrinol Metab 2001; 86: 4339-4343.
38. Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 2003; 17: 1195-1214. (Pubitemid 36775767)
39. Kupper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite TJ, Boneberg EM, Woitsch S, Weiller M, Abela R, Grolimund D, Potin P, Butler A, Luther GW 3rd, Kroneck PM, Meyer-Klaucke W, Feiters MC. Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad Sci USA 2008; 105: 6954-6958.
40. Fox MS, Klawansky S. Interruption of cell transformation and cancer formation. FASEB J 2006; 20: 2209-2213.
41. Wiseman SM, Loree TR, Rigual NR, Hicks WL Jr, Douglas WG, Anderson GR, Stoler DL. Anaplastic transformation of thyroid cancer: review of clinical, pathologic, and molecular evidence provides new insights into disease biology and future therapy. Head Neck 2003; 25: 662-670.
42. Wiseman SM, Grifth OL, Deen S, Rajput A, Masoudi H, Gilks B, Goldstein L, Gown A, Jones SJ. Identifcation of molecular markers altered during transformation of difer-entiated into anaplastic thyroid carcinoma. Arch Surg 2007; 142: 717-727; discussion 727-729.
43. Ozaki O, Ito K, Mimura T, Sugino K. Anaplastic transformation of papillary thyroid carcinoma in recurrent disease in regional lymph nodes: a histologic and immunohistochemi-cal study. J Surg Oncol 1999; 70: 45-48.
44. Wang HM, Huang YW, Huang JS, Wang CH, Kok VC, Hung CM, Chen HM, Tzen CY. Anaplastic carcinoma of the thyroid arising more often from follicular carcinoma than papillary carcinoma. Ann Surg Oncol 2007; 14: 3011-3018.
45. Mooradian AD, Allam CK, Khalil MF, Salti I, Salem PA. Anaplastic transformation of thyroid cancer: report of two cases and review of the literature. J Surg Oncol 1983; 23: 95-98.
46. Takeshita Y, Takamura T, Minato H, Misu H, Ando H, Yamashita T, Ikeda H, Nakanuma Y, Kaneko S. Transformation of p53-positive papillary thyroid carcinoma to anaplastic carcinoma of the liver following postoperative radioactive iodine-131 therapy. Intern Med 2008; 47: 1709-1712.
47. Rodrigues RF, Roque L, Rosa-Santos J, Cid O, Soares J. Chromosomal imbalances associated with anaplastic transformation of follicular thyroid carcinomas. Br J Cancer 2004; 90: 492-496.
48. Kilfoy BA, Zheng T, Holford TR, Han X, Ward MH, Sjodin A, Zhang Y, Bai Y, Zhu C, Guo GL, Rothman N. International patterns and trends in thyroid cancer incidence, 1973-2002. Cancer Causes Control 2009; 20: 525-531.
49. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 2006; 295: 2164-2167.
50. Liu S, Semenciw R, Ugnat AM, Mao Y. Increasing thyroid cancer incidence in Canada, 1970-1996: time trends and age-period-cohort efects. Br J Cancer 2001; 85: 1335-1339.
51. Colonna M, Guizard AV, Schvartz C, Velten M, Raverdy N, Molinie F, Delafosse P, Franc B, Grosclaude P. A time trend analysis of papillary and follicular cancers as a function of tumour size: a study of data from six cancer registries in France (1983-2000). Eur J Cancer 2007; 43: 891-900.
52. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 2006; 295: 2164-2167.
53. Grodski S, Brown T, Sidhu S, Gill A, Robinson B, Learoyd D, Sywak M, Reeve T, Delbridge L. Increasing incidence of thyroid cancer is due to increased pathologic detection. Surgery 2008; 144: 1038-1043.
54. Leenhardt L, Bernier MO, Boin-Pineau MH, Conte Devolx B, Marechaud R, Niccoli-Sire P, Nocaudie M, Orgiazzi J, Schlumberger M, Wemeau JL, Cherie-Challine L, De Vathaire F. Advances in diagnostic practices afect thyroid cancer incidence in France. Eur J Endocrinol 2004; 150: 133-139.
55. Hodgson NC, Button J, Solorzano CC. Tyroid cancer: is the incidence still increasing? Ann Surg Oncol 2004; 11: 1093-1097. (Pubitemid 40486656)
56. Guan H, Ji M, Bao R, Yu H, Wang Y, Hou P, Zhang Y, Shan Z, Teng W, Xing M. Association of high iodine intake with the T1799A BRAF mutation in papillary thyroid cancer. J Clin Endocrinol Metab 2009; 94: 1612-1617.
57. Harach HR, Ceballos GA. Tyroid cancer, thyroiditis and dietary iodine: a review based on the Salta, Argentina model. Endocr Pathol 2008; 19: 209-220.
58. Lind P, Langsteger W, Molnar M, Gallowitsch HJ, Mikosch P, Gomez I. Epidemiology of thyroid diseases in iodine suf-ciency. Tyroid 1998; 8: 1179-1183.
59. Pettersson B, Coleman MP, Ron E, Adami HO. Iodine supplementation in Sweden and regional trends in thyroid cancer incidence by histopathologic type. Int J Cancer 1996; 65: 13-19.
60. Sehestedt T, Knudsen N, Perrild H, Johansen C. Iodine intake and incidence of thyroid cancer in Denmark. Clin Endocrinol (Oxf) 2006; 65: 229-233.
61. Delange F, Lecomte P. Iodine supplementation: benefts outweigh risks. Drug Saf 2000; 22: 89-95.
62. Kapp DS, LiVolsi VA, Sanders MM. Anaplastic carcinoma following well-diferentiated thyroid cancer: etiological considerations. Yale J Biol Med 1982; 55: 521-528.
63. Smerdely P, Pitsiavas V, Boyages SC. Evidence that the inhibitory efects of iodide on thyroid cell proliferation are due to arrest of the cell cycle at G0G1 and G2M phases. Endocrinology 1993; 133: 2881-2888.
64. Tramontano D, Veneziani BM, Lombardi A, Villone G, Ingbar SH. Iodine inhibits the proliferation of rat thyroid cells in culture. Endocrinology 1989; 125: 984-992.
65. Eskin BA, Shuman R, Krouse T, Merion JA. Rat mammary gland atypia produced by iodine blockade with perchlorate. Cancer Res 1975; 35: 2332-2339.
66. Unger J, Lambert M, Jonckheer MH, Denayer P. Amiodarone and the thyroid: pharmacological, toxic and therapeutic efects. J Intern Med 1993; 233: 435-443.
67. Martino E, Bartalena L, Bogazzi F, Braverman LE. Te efects of amiodarone on the thyroid. Endocr Rev 2001; 22: 240-254.
68. Mahmoud I, Colin I, Many MC, Denef JF. Direct toxic efect of iodide in excess on iodine-defcient thyroid glands: epithelial necrosis and infammation associated with lipofuscin accumulation. Exp Mol Pathol 1986; 44: 259-271.
69. Filetti S, Rapoport B. Evidence that organic iodine attenuates the adenosine 3′,5′-monophosphate response to thyro-tropin stimulation in thyroid tissue by an action at or near the adenylate cyclase catalytic unit. Endocrinology 1983; 113: 1608-1615.
70. Yuasa R, Eggo MC, Meinkoth J, Dillmann WH, Burrow GN. Iodide induces transforming growth factor beta 1 (TGF-beta 1) mRNA in sheep thyroid cells. Tyroid 1992; 2: 141-145.
71. Pang XP, Park M, Hershman JM. Transforming growth factor-beta blocks protein kinase-A-mediated iodide transport and protein kinase-C-mediated DNA synthesis in FRTL-5 rat thyroid cells. Endocrinology 1992; 131: 45-50.
72. Bidey SP. Control of thyroid cell and follicle growth. Recent advances and current controversies. Trends Endocrinol Metab 1990; 1: 174-178.
73. Golstein J, Dumont JE. Cytotoxic efects of iodide on thyroid cells: diference between rat thyroid FRTL-5 cell and primary dog thyrocyte responsiveness. J Endocrinol Invest 1996; 19: 119-126.
74. Huang M, Batra RK, Kogai T, Lin YQ, Hershman JM, Lichtenstein A, Sharma S, Zhu LX, Brent GA, Dubinett SM. Ectopic expression of the thyroperoxidase gene augments radioiodide uptake and retention mediated by the sodium iodide symporter in non-small cell lung cancer. Cancer Gene Ter 2001; 8: 612-618.
75. Zhang L, Sharma S, Zhu LX, Kogai T, Hershman JM, Brent GA, Dubinett SM, Huang M. Nonradioactive iodide efectively induces apoptosis in genetically modifed lung cancer cells. Cancer Res 2003; 63: 5065-5072.
76. Garcia-Solis P, Alfaro Y, Anguiano B, Delgado G, Guzman RC, Nandi S, Diaz-Munoz M, Vazquez-Martinez O, Aceves C. Inhibition of N-methyl-N- nitrosourea-induced mammary carcinogenesis by molecular iodine (I2) but not by iodide (I-) treatment. Evidence that I2 prevents cancer promotion. Mol Cell Endocrinol 2005; 236: 49-57.
77. Shrivastava A, Tiwari M, Sinha RA, Kumar A, Balapure AK, Bajpai VK, Sharma R, Mitra K, Tandon A, Godbole MM. Molecular iodine induces caspase-independent apop-tosis in human breast carcinoma cells involving the mitochondria-mediated pathway. J Biol Chem 2006; 281: 19762-19771.
78. Langer R, Burzler C, Bechtner G, Gartner R. Infuence of iodide and iodolactones on thyroid apoptosis. Evidence that apoptosis induced by iodide is mediated by iodolactones in intact porcine thyroid follicles. Exp Clin Endocrinol Diabetes 2003; 111: 325-329.
79. Upadhyay G, Singh R, Sharma R, Balapure AK, Godbole MM. Diferential action of iodine on mitochondria from human tumoral-and extra-tumoral tissue in inducing the release of apoptogenic proteins. Mitochondrion 2002; 2: 199-210.
80. Xing M. BRAF mutation in thyroid cancer. Endocr Relat Cancer 2005; 12: 245-262.
81. Henderson YC, Shellenberger TD, Williams MD, El-Naggar AK, Fredrick MJ, Cieply KM, Clayman GL. High rate of BRAF and RET/PTC dual mutations associated with recurrent papillary thyroid carcinoma. Clin Cancer Res 2009; 15: 485-491.
82. Nikiforova MN, Kimura ET, Gandhi M, Biddinger PW, Knauf JA, Basolo F, Zhu Z, Giannini R, Salvatore G, Fusco A, Santoro M, Fagin JA, Nikiforov YE. BRAF mutations in thyroid tumors are restricted to papillary carcinomas and ana-plastic or poorly diferentiated carcinomas arising from papillary carcinomas. J Clin Endocrinol Metab 2003; 88: 5399-5404.
83. Takano T, Ito Y, Hirokawa M, Yoshida H, Miyauchi A. BRAF V600E mutation in anaplastic thyroid carcinomas and their accompanying diferentiated carcinomas. Br J Cancer 2007; 96: 1549-1553.
84. Takahashi K, Eguchi H, Arihiro K, Ito R, Koyama K, Soda M, Cologne J, Hayashi Y, Nakata Y, Nakachi K, Hamatani K. Te presence of BRAF point mutation in adult papillary thyroid carcinomas from atomic bomb survivors correlates with radiation dose. Mol Carcinog 2007; 46: 242-248.
85. Oler G, Cerutti JM. High prevalence of BRAF mutation in a Brazilian cohort of patients with sporadic papillary thyroid carcinomas: correlation with more aggressive phenotype and decreased expression of iodide-metabolizing genes. Cancer 2009; 115: 972-980.
86. Romei C, Ciampi R, Faviana P, Agate L, Molinaro E, Bottici V, Basolo F, Miccoli P, Pacini F, Pinchera A, Elisei R. BRAFV600E mutation, but not RET/PTC rearrangements, is correlated with a lower expression of both thyroperoxidase and sodium iodide symporter genes in papillary thyroid cancer. Endocr Relat Cancer 2008; 15: 511-520.
87. Durante C, Puxeddu E, Ferretti E, Morisi R, Moretti S, Bruno R, Barbi F, Avenia N, Scipioni A, Verrienti A, Tosi E, Cavaliere A, Gulino A, Filetti S, Russo D. BRAF mutations in papillary thyroid carcinomas inhibit genes involved in iodine metabolism. J Clin Endocrinol Metab 2007; 92: 2840-2843.
88. Espadinha C, Santos JR, Sobrinho LG, Bugalho MJ. Expression of iodine metabolism genes in human thyroid tissues: evidence for age and BRAF(V600E) mutation dependency. Clin Endocrinol (Oxf) 2009; 70: 629-635.
89. Knauf JA, Ma X, Smith EP, Zhang L, Mitsutake N, Liao XH, Refetof S, Nikiforov YE, Fagin JA. Targeted expression of BRAFV600E in thyroid cells of transgenic mice results in papillary thyroid cancers that undergo dediferentiation. Cancer Res 2005; 65: 4238-4245.
90. Henderson YC, Fredrick MJ, Clayman GL. Diferential responses of human papillary thyroid cancer cell lines carrying the RET/PTC1 rearrangement or a BRAF mutation to MEK1/2 inhibitors. Arch Otolaryngol Head Neck Surg 2007; 133: 810-815.
91. Leboeuf R, Baumgartner JE, Benezra M, Malaguarnera R, Solit D, Pratilas CA, Rosen N, Knauf JA, Fagin JA. BRAFV600E mutation is associated with preferential sensitivity to mitogen-ac-tivated protein kinase kinase inhibition in thyroid cancer cell lines. J Clin Endocrinol Metab 2008; 93: 2194-2201.
92. Liu Z, Hou P, Ji M, Guan H, Studeman K, Jensen K, Vasko V, El-Naggar AK, Xing M. Highly prevalent genetic alterations in receptor tyrosine kinases and phosphatidylinositol 3-kinase/akt and mitogen-activated protein kinase pathways in anaplastic and follicular thyroid cancers. J Clin Endocrinol Metab 2008; 93: 3106-3116.
93. Namba H, Saenko V, Yamashita S. Nuclear factor-kB in thyroid carcinogenesis and progression: a novel therapeutic target for advanced thyroid cancer. Arq Bras Endocrinol Metabol 2007; 51: 843-851.
94. Mitsiades CS, Negri J, McMullan C, McMillin DW, Sozopoulos E, Fanourakis G, Voutsinas G, Tseleni-Balafouta S, Poulaki V, Batt D, Mitsiades N. Targeting BRAFV600E in thyroid carcinoma: therapeutic implications. Mol Cancer Ter 2007; 6: 1070-1078.
95. Mian C, Barollo S, Pennelli G, Pavan N, Rugge M, Pelizzo MR, Mazzarotto R, Casara D, Nacamulli D, Mantero F, Opocher G, Busnardo B, Girelli ME. Molecular characteristics in papillary thyroid cancers (PTCs) with no 131I uptake. Clin Endocrinol (Oxf) 2008; 68: 108-116.
96. Durand S, Ferraro-Peyret C, Joufre M, Chave A, Borson-Chazot F, Selmi-Ruby S, Rousset B. Molecular characteristics of papillary thyroid carcinomas without BRAF mutation or RET/PTC rearrangement. Relationship with clinicopathological features. Endocr Relat Cancer 2009; 16: 467-481.
97. Kondo T, Ezzat S, Asa SL. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 2006; 6: 292-306.
98. Hamatani K, Eguchi H, Ito R, Mukai M, Takahashi K, Taga M, Imai K, Cologne J, Soda M, Arihiro K, Fujihara M, Abe K, Hayashi T, Nakashima M, Sekine I, Yasui W, Hayashi Y, Nakachi K. RET/PTC rearrangements preferentially occurred in papillary thyroid cancer among atomic bomb survivors exposed to high radiation dose. Cancer Res 2008; 68: 7176-7182.
99. Nakashima M, Takamura N, Namba H, Saenko V, Meirmanov S, Matsumoto N, Hayashi T, Maeda S, Sekine I. RET oncogene amplifcation in thyroid cancer: correlations with radiation-associated and high-grade malignancy. Hum Pathol 2007; 38: 621-628.
100. Rabes HM, Demidchik EP, Sidorow JD, Lengfelder E, Beimfohr C, Hoelzel D, Klugbauer S. Pattern of radiation-induced RET and NTRK1 rearrangements in 191 post-Chernobyl papillary thyroid carcinomas: biological, phenotypic, and clinical implications. Clin Cancer Res 2000; 6: 1093-1103.
101. Gujral TS, van Veelen W, Richardson DS, Myers SM, Meens JA, Acton DS, Dunach M, Elliott BE, Hoppener JW, Mulligan LM. A novel RET kinase-beta-catenin signaling pathway contributes to tumorigenesis in thyroid carcinoma. Cancer Res 2008; 68: 1338-1346.
102. Kim DW, Chung HK, Park KC, Hwang JH, Jo YS, Chung J, Kalvakolanu DV, Resta N, Shong M. Tumor suppressor LKB1 inhibits activation of signal transducer and activator of transcription 3 (STAT3) by thyroid oncogenic tyrosine kinase rearranged in transformation (RET)/papillary thyroid carcinoma (PTC). Mol Endocrinol 2007; 21: 3039-3049.
103. Kim YR, Byun HS, Won M, Park KA, Kim JM, Choi BL, Lee H, Hong JH, Park J, Seok JH, Kim DW, Shong M, Park SK, Hur GM. Modulatory role of phospholipase D in the activation of signal transducer and activator of transcription (STAT)-3 by thyroid oncogenic kinase RET/PTC. BMC Cancer 2008; 8: 144-154.
104. Suchy B, Waldmann V, Klugbauer S, Rabes HM. Absence of RAS and p53 mutations in thyroid carcinomas of children after Chernobyl in contrast to adult thyroid tumours. Br J Cancer 1998; 77: 952-955.
105. Shi YF, Zou MJ, Schmidt H, Juhasz F, Stensky V, Robb D, Farid NR. High rates of ras codon 61 mutation in thyroid tumors in an iodide-defcient area. Cancer Res 1991; 51: 2690-2693.
106. Garcia-Silva S, Aranda A. Te thyroid hormone receptor is a suppressor of ras-mediated transcription, proliferation, and transformation. Mol Cell Biol 2004; 24: 7514-7523.
107. Vitagliano D, Portella G, Troncone G, Francione A, Rossi C, Bruno A, Giorgini A, Coluzzi S, Nappi TC, Rothstein JL, Pasquinelli R, Chiappetta G, Terracciano D, Macchia V, Melillo RM, Fusco A, Santoro M. Tyroid targeting of the N-ras(Gln61Lys) oncogene in transgenic mice results in follicular tumors that progress to poorly diferentiated carcinomas. Oncogene 2006; 25: 5467-5474.
108. Melillo RM, Castellone MD, Guarino V, De Falco V, Cirafci AM, Salvatore G, Caiazzo F, Basolo F, Giannini R, Kruhofer M, Orntoft T, Fusco A, Santoro M. Te RET/PTC-RAS-BRAF linear signaling cascade mediates the motile and mitogenic phenotype of thyroid cancer cells. J Clin Invest 2005; 115: 1068-1081.
109. Cass LA, Meinkoth JL. Ras signaling through PI3K confers hormone-independent proliferation that is compatible with diferentiation. Oncogene 2000; 19: 924-932.
110. Liu D, Liu Z, Jiang D, Dackiw AP, Xing M. Inhibitory efects of the mitogen-activated protein kinase kinase inhibitor CI-1040 on the proliferation and tumor growth of thyroid. cancer cells with BRAF or RAS mutations. J Clin Endocrinol Metab 2007; 92: 4686-4695.
111. Hou P, Liu D, Shan Y, Hu S, Studeman K, Condouris S, Wang Y, Trink A, El-Naggar AK, Tallini G, Vasko V, Xing M. Genetic alterations and their relationship in the phosphati-dylinositol 3-kinase/Akt pathway in thyroid cancer. Clin Cancer Res 2007; 13: 1161-1170.
112. Garcia-Rostan G, Zhao H, Camp RL, Pollan M, Herrero A, Pardo J, Wu R, Carcangiu ML, Costa J, Tallini G. ras mutations are associated with aggressive tumor phenotypes and poor prognosis in thyroid cancer. J Clin Oncol 2003; 21: 3226-3235.
113. Brzezianska E, Karbownik M, Migdalska-Sek M, Pastuszak-Lewandoska D, Wloch J, Lewinski A. Molecular analysis of the RET and NTRK1 gene rearrangements in papillary thyroid carcinoma in the Polish population. Mutat Res 2006; 599: 26-35.
114. Brzezianska E, Pastuszak-Lewandoska D, Lewinski A. Rearrangements of NTRK1 oncogene in papillary thyroid carcinoma. Neuro Endocrinol Lett 2007; 28: 221-229.
115. Frattini M, Ferrario C, Bressan P, Balestra D, De Cecco L, Mondellini P, Bongarzone I, Collini P, Gariboldi M, Pilotti S, Pierotti MA, Greco A. Alternative mutations of BRAF, RET and NTRK1 are associated with similar but distinct gene expression patterns in papillary thyroid cancer. Oncogene 2004; 23: 7436-7440.
116. Beimfohr C, Klugbauer S, Demidchik EP, Lengfelder E, Rabes HM. NTRK1 re-arrangement in papillary thyroid carcinomas of children after the Chernobyl reactor accident. Int J Cancer 1999; 80: 842-847.
117. Musholt TJ, Brehm C, Hanack J, von Wasielewski R, Musholt PB. Identifcation of diferentially expressed genes in papillary thyroid carcinomas with and without rearrangements of the tyrosine kinase receptors RET and/or NTRK1. J Surg Res 2006; 131: 15-25.
118. Musholt TJ, Musholt PB, Khaladj N, Schulz D, Scheumann GF, Klempnauer J. Prognostic signifcance of RET and NTRK1 rearrangements in sporadic papillary thyroid carcinoma. Surgery 2000; 128: 984-993.
119. Barzon L, Gnatta E, Castagliuolo I, Trevisan M, Moretti F, Pontecorvi A, Boscaro M, Palu G. Modulation of retrovirally driven therapeutic genes by mutant TP53 in anaplastic thyroid carcinoma. Cancer Gene Ter 2005; 12: 381-388.
120. Ito Y, Motoo Y, Yoshida H, Iovanna JL, Nakamura Y, Kuma K, Miyauchi A. High level of tumour protein p53-induced nuclear protein 1 (TP53INP1) expression in anaplastic carcinoma of the thyroid. Pathology 2006; 38: 545-547. (Pubitemid 47215679)
121. Moretti F, Farsetti A, Soddu S, Misiti S, Crescenzi M, Filetti S, Andreoli M, Sacchi A, Pontecorvi A. p53 re-expression inhibits proliferation and restores diferentiation of human thyroid anaplastic carcinoma cells. Oncogene 1997; 14: 729-740.
122. Whibley C, Pharoah PD, Hollstein M. p53 polymorphisms: cancer implications. Nat Rev Cancer 2009; 9: 95-107.
123. Bachmann K, Pawliska D, Kaif J, Schurr P, Zorb J, Mann O, Kahl HJ, Izbicki JR, Strate T. P53 is an independent prognostic factor for survival in thyroid cancer. Anticancer Res 2007; 27: 3993-3997.
124. Nikiforov YE. Tyroid carcinoma: molecular pathways and therapeutic targets. Mod Pathol 2008; 21(Suppl 2): S37-S43.
125. Tepmongkol S, Keelawat S, Honsawek S, Ruangvejvorachai P. Rosiglitazone efect on radioiodine uptake in thyroid carcinoma patients with high thyroglobulin but negative total body scan: a correlation with the expression of peroxisome proliferator-activated receptor-gamma. Tyroid 2008; 18: 697-704.
126. Espadinha C, Cavaco BM, Leite V. PAX8PPARgamma stimulates cell viability and modulates expression of thyroid-specifc genes in a human thyroid cell line. Tyroid 2007; 17: 497-509.
127. Lui WO, Foukakis T, Liden J, Toppe SR, Dwight T, Hoog A, Zedenius J, Wallin G, Reimers M, Larsson C. Expression pro-fling reveals a distinct transcription signature in follicular thyroid carcinomas with a PAX8-PPARγ fusion oncogene. Oncogene 2005; 24: 1467-1476.
128. Kato Y, Ying H, Zhao L, Furuya F, Araki O, Willingham MC, Cheng SY. PPARgamma insufficiency promotes follicu-lar thyroid carcinogenesis via activation of the nuclear factor-kappaB signaling pathway. Oncogene 2006; 25: 2736-2747.
129. Sahin M, Allard BL, Yates M, Powell JG, Wang XL, Hay ID, Zhao Y, Goellner JR, Sebo TJ, Grebe SK, Eberhardt NL, McIver B. PPARgamma staining as a surrogate for PAX8/PPARgamma fusion oncogene expression in follicular neoplasms: clinico-pathological correlation and histopathological diagnostic value. J Clin Endocrinol Metab 2005; 90: 463-468.
130. Guigon CJ, Zhao L, Lu C, Willingham MC, Cheng SY. Regulation of beta-catenin by a novel nongenomic action of thyroid hormone beta receptor. Mol Cell Biol 2008; 28: 4598-4608.
131. Kim WB, Lewis CJ, McCall KD, Malgor R, Kohn AD, Moon RT, Kohn LD. Overexpression of Wnt-1 in thyrocytes enhances cellular growth but suppresses transcription of the thy-roperoxidase gene via diferent signaling mechanisms. J Endocrinol 2007; 193: 93-106.
132. Kitamura Y, Shimizu K, Tanaka S, Ito K, Emi M. Allelotyping of anaplastic thyroid carcinoma: frequent allelic losses on 1q, 9p, 11, 17, 19p, and 22q. Genes Chromosomes Cancer 2000; 27: 244-251.
133. Abbosh PH, Nephew KP. Multiple signaling pathways converge on beta-catenin in thyroid cancer. Tyroid 2005; 15: 551-561.
134. Abbosh PH, Li X, Li L, Gardner TA, Kao C, Nephew KP. A conditionally replicative, Wnt/beta-catenin pathway-based adenovirus therapy for anaplastic thyroid cancer. Cancer Gene Ter 2007; 14: 399-408.
135. Garcia-Rostan G, Camp RL, Herrero A, Carcangiu ML, Rimm DL, Tallini G. Beta-catenin dysregulation in thyroid neoplasms: down-regulation, aberrant nuclear expression, and CTNNB1 exon 3 mutations are markers for aggressive tumor phenotypes and poor prognosis. Am J Pathol 2001; 158: 987-996.
136. Riesco-Eizaguirre G, Santisteban P. A perspective view of sodium iodide symporter research and its clinical implications. Eur J Endocrinol 2006; 155: 495-512.
137. Dadachova E, Carrasco N. Te Na/I symporter (NIS): imaging and therapeutic applications. Semin Nucl Med 2004; 34: 23-31.
138. Dai G, Levy O, Carrasco N. Cloning and characterization of the thyroid iodide transporter. Nature 1996; 379: 458-460.
139. Smanik PA, Ryu KY, Teil KS, Mazzaferri EL, Jhiang SM. Expression, exon-intron organization, and chromosome mapping of the human sodium iodide symporter. Endocrinology 1997; 138: 3555-3558.
140. Scott DA, Wang R, Kreman TM, Shefeld VC, Karniski LP. Te Pendred syndrome gene encodes a chloride-iodide transport protein. Nat Genet 1999; 21: 440-443.
141. Rodriguez AM, Perron B, Lacroix L, Caillou B, Leblanc G, Schlumberger M, Bidart JM, Pourcher T. Identifcation and characterization of a putative human iodide transporter located at the apical membrane of thyrocytes. J Clin Endocrinol Metab 2002; 87: 3500-3503.
142. Sarlis NJ. Metastatic thyroid cancer unresponsive to conventional therapies: novel management approaches through translational clinical research. Curr Drug Targets Immune Endocr Metabol Disord 2001; 1: 103-115.
143. Giufrida D, Gharib H. Anaplastic thyroid carcinoma: current diagnosis and treatment. Ann Oncol 2000; 11: 1083-1089.
144. Trapasso F, Iuliano R, Chiefari E, Arturi F, Stella A, Filetti S, Fusco A, Russo D. Iodide symporter gene expression in normal and transformed rat thyroid cells. Eur J Endocrinol 1999; 140: 447-451.
145. Ward LS, Santarosa PL, Granja F, da Assumpcao LV, Savoldi M, Goldman GH. Low expression of sodium iodide symporter identifes aggressive thyroid tumors. Cancer Lett 2003; 200: 85-91.
146. Are C, Shaha AR. Anaplastic thyroid carcinoma: biology, pathogenesis, prognostic factors, and treatment approaches. Ann Surg Oncol 2006; 13: 453-464.
147. Baker CH, Morris JC. Te sodium-iodide symporter. Curr Drug Targets Immune Endocr Metabol Disord 2004; 4: 167-174.
148. Riedel C, Dohan O, De la Vieja A, Ginter CS, Carrasco N. Journey of the iodide transporter NIS: from its molecular identifcation to its clinical role in cancer. Trends Biochem Sci 2001; 26: 490-496.
149. Lazar V, Bidart JM, Caillou B, Mahe C, Lacroix L, Filetti S, Schlumberger M. Expression of the Na+/I-symporter gene in human thyroid tumors: a comparison study with other thyroid-specifc genes. J Clin Endocrinol Metab 1999; 84: 3228-3234.
150. Park HJ, Kim JY, Park KY, Gong G, Hong SJ, Ahn IM. Expressions of human sodium iodide symporter mRNA in primary and metastatic papillary thyroid carcinomas. Tyroid 2000; 10: 211-217.
151. Arturi F, Russo D, Schlumberger M, du Villard JA, Caillou B, Vigneri P, Wicker R, Chiefari E, Suarez HG, Filetti S. Iodide symporter gene expression in human thyroid tumors. J Clin Endocrinol Metab 1998; 83: 2493-2496.
152. Mishra A, Pal L, Mishra SK. Distribution of Na+/I-sym-porter in thyroid cancers in an iodine-defcient population: an immunohistochemical study. World J Surg 2007; 31: 1737-1742.
153. Wapnir IL, van de Rijn M, Nowels K, Amenta PS, Walton K, Montgomery K, Greco RS, Dohan O, Carrasco N. Immunohistochemical profle of the sodium/iodide sym-porter in thyroid, breast, and other carcinomas using high density tissue microarrays and conventional sections. J Clin Endocrinol Metab 2003; 88: 1880-1888.
154. Saito T, Endo T, Kawaguchi A, Ikeda M, Katoh R, Kawaoi A, Muramatsu A, Onaya T. Increased expression of the sodium/ iodide symporter in papillary thyroid carcinomas. J Clin Invest 1998; 101: 1296-1300.
155. Peyrottes I, Navarro V, Ondo-Mendez A, Marcellin D, Bellanger L, Marsault R, Lindenthal S, Ettore F, Darcourt J, Pourcher T. Immunoanalysis indicates that the sodium iodide symporter is not overexpressed in intracellular compartments in thyroid and breast cancers. Eur J Endocrinol 2009; 160: 215-225.
156. Kogai T, Curcio F, Hyman S, Cornford EM, Brent GA, Hershman JM. Induction of follicle formation in long-term cultured normal human thyroid cells treated with thyrotro-pin stimulates iodide uptake but not sodium/iodide sym-porter messenger RNA and protein expression. J Endocrinol 2000; 167: 125-135.
157. Fujiwara H, Tatsumi K, Miki K, Harada T, Miyai K, Takai S, Amino N. Congenital hypothyroidism caused by a mutation in the Na+/I-symporter. Nat Genet 1997; 16: 124-125.
158. Fujiwara H, Tatsumi K, Miki K, Harada T, Okada S, Nose O, Kodama S, Amino N. Recurrent T354P mutation of the Na+/I-symporter in patients with iodide transport defect. J Clin Endocrinol Metab 1998; 83: 2940-2943.
159. Kosugi S, Bhayana S, Dean HJ. A novel mutation in the sodium/iodide symporter gene in the largest family with iodide transport defect. J Clin Endocrinol Metab 1999; 84: 3248-3253.
160. Kosugi S, Okamoto H, Tamada A, Sanchez-Franco F. A novel peculiar mutation in the sodium/iodide symporter gene in Spanish siblings with iodide transport defect. J Clin Endocrinol Metab 2002; 87: 3830-3836.
161. Kosugi S, Sato Y, Matsuda A, Ohyama Y, Fujieda K, Inomata H, Kameya T, Isozaki O, Jhiang SM. High prevalence of T354P sodium/iodide symporter gene mutation in Japanese patients with iodide transport defect who have heterogeneous clinical pictures. J Clin Endocrinol Metab 1998; 83: 4123-4129.
162. Matsuda A, Kosugi S. A homozygous missense mutation of the sodium/iodide symporter gene causing iodide transport defect. J Clin Endocrinol Metab 1997; 82: 3966-3971.
163. Pohlenz J, Medeiros-Neto G, Gross JL, Silveiro SP, Knobel M, Refetof S. Hypothyroidism in a Brazilian kindred due to iodide trapping defect caused by a homozygous mutation in the sodium/iodide symporter gene. Biochem Biophys Res Commun 1997; 240: 488-491.
164. De La Vieja A, Ginter CS, Carrasco N. Te Q267E mutation in the sodium/iodide symporter (NIS) causes congenital iodide transport defect (ITD) by decreasing the NIS turnover number. J Cell Sci 2004; 117: 677-687.
165. Szinnai G, Kosugi S, Derrien C, Lucidarme N, David V, Czernichow P, Polak M. Extending the clinical heterogeneity of iodide transport defect (ITD): a novel mutation R124H of the sodium/iodide symporter gene and review of genotype-phenotype correlations in ITD. J Clin Endocrinol Metab 2006; 91: 1199-1204.
166. Russo D, Manole D, Arturi F, Suarez HG, Schlumberger M, Filetti S, Derwahl M. Absence of sodium/iodide symporter gene mutations in diferentiated human thyroid carcinomas. Tyroid 2001; 11: 37-39.
167. Sodre AK, Rubio IG, Galrao AL, Knobel M, Tomimori EK, Alves VA, Kanamura CT, Buchpiguel CA, Watanabe T, Friguglietti CU, Kulcsar MA, Medeiros-Neto G, Camargo RY. Association of low sodium-iodide symporter messenger ribonucleic acid expression in malignant thyroid nodules with increased intracellular protein staining. J Clin Endocrinol Metab 2008; 93: 4141-4145.
168. Dohan O, Baloch Z, Banrevi Z, Livolsi V, Carrasco N. Predominant intracellular overexpression of the Na+/I-sym-porter (NIS) in a large sampling of thyroid cancer cases. J Clin Endocrinol Metab 2001; 86: 2697-2700.
169. Kogai T, Taki K, Brent GA. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer 2006; 13: 797-826.
170. Arturi F, Presta I, Scarpelli D, Bidart JM, Schlumberger M, Filetti S, Russo D. Stimulation of iodide uptake by human chorionic gonadotropin in FRTL-5 cells: efects on sodium/ iodide symporter gene and protein expression. Eur J Endocrinol 2002; 147: 655-661.
171. van Hoek I, Daminet S, Vandermeulen E, Dobbeleir A, Duchateau L, Peremans K. Recombinant human thyrotro-pin administration enhances thyroid uptake of radioactive iodine in hyperthyroid cats. J Vet Intern Med 2008; 22: 1340-1344.
172. Coelho SM, Vaisman M, Carvalho DP. Tumour re-diferentiation efect of retinoic acid: a novel therapeutic approach for advanced thyroid cancer. Curr Pharm Des 2005; 11: 2525-2531.
173. Kurebayashi J, Tanaka K, Otsuki T, Moriya T, Kunisue H, Uno M, Sonoo H. All-trans-retinoic acid modulates expression levels of thyroglobulin and cytokines in a new human poorly diferentiated papillary thyroid carcinoma cell line, KTC-1. J Clin Endocrinol Metab 2000; 85: 2889-2896.
174. Schumm-Draeger PM. Sodium/iodide symporter (NIS) and cytokines. Exp Clin Endocrinol Diabetes 2001; 109: 32-34.
175. Kawaguchi A, Ikeda M, Endo T, Kogai T, Miyazaki A, Onaya T. Transforming growth factor-beta1 suppresses thyrotropin-induced Na+/I-symporter messenger RNA and protein levels in FRTL-5 rat thyroid cells. Tyroid 1997; 7: 789-794.
176. Spitzweg C, Joba W, Morris JC, Heufelder AE. Regulation of sodium iodide symporter gene expression in FRTL-5 rat thyroid cells. Tyroid 1999; 9: 821-830.
177. Fortunati N, Catalano MG, Arena K, Brignardello E, Piovesan A, Boccuzzi G. Valproic acid induces the expression of the Na+/I-symporter and iodine uptake in poorly diferentiated thyroid cancer cells. J Clin Endocrinol Metab 2004; 89: 1006-1009.
178. Catalano MG, Fortunati N, Pugliese M, Costantino L, Poli R, Bosco O, Boccuzzi G. Valproic acid induces apoptosis and cell cycle arrest in poorly diferentiated thyroid cancer cells. J Clin Endocrinol Metab 2005; 90: 1383-1389.
179. Kitazono M, Robey R, Zhan Z, Sarlis NJ, Skarulis MC, Aikou T, Bates S, Fojo T. Low concentrations of the histone deacety-lase inhibitor, depsipeptide (FR901228), increase expression of the Na+/I-symporter and iodine accumulation in poorly diferentiated thyroid carcinoma cells. J Clin Endocrinol Metab 2001; 86: 3430-3435.
180. Akagi T, Luong QT, Gui D, Said J, Selektar J, Yung A, Bunce CM, Braunstein GD, Koefer HP. Induction of sodium iodide symporter gene and molecular characterisation of HNF3 beta/FoxA2, TTF-1 and C/EBP beta in thyroid carcinoma cells. Br J Cancer 2008; 99: 781-788.
181. Vassart G, Dumont JE. Te thyrotropin receptor and the regulation of thyrocyte function and growth. Endocr Rev 1992; 13: 596-611.
182. Levy O, Dai G, Riedel C, Ginter CS, Paul EM, Lebowitz AN, Carrasco N. Characterization of the thyroid Na+/I-symporter with an anti-COOH terminus antibody. Proc Natl Acad Sci USA 1997; 94: 5568-5573.
183. Kogai T, Endo T, Saito T, Miyazaki A, Kawaguchi A, Onaya T. Regulation by thyroid-stimulating hormone of sodium/ iodide symporter gene expression and protein levels in FRTL-5 cells. Endocrinology 1997; 138: 2227-2232.
184. Weiss SJ, Philp NJ, Ambesi-Impiombato FS, Grollman EF. Tyrotropin-stimulated iodide transport mediated by ade-nosine 3′,5′-monophosphate and dependent on protein synthesis. Endocrinology 1984; 114: 1099-1107.
185. Ohno M, Zannini M, Levy O, Carrasco N, di Lauro R. Te paired-domain transcription factor Pax8 binds to the upstream enhancer of the rat sodium/iodide symporter gene and participates in both thyroid-specifc and cyclic-AMP-dependent transcription. Mol Cell Biol 1999; 19: 2051-2060.
186. Riedel C, Levy O, Carrasco N. Post-transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem 2001; 276: 21458-21463.
187. Chun JT, Di Dato V, D'Andrea B, Zannini M, Di Lauro R. Te CRE-like element inside the 5′-upstream region of the rat sodium/iodide symporter gene interacts with diverse classes of b-Zip molecules that regulate transcriptional activities through strong synergy with Pax-8. Mol Endocrinol 2004; 18: 2817-2829.
188. Endo T, Kaneshige M, Nakazato M, Ohmori M, Harii N, Onaya T. Tyroid transcription factor-1 activates the promoter activity of rat thyroid Na+/I-symporter gene. Mol Endocrinol 1997; 11: 1747-1755.
189. Taki K, Kogai T, Kanamoto Y, Hershman JM, Brent GA. A thyroid-specifc far-upstream enhancer in the human sodium/iodide symporter gene requires Pax-8 binding and cyclic adenosine 3′,5′-monophosphate response elementlike sequence binding proteins for full activity and is differentially regulated in normal and thyroid cancer cells. Mol Endocrinol 2002; 16: 2266-2282.
190. Presta I, Arturi F, Ferretti E, Mattei T, Scarpelli D, Tosi E, Scipioni A, Celano M, Gulino A, Filetti S, Russo D. Recovery of NIS expression in thyroid cancer cells by overexpression of Pax8 gene. BMC Cancer 2005; 5: 80-89.
191. Furuya F, Shimura H, Miyazaki A, Taki K, Ohta K, Haraguchi K, Onaya T, Endo T, Kobayashi T. Adenovirus-mediated transfer of thyroid transcription factor-1 induces radioiodide organifcation and retention in thyroid cancer cells. Endocrinology 2004; 145: 5397-5405.
192. Bruno R, Ferretti E, Tosi E, Arturi F, Giannasio P, Mattei T, Scipioni A, Presta I, Morisi R, Gulino A, Filetti S, Russo D. Modulation of thyroid-specifc gene expression in normal and nodular human thyroid tissues from adults: an in vivo efect of thyrotropin. J Clin Endocrinol Metab 2005; 90: 5692-5697.
193. Kogai T, Sajid-Crockett S, Newmarch LS, Liu YY, Brent GA. Phosphoinositide-3-kinase inhibition induces sodium/ iodide symporter expression in rat thyroid cells and human papillary thyroid cancer cells. J Endocrinol 2008; 199: 243-252.
194. Chang F, Lee JT, Navolanic PM, Steelman LS, Shelton JG, Blalock WL, Franklin RA, McCubrey JA. Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: a target for cancer chemotherapy. Leukemia 2003; 17: 590-603.
195. Rivas M, Santisteban P. TSH-activated signaling pathways in thyroid tumorigenesis. Mol Cell Endocrinol 2003; 213: 31-45.
196. Paes JE, Ringel MD. Dysregulation of the phosphatidyli-nositol 3-kinase pathway in thyroid neoplasia. Endocrinol Metab Clin North Am 2008; 37: 375-387.
197. Hofmann S, Maschuw K, Hassan I, Wunderlich A, Lingelbach S, Ramaswamy A, Hofbauer LC, Zielke A. Functional thyrotropin receptor attenuates malignant phe-notype of follicular thyroid cancer cells. Endocrine 2006; 30: 129-138.
198. Milas M, Mazzaglia P, Chia SY, Skugor M, Berber E, Reddy S, Gupta M, Siperstein A. Te utility of peripheral thyrotropin mRNA in the diagnosis of follicular neoplasms and surveillance of thyroid cancers. Surgery 2007; 141: 137-146; discussion 146.
199. Matsumoto H, Sakamoto A, Fujiwara M, Yano Y, Shishido-Hara Y, Fujioka Y, Kamma H. Decreased expression of the thyroid-stimulating hormone receptor in poorly-diferentiated carcinoma of the thyroid. Oncol Rep 2008; 19: 1405-1411.
200. Xing M, Usadel H, Cohen Y, Tokumaru Y, Guo Z, Westra WB, Tong BC, Tallini G, Udelsman R, Califano JA, Ladenson PW, Sidransky D. Methylation of the thyroid-stimulating hormone receptor gene in epithelial thyroid tumors: a marker of malignancy and a cause of gene silencing. Cancer Res 2003; 63: 2316-2321.
201. Brabant G, Maenhaut C, Kohrle J, Scheumann G, Dralle H, Hoang-Vu C, Hesch RD, von zur Muhlen A, Vassart G, Dumont JE. Human thyrotropin receptor gene: expression in thyroid tumors and correlation to markers of thyroid differentiation and dediferentiation. Mol Cell Endocrinol 1991; 82: R7-R12.
202. Elisei R, Pinchera A, Romei C, Gryczynska M, Pohl V, Maenhaut C, Fugazzola L, Pacini F. Expression of thyrotro-pin receptor (TSH-R), thyroglobulin, thyroperoxidase, and calcitonin messenger ribonucleic acids in thyroid carcinomas: evidence of TSH-R gene transcript in medullary histo-type. J Clin Endocrinol Metab 1994; 78: 867-871.
203. Lin JD. Tyroglobulin and human thyroid cancer. Clin Chim Acta 2008; 388: 15-21.
204. Giovanella L. Highly sensitive thyroglobulin measurements in diferentiated thyroid carcinoma management. Clin Chem Lab Med 2008; 46: 1067-1073.
205. Spencer CA, Lopresti JS. Measuring thyroglobulin and thy-roglobulin autoantibody in patients with diferentiated thyroid cancer. Nat Clin Pract Endocrinol Metab 2008; 4: 223-233
206. Kohn LD, Suzuki K, Nakazato M, Royaux I, Green ED. Efects of thyroglobulin and pendrin on iodide fux through the thy-rocyte. Trends Endocrinol Metab 2001; 12: 10-16.
207. Suzuki K, Lavaroni S, Mori A, Ohta M, Saito J, Pietrarelli M, Singer DS, Kimura S, Katoh R, Kawaoi A, Kohn LD. Autoregulation of thyroid-specifc gene transcription by thyroglobulin. Proc Natl Acad Sci USA 1998; 95: 8251-8256.
208. Suzuki K, Mori A, Saito J, Moriyama E, Ullianich L, Kohn LD. Follicular thyroglobulin suppresses iodide uptake by suppressing expression of the sodium/iodide symporter gene. Endocrinology 1999; 140: 5422-5430. (Pubitemid 30687154)
209. Eng PH, Cardona GR, Fang SL, Previti M, Alex S, Carrasco N, Chin WW, Braverman LE. Escape from the acute Wolf-Chaikof efect is associated with a decrease in thyroid sodium/iodide symporter messenger ribonucleic acid and protein. Endocrinology 1999; 140: 3404-3410.
210. Leoni SG, Galante PA, Ricarte-Filho JC, Kimura ET. Diferential gene expression analysis of iodide-treated rat thyroid follicular cell line PCCl3. Genomics 2008; 91: 356-366.
211. Uyttersprot N, Pelgrims N, Carrasco N, Gervy C, Maenhaut C, Dumont JE, Miot F. Moderate doses of iodide in vivo inhibit cell proliferation and the expression of thy-roperoxidase and Na+/I-symporter mRNAs in dog thyroid. Mol Cell Endocrinol 1997; 131: 195-203.
212. 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.
213. Yamazaki K, Mitsuhashi T, Yamada E, Yamada T, Kosaka S, Takano K, Obara T, Sato K. Amiodarone reversibly decreases sodium-iodide symporter mRNA expression at therapeutic concentrations and induces antioxidant responses at sup-raphysiological concentrations in cultured human thyroid follicles. Tyroid 2007; 17: 1189-1200.
214. Postgard P, Himmelman J, Lindencrona U, Bhogal N, Wiberg D, Berg G, Jansson S, Nystrom E, Forssell-Aronsson E, Nilsson M. Stunning of iodide transport by 131I irradiation in cultured thyroid epithelial cells. J Nucl Med 2002; 43: 828-834.
215. Lundh C, Norden MM, Nilsson M, Forssell-Aronsson E. Reduced iodide transport (stunning) and DNA synthesis in thyrocytes exposed to low absorbed doses from 131I in vitro. J Nucl Med 2007; 48: 481-486.
216. Meller B, Gaspar E, Deisting W, Czarnocka B, Baehre M, Wenzel BE. Decreased radioiodine uptake of FRTL-5 cells after 131I incubation in vitro: molecular biological investigations indicate a cell cycle-dependent pathway. Eur J Nucl Med Mol Imaging 2008; 35: 1204-1212.
217. Schroder-van der Elst JP, van der Heide D, Kastelijn J, Rousset B, Obregon MJ. Te expression of the sodium/iodide sym-porter is up-regulated in the thyroid of fetuses of iodine-def-cient rats. Endocrinology 2001; 142: 3736-3741.
218. Li H, Richard K, McKinnon B, Mortimer RH. Efect of iodide on human choriogonadotropin, sodium-iodide symporter expression, and iodide uptake in BeWo choriocarcinoma cells. J Clin Endocrinol Metab 2007; 92: 4046-4051
219. Everett LA, Glaser B, Beck JC, Idol JR, Buchs A, Heyman M, Adawi F, Hazani E, Nassir E, Baxevanis AD, Shefeld VC, Green ED. Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 1997; 17: 411-422.
220. Kopp P, Pesce L, Solis SJ. Pendred syndrome and iodide transport in the thyroid. Trends Endocrinol Metab 2008; 19: 260-268
221. Royaux IE, Suzuki K, Mori A, Katoh R, Everett LA, Kohn LD, Green ED. Pendrin, the protein encoded by the Pendred syndrome gene (PDS), is an apical porter of iodide in the thyroid and is regulated by thyroglobulin in FRTL-5 cells. Endocrinology 2000; 141: 839-845.
222. Bidart JM, Mian C, Lazar V, Russo D, Filetti S, Caillou B, Schlumberger M. Expression of pendrin and the Pendred syndrome (PDS) gene in human thyroid tissues. J Clin Endocrinol Metab 2000; 85: 2028-2033.
223. Yoshida A, Taniguchi S, Hisatome I, Royaux IE, Green ED, Kohn LD, Suzuki K. Pendrin is an iodide-specifc apical porter responsible for iodide efux from thyroid cells. J Clin Endocrinol Metab 2002; 87: 3356-3361.
224. Gopal E, Fei YJ, Sugawara M, Miyauchi S, Zhuang L, Martin P, Smith SB, Prasad PD, Ganapathy V. Expression of slc5a8 in kidney and its role in Na+-coupled transport of lactate. J Biol Chem 2004; 279: 44522-44532.
225. Gopal E, Miyauchi S, Martin PM, Ananth S, Roon P, Smith SB, Ganapathy V. Transport of nicotinate and structurally related compounds by human SMCT1 (SLC5A8) and its relevance to drug transport in the mammalian intestinal tract. Pharm Res 2007; 24: 575-584.
226. Li H, Myerof L, Smiraglia D, Romero MF, Pretlow TP, Kasturi L, Lutterbaugh J, Rerko RM, Casey G, Issa JP, Willis J, Willson JK, Plass C, Markowitz SD. SLC5A8, a sodium transporter, is a tumor suppressor gene silenced by methylation in human colon aberrant crypt foci and cancers. Proc Natl Acad Sci USA 2003; 100: 8412-8417.
227. Ganapathy V, Gopal E, Miyauchi S, Prasad PD. Biological functions of SLC5A8, a candidate tumour suppressor. Biochem Soc Trans 2005; 33: 237-240.
228. Tangaraju M, Gopal E, Martin PM, Ananth S, Smith SB, Prasad PD, Sterneck E, Ganapathy V. SLC5A8 triggers tumor cell apoptosis through pyruvate-dependent inhibition of histone deacetylases. Cancer Res 2006; 66: 11560-11564.
229. Mian C, Lacroix L, Bidart JM, Caillou B, Filetti S, Schlumberger M. Sodium/iodide symporter in thyroid cancer. Exp Clin Endocrinol Diabetes 2001; 109: 47-51.
230. Arturi F, Russo D, Bidart JM, Scarpelli D, Schlumberger M, Filetti S. Expression pattern of the pendrin and sodium/ iodide symporter genes in human thyroid carcinoma cell lines and human thyroid tumors. Eur J Endocrinol 2001; 145: 129-135.
231. Kondo T, Nakamura N, Suzuki K, Murata S, Muramatsu A, Kawaoi A, Katoh R. Expression of human pendrin in diseased thyroids. J Histochem Cytochem 2003; 51: 167-173.
232. Skubis-Zegadlo J, Nikodemska A, Przytula E, Mikula M, Bardadin K, Ostrowski J, Wenzel BE, Czarnocka B. Expression of pendrin in benign and malignant human thyroid tissues. Br J Cancer 2005; 93: 144-151.
233. 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 efux. J Biol Chem 2004; 279: 13004-13010.
234. Porra V, Bernier-Valentin F, Trouttet-Masson S, Berger-Dutrieux N, Peix JL, Perrin A, Selmi-Ruby S, Rousset B. Characterization and semiquantitative analyses of pendrin expressed in normal and tumoral human thyroid tissues. J Clin Endocrinol Metab 2002; 87: 1700-1707.
235. Lacroix L, Pourcher T, Magnon C, Bellon N, Talbot M, Intaraphairot T, Caillou B, Schlumberger M, Bidart JM. Expression of the apical iodide transporter in human thyroid tissues: a comparison study with other iodide transporters. J Clin Endocrinol Metab 2004; 89: 1423-1428.
236. Porra V, Ferraro-Peyret C, Durand C, Selmi-Ruby S, Giroud H, Berger-Dutrieux N, Decaussin M, Peix JL, Bournaud C, Orgiazzi J, Borson-Chazot F, Dante R, Rousset B. Silencing of the tumor suppressor gene SLC5A8 is associated with BRAF mutations in classical papillary thyroid carcinomas. J Clin Endocrinol Metab 2005; 90: 3028-3035.
237. Suzuki K, Kohn LD. Diferential regulation of apical and basal iodide transporters in the thyroid by thyroglobulin. J Endocrinol 2006; 189: 247-255.