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Clinical and Translational Oncology

Erschienen in:

08.06.2021 | Review Article

Mechanisms of regulating NIS transport to the cell membrane and redifferentiation therapy in thyroid cancer

verfasst von: X. Cai, R. Wang, J. Tan, Z. Meng, N. Li

Erschienen in: Clinical and Translational Oncology | Ausgabe 12/2021

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Abstract

Iodine is an essential constituent of thyroid hormone. Active iodide accumulation in the thyroid is mediated by the sodium iodide symporter (NIS), comprising the first step in thyroid hormone biosynthesis, which relies on the functional expression of NIS on the cell membrane. The retention of NIS expressed in differentiated thyroid cancer (DTC) cells allows further treatment with post-operative radioactive iodine (RAI) therapy. However, compared with normal thyroid tissue, differentiated thyroid tumors usually show a decrease in the active iodide conveyance and NIS is generally retained within the cells, indicating that posttranslational protein transfer to the plasma membrane is abnormal. In recent years, through in vitro studies and studies of patients with DTC, various methods have been tested to increase the transport rate of NIS to the cell membrane and increase the absorption of iodine. An in-depth understanding of the mechanism of NIS transport to the plasma membrane could lead to improvements in RAI therapy. Therefore, in this review, we discuss the current knowledge concerning the post-translational mechanisms that regulate NIS transport to the cell membrane and the current status of redifferentiation therapy for patients with RAI-refractory (RAIR)-DTC.

Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM. Trends in thyroid cancer incidence and mortality in the United States, 1974–2013. JAMA. 2017;317(13):1338–48.PubMedPubMedCentralCrossRef

Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L. 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer the american thyroid association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid. 2016;26(1):1–133.PubMedPubMedCentralCrossRef

Berdelou A, Lamartina L, Klain M, Leboulleux S, Schlumberger M. Treatment of refractory thyroid cancer. Endocr Relat Cancer. 2018;25(4):R209–23.PubMedCrossRef

Fraser S, Go C, Aniss A, Sidhu S, Delbridge L, Learoyd D, Clifton-Bligh R, Tacon L, Tsang V, Robinson B, Gill AJ, Sywak M. BRAF(V600E) mutation is associated with decreased disease-free survival in papillary thyroid cancer. World J Surg. 2016;40(7):1618–24.PubMedCrossRef

Lang BH, Lo CY, Chan WF, Lam KY, Wan KY. Staging systems for papillary thyroid carcinoma: a review and comparison. Ann Surg. 2007;245(3):366–78.PubMedPubMedCentralCrossRef

Lin JD, Hsueh C, Chao TC. Long-term follow-up of the therapeutic outcomes for papillary thyroid carcinoma with distant metastasis. Medicine (Baltimore). 2015;94(26):e1063.PubMedPubMedCentralCrossRef

Schlumberger MJ. Papillary and follicular thyroid carcinoma. N Engl J Med. 1998;338(5):297–306.PubMedCrossRef

Su DH, Chang SH, Chang TC. The impact of locoregional recurrences and distant metastases on the survival of patients with papillary thyroid carcinoma. Clin Endocrinol (Oxf). 2015;82(2):286–94.CrossRef

Rivera M, Ghossein RA, Schoder H, Gomez D, Larson SM, Tuttle RM. Histopathologic characterization of radioactive iodine-refractory fluorodeoxyglucose-positron emission tomography-positive thyroid carcinoma. Cancer. 2008;113(1):48–56.PubMedCrossRef

10.

Schlumberger M, Brose M, Elisei R, Leboulleux S, Luster M, Pitoia F, Pacini F. Definition and management of radioactive iodine-refractory differentiated thyroid cancer. Lancet Diabetes Endocrinol. 2014;2(5):356–8.PubMedCrossRef

11.

Dai G, Levy O, Carrasco N. Cloning and characterization of the thyroid iodide transporter. Nature. 1996;379(6564):458–60.PubMedCrossRef

12.

De la Vieja A, Santisteban P. Role of iodide metabolism in physiology and cancer. Endocr Relat Cancer. 2018;25(4):R225–45.PubMedCrossRef

13.

Fernández LP, López-Márquez A, Santisteban P. Thyroid transcription factors in development, differentiation and disease. Nat Rev Endocrinol. 2014;11(1):29–42.PubMedCrossRef

14.

Martín M, Geysels RC, Peyret V, Bernal Barquero CE, Masini-Repiso AM, Nicola JP. Implications of Na+/I- symporter transport to the plasma membrane for thyroid hormonogenesis and radioiodide therapy. J Endocrine Soc. 2019;3(1):222–34.CrossRef

15.

Fagin JA, Longo DL, Wells SA. Biologic and clinical perspectives on thyroid cancer. N Engl J Med. 2016;375(11):1054–67.PubMedPubMedCentralCrossRef

16.

Tavares C, Coelho MJ, Eloy C, Melo M, da Rocha AG, Pestana A, Batista R, Ferreira LB, Rios E, Selmi-Ruby S, Cavadas B, Pereira L, Sobrinho Simões M, Soares P. NIS expression in thyroid tumors, relation with prognosis clinicopathological and molecular features. Endocr Connect. 2018;7(1):78–90.PubMedCrossRef

17.

Trouttet-Masson S, Selmi-Ruby S, Berger-Dutrieux N, Decaussin M, Peix JL, Perrin A, Bournaud C, Orgiazzi J, Borson-Chazot F, Franc B, Roussett B. Evidence for transcriptional and posttranscriptional alterations of the sodium/iodide symporter expression in hypofunctioning benign and malignant thyroid tumors. Am J Pathol. 2004;165(1):25–34.PubMedPubMedCentralCrossRef

18.

Gerard AC, Daumerie C, Mestdagh C, Gohy S, de Burbure C, Costagliola S, Miot F, Nollevaux MC, Denef JF, Rahier J, Franc B, De Vijlder JJM, Colin IM, Many MC. Correlation between the loss of thyroglobulin iodination and the expression of thyroid-specific proteins involved in iodine metabolism in thyroid carcinomas. J Clin Endocrinol Metab. 2003;88(10):4977–83.PubMedCrossRef

19.

Faggiano A, Caillou B, Lacroix L, Talbot M, Filetti S, Bidart JM, Schlumberger M. Functional characterization of human thyroid tissue with immunohistochemistry. Thyroid. 2007;17(3):203–11.PubMedCrossRef

20.

Wapnir IL, van de Rijn M, Nowels K, Amenta PS, Walton K, Montgomery K, Greco RS, Dohan O, Carrasco N. Immunohistochemical profile of the sodium/iodide symporter in thyroid, breast, and other carcinomas using high density tissue microarrays and conventional sections. J Clin Endocrinol Metab. 2003;88(4):1880–8.PubMedCrossRef

21.

Dohan O, Baloch Z, Banrevi Z, Livolsi V, Carrasco N. Predominant intracellular overexpression of the Na(+)/I(-) symporter (NIS) in a large sampling of thyroid cancer cases. J Clin Endocrinol Metab. 2001;86(6):2697–700.PubMed

22.

Castro MR, Bergert ER, Beito TG, Roche PC, Ziesmer SC, Jhiang SM, Goellner JR, Morris JC. Monoclonal antibodies against the human sodium iodide symporter: utility for immunocytochemistry of thyroid cancer. J Endocrinol. 1999;163(3):495–504.PubMedCrossRef

23.

Spitzweg C, Harrington KJ, Pinke LA, Vile RG, Morris JC. Clinical review 132: The sodium iodide symporter and its potential role in cancer therapy. J Clin Endocrinol Metab. 2001;86(7):3327–35.PubMedCrossRef

24.

Weiss SJ, Philp NJ, Ambesi-Impiombato FS, Grollman EF. Thyrotropin-stimulated iodide transport mediated by adenosine 3’,5’-monophosphate and dependent on protein synthesis. Endocrinology. 1984;114(4):1099–107.PubMedCrossRef

25.

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(6):2227–32.PubMedCrossRef

26.

Ohno M, Zannini M, Levy O, Carrasco N, Di Lauro R. 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-dependermt transcription. Mol Cell Biol. 1999;19(3):2051–60.PubMedPubMedCentralCrossRef

27.

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 thyrotropin stimulates iodide uptake but not sodium/iodide symporter messenger RNA and protein expression. J Endocrinol. 2000;167(1):125–35.PubMedCrossRef

28.

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 U S A. 1994;91(9):3789–93.PubMedPubMedCentralCrossRef

29.

Riedel C, Levy O, Carrasco N. Post-transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem. 2001;276(24):21458–63.PubMedCrossRef

30.

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 Biol Chem. 2007;282(51):36820–8.PubMedCrossRef

31.

Chien WW, Pei L. A novel binding factor facilitates nuclear translocation and transcriptional activation function of the pituitary tumor-transforming gene product. J Biol Chem. 2000;275(25):19422–7.PubMedCrossRef

32.

Smith VE, Sharma N, Watkins RJ, Read ML, Ryan GA, Kwan PP, Martin A, Watkinson JC, Boelaert K, Franklyn JA, McCabe CJ. Manipulation of PBF/PTTG1IP phosphorylation status; a potential new therapeutic strategy for improving radioiodine uptake in thyroid and other tumors. J Clin Endocrinol Metab. 2013;98(7):2876–86.PubMedPubMedCentralCrossRef

33.

Stratford AL, Boelaert K, Tannahill LA, Kim DS, Warfield A, Eggo MC, Gittoes NJL, Young LS, Franklyn JA, McCabe CJ. Pituitary tumor transforming gene binding factor: A novel transforming gene in thyroid tumorigenesis. J Clin Endocrinol Metab. 2005;90(7):4341–9.PubMedCrossRef

34.

Heaney AP, Nelson V, Fernando M, Horwitz G. Transforming events in thyroid tumorigenesis and their association with follicular lesions. J Clin Endocrinol Metab. 2001;86(10):5025–32.PubMedCrossRef

35.

Saez C, Martinez-Brocca MA, Castilla C, Soto A, Navarro E, Tortolero M, Pintor-Toro JA, Japon MA. Prognostic significance of human pituitary tumor-transforming gene immunohistochemical expression in differentiated thyroid cancer. J Clin Endocrinol Metab. 2006;91(4):1404–9.PubMedCrossRef

36.

Smith VE, Read ML, Turnell AS, Watkins RJ, Watkinson JC, Lewy GD, Fong JCW, James SR, Eggo MC, Boelaert K, Franklyn JA, McCabe CJ. A novel mechanism of sodium iodide symporter repression in differentiated thyroid cancer. J Cell Sci. 2009;122(18):3393–402.PubMedPubMedCentralCrossRef

37.

Sastre-Perona A, Santisteban P. Wnt-independent role of β-catenin in thyroid cell proliferation and differentiation. Mol Endocrinol. 2014;28(5):681–95.PubMedPubMedCentralCrossRef

38.

Rossi ED, Straccia P, Palumbo M, Stigliano E, Revelli L, Lombardi CP, Santeusanio G, Pontecorvi A, Fadda G. Diagnostic and prognostic role of HBME-1, Galectin-3, and b-Catenin in poorly differentiated and anaplastic thyroid carcinomas. Appl Immunohistochem Mol Morphol. 2013;21(3):237–41.PubMedCrossRef

39.

Patel NR, Anzalone ML, Buja LM, Elghetany MT. β-Catenin as a Morpho-immunohistochemical marker for the diagnosis of papillary thyroid carcinoma. Arch Pathol Lab Med. 2015;139(5):571–2.PubMedCrossRef

40.

Lan L, Basourakos S, Cui D, Zuo X, Deng W, Huo L, Chen L, Zhang G, Deng L, Shi B, Luo Y. Inhibiting β-catenin expression promotes efficiency of radioiodine treatment in aggressive follicular thyroid cancer cells probably through mediating NIS localization. Oncol Rep. 2017;37(1):426–34.PubMedCrossRef

41.

Amit M, Na’ara S, Francis D, Matanis W, Zolotov S, Eisenhaber B, Eisenhaber F, Weiler Sagie M, Malkin L, Billan S, Charas T, Gil Z. Post-translational regulation of radioactive iodine therapy response in papillary thyroid carcinoma. J Natl Cancer Inst. 2017;109(12). https://doi.org/10.1093/jnci/djx092.

42.

Eisenhaber B, Bork P, Eisenhaber F. Sequence properties of GPI-anchored proteins near the omega-site: constraints for the polypeptide binding site of the putative transamidase. Protein Eng. 1998;11(12):1155–61.PubMedCrossRef

43.

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 U S A. 1997;94(11):5568–73.PubMedPubMedCentralCrossRef

44.

Zhou F, Xu W, Hong M, Pan Z, Sinko PJ, Ma J, You G. The role of N-linked glycosylation in protein folding, membrane targeting, and substrate binding of human organic anion transporter hOAT4. Mol Pharmacol. 2005;67(3):868–76.PubMedCrossRef

45.

Chung T, Youn H, Yeom CJ, Kang KW, Chung JK. Glycosylation of sodium/iodide symporter (NIS) regulates its membrane translocation and radioiodine uptake. PLoS One. 2015;10(11):e0142984.PubMedPubMedCentralCrossRef

46.

Knostman KAB, McCubrey JA, Morrison CD, Zhang ZX, Capen CC, Jhiang SM. PI3K activation is associated with intracellular sodium/iodide symporter protein expression in breast cancer. Bmc Cancer. 2007;7(1):137.PubMedPubMedCentralCrossRef

47.

Feng F, Yehia L, Ni Y, Chang YS, Jhiang SM, Eng C. A nonpump function of sodium iodide symporter in thyroid cancer via cross-talk with PTEN signaling. Cancer Res. 2018;78(21):6121–33.PubMedPubMedCentralCrossRef

48.

Vidi PA, Chen JJ, Irudayaraj JMK, Watts VJ. Adenosine A(2A) receptors assemble into higher-order oligomers at the plasma membrane. FEBS Lett. 2008;582(29):3985–90.PubMedCrossRef

49.

Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 2000;103(2):211–25.PubMedCrossRef

50.

Maurel D, Comps-Agrar L, Brock C, Rives ML, Bourrier E, Ayoub MA, Bazin H, Tinel N, Durroux T, Prezeau L, Trinquet E, Pin JP. Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat Methods. 2008;5(6):561–7.PubMedPubMedCentralCrossRef

51.

Maruyama IN. Activation of transmembrane cell-surface receptors via a common mechanism? The “rotation model’’’.” BioEssays. 2015;37(9):959–67.PubMedPubMedCentralCrossRef

52.

Li E, You M, Hristova K. Sodium dodecyl sulfate - Polyacrylamide gel electrophoresis and Forster resonance energy transfer suggest weak interactions between fibroblast growth factor receptor 3 (FGFR3) transmembrane domains in the absence of extracellular domains and ligands. Biochemistry. 2005;44(1):352–60.PubMedCrossRef

53.

Bocharov EV, Mineev KS, Volynsky PE, Ermolyuk YS, Tkach EN, Sobol AG, Chupin VV, Kirpichnikov MP, Efremov RG, Arseniev AS. Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. J Biol Chem. 2008;283(11):6950–6.PubMedCrossRef

54.

Huc-Brandt S, Marcellin D, Graslin F, Averseng O, Bellanger L, Hivin P, Quemeneur E, Basquin C, Navarro V, Pourcher T, Darrouzet E. 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-terminal fragment. BBA-Biomembranes. 2011;1808(1):65–77.PubMedCrossRef

55.

Thompson RJ, Fletcher A, Brookes K, Nieto H, Alshahrani MM, Mueller JW, Fine NHF, Hodson DJ, Boelaert K, Read ML, Smith VE, McCabe CJ. Dimerization of the sodium/iodide symporter. Thyroid. 2019;29(10):1485–98.PubMedPubMedCentralCrossRef

56.

Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, Mangelsdorf DJ. Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell. 2006;126(4):789–99.PubMedPubMedCentralCrossRef

57.

Kim D-K, Gang G-T, Ryu D, Koh M, Kim Y-N, Kim SS, Park J, Kim Y-H, Sim T, Lee I-K, Choi CS, Park SB, Lee C-H, Koo S-H, Choi H-S. Inverse agonist of nuclear receptor ERRg mediates antidiabetic effect through inhibition of hepatic gluconeogenesis. Diabetes. 2013;62(9):3093–102.PubMedPubMedCentralCrossRef

58.

Kim D-K, Kim JR, Koh M, Kim YD, Lee J-M, Chanda D, Park SB, Min J-J, Lee C-H, Park T-S, Choi H-S. Estrogen-related Receptor γ (ERRγ) is a novel transcriptional regulator of phosphatidic acid phosphatase, LIPIN1, and Inhibits hepatic insulin signaling. J Biol Chem. 2011;286(44):38035–42.PubMedPubMedCentralCrossRef

59.

Kim D-K, Jeong J-H, Lee J-M, Kim KS, Park S-H, Kim YD, Koh M, Shin M, Jung YS, Kim H-S, Lee T-H, Oh B-C, Kim JI, Park HT, Jeong W-I, Lee C-H, Park SB, Min J-J, Jung S-I, Choi S-Y, Choy HE, Choi H-S. Inverse agonist of estrogen-related receptor γ controls Salmonella typhimurium infection by modulating host iron homeostasis. Nat Med. 2014;20(4):419–24.PubMedCrossRef

60.

Kwon D-H, Eom GH, Kee HJ, Nam YS, Cho YK, Kim D-K, Koo JY, Kim H-S, Nam K-I, Kim KK, Lee I-K, Park SB, Choi H-S, Kook H. Estrogen-related receptor gamma induces cardiac hypertrophy by activating GATA4. J Mol Cell Cardiol. 2013;65:88–97.PubMedCrossRef

61.

Singh TD, Jeong SY, Lee SW, Ha JH, Lee IK, Kim SH, Kim J, Cho SJ, Ahn BC, Lee J, Jeon YH. Inverse agonist of estrogen-related receptor enhances sodium iodide symporter function through mitogen-activated protein kinase signaling in anaplastic thyroid cancer cells. J Nucl Med. 2015;56(11):1690–6.PubMedCrossRef

62.

Fletcher A, Read ML, Thornton CEM, Larner DP, Poole VL, Brookes K, Nieto HR, Alshahrani M, Thompson RJ, Lavery GG, Landa I, Fagin JA, Campbell MJ, Boelaert K, Turnell AS, Smith VE, McCabe CJ. Targeting novel sodium iodide symporter interactors ADP-ribosylation factor 4 and valosin-containing protein enhances radioiodine uptake. Cancer Res. 2020;80(1):102–15.PubMedCrossRef

63.

Wang J, Fresquez T, Kandachar V, Deretic D. The Arf GEF GBF1 and Arf4 synergize with the sensory receptor cargo, rhodopsin, to regulate ciliary membrane trafficking. J Cell Sci. 2017;130(23):3975–87.PubMedPubMedCentral

64.

Spitzweg C, Bible KC, Hofbauer LC, Morris JC. Advanced radioiodine-refractory differentiated thyroid cancer: the sodium iodide symporter and other emerging therapeutic targets. Lancet Diabetes Endocrinol. 2014;2(10):830–42.PubMedCrossRef

65.

Schlumberger M, Lacroix L, Russo D, Filetti S, Bidart JM. Defects in iodide metabolism in thyroid cancer and implications for the follow-up and treatment of patients. Nat Clin Pract Endocrinol Metab. 2007;3(3):260–9.PubMedCrossRef

66.

Konrad M, Merz WE. Long-term effect of cyclic AMP on N-glycosylation is caused by an increase in the activity of the cis-prenyltransferase. Biochem J. 1996;316(Pt 2):575–81.PubMedPubMedCentralCrossRef

67.

Konrad M, Merz WE. Regulation of N-glycosylation. Long term effect of cyclic AMP mediates enhanced synthesis of the dolichol pyrophosphate core oligosaccharide. J Biol Chem. 1994;269(12):8659–66.PubMedCrossRef

68.

Kogai T, Taki K, Brent GA. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer. 2006;13(3):797–826.PubMedCrossRef

69.

Singh TD, Song J, Kim J, Chin J, Ji HD, Lee J-E, Lee SB, Yoon H, Yu JH, Kim SK, Yoon GS, Hwang H, Lee HW, Oh JM, Lee S-W, Lee J, Choi H-S, Na S-Y, Choi W-I, Park YJ, Song YS, Kim YA, Lee I-K, Cho SJ, Jeon YH. A novel orally active inverse agonist of estrogen-related receptor gamma (ERRγ), DN200434, a booster of NIS in anaplastic thyroid cancer. Clin Cancer Res. 2019;25(16):5069–81.PubMedCrossRef

70.

Segura-Cabrera A, Tripathi R, Zhang XY, Gui L, Chou TF, Komurov K. A structure- and chemical genomics-based approach for repositioning of drugs against VCP/p97 ATPase. Sci Rep. 2017;7:44912.PubMedPubMedCentralCrossRef

71.

Schmutzler C, Schmitt TL, Glaser F, Loos U, Kohrle J. The promoter of the human sodium/iodide-symporter gene responds to retinoic acid. Mol Cell Endocrinol. 2002;189(1–2):145–55.PubMedCrossRef

72.

Pak K, Shin S, Kim S-J, Kim I-J, Chang S, Koo P, Kwak J, Kim J-H. Response of retinoic acid in patients with radioactive iodine-refractory thyroid cancer: a meta-analysis. Oncol Res Treatment. 2018;41(3):100–4.CrossRef

73.

Corton JC, Anderson SP, Stauber A. Central role of peroxisome proliferator-activated receptors in the actions of peroxisome proliferators. Annu Rev Pharmacol Toxicol. 2000;40:491–518.PubMedCrossRef

74.

Roberts-Thomson SJ. Peroxisome proliferator-activated receptors in tumorigenesis: targets of tumour promotion and treatment. Immunol Cell Biol. 2000;78(4):436–41.PubMedCrossRef

75.

Frohlich E, Machicao F, Wahl R. Action of thiazolidinediones on differentiation, proliferation and apoptosis of normal and transformed thyrocytes in culture. Endocr Relat Cancer. 2005;12(2):291–303.PubMedCrossRef

76.

Park JW, Zarnegar R, Kanauchi H, Wong MG, Hyun WC, Ginzinger DG, Lobo M, Cotter P, Duh QY, Clark OH. Troglitazone, the peroxisome proliferator-activated receptor-gamma agonist, induces antiproliferation and redifferentiation in human thyroid cancer cell lines. Thyroid. 2005;15(3):222–31.PubMedCrossRef

77.

Elola M, Yoldi A, Emparanza JI, Matteucci T, Bilbao I, Goena M. Redifferentiation therapy with rosiglitazone in a case of differentiated thyroid cancer with pulmonary metastases and absence of radioiodine uptake. Revista Española de Medicina Nuclear (English Edition). 2011;30(4):241–3.CrossRef

78.

Rosenbaum-Krumme SJ, Freudenberg LS, Jentzen W, Bockisch A, Nagarajah J. Effects of rosiglitazone on radioiodine negative and progressive differentiated thyroid carcinoma as assessed by 124I PET/CT imaging. Clin Nucl Med. 2012;37(3):47–52.CrossRef

79.

Xing M. Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer. 2013;13(3):184–99.PubMedPubMedCentralCrossRef

80.

Fu H, Cheng L, Jin Y, Cheng L, Liu M, Chen L. MAPK Inhibitors enhance HDAC inhibitor-induced redifferentiation in papillary thyroid cancer cells harboring BRAFV600E: an in vitro study. Molecular Therapy Oncolytics. 2019;12:235–45.PubMedPubMedCentralCrossRef

81.

Wachter S, Damanakis A, Elxnat M, Roth S, Wunderlich A, Verburg F, Fellinger S, Bartsch D, Di Fazio P. Epigenetic modiications in thyroid cancer cells restore NIS and radio-iodine uptake and promote cell death. J Clin Med. 2018;7(4):61.PubMedCentralCrossRef

82.

Massimino M, TirrÒ E, Stella S, Frasca F, Vella V, Sciacca L, Pennisi MS, Vitale SR, Puma A, Romano C, Manzella L. Effect of combined epigenetic treatments and ectopic NIS expression on undifferentiated thyroid cancer cells. Anticancer Res. 2018;38(12):6653–62.PubMedCrossRef

83.

Cheng W, Liu R, Zhu G, Wang H, Xing M. Robust Thyroid gene expression and radioiodine uptake induced by simultaneous suppression of BRAF V600E and histone deacetylase in thyroid cancer cells. J Clin Endocrinol Metab. 2016;101(3):962–71.PubMedPubMedCentralCrossRef

84.

Amiri-Kordestani L, Luchenko V, Peer CJ, Ghafourian K, Reynolds J, Draper D, Frye R, Woo S, Venzon D, Wright J, Skarulis M, Figg WD, Fojo T, Bates SE, Piekarz RL. Phase I trial of a new schedule of romidepsin in patients with advanced cancers. Clin Cancer Res. 2013;19(16):4499–507.PubMedPubMedCentralCrossRef

85.

Kelly WK, O’Connor OA, Krug LM, Chiao JH, Heaney M, Curley T, MacGregore-Cortelli B, Tong W, Secrist JP, Schwartz L, Richardson S, Chu E, Olgac S, Marks PA, Scher H, Richon VM. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol. 2005;23(17):3923–31.PubMedCrossRef

86.

Nilubol N, Merkel R, Yang L, Patel D, Reynolds JC, Sadowski SM, Neychev V, Kebebew E. A phase II trial of valproic acid in patients with advanced, radioiodine-resistant thyroid cancers of follicular cell origin. Clin Endocrinol. 2017;86(1):128–33.CrossRef

87.

Sherman EJ, Su YB, Lyall A, Schöder H, Fury MG, Ghossein RA, Haque S, Lisa D, Shaha AR, Tuttle RM, Pfister DG. Evaluation of romidepsin for clinical activity and radioactive iodine reuptake in radioactive iodine-refractory thyroid carcinoma. Thyroid. 2013;23(5):593–9.PubMedPubMedCentralCrossRef

88.

Chakravarty D, Santos E, Ryder M, Knauf JA, Liao XH, West BL, Bollag G, Kolesnick R, Thin TH, Rosen N, Zanzonico P, Larson SM, Refetoff S, Ghossein R, Fagin JA. Small-molecule MAPK inhibitors restore radioiodine incorporation in mouse thyroid cancers with conditional BRAF activation. J Clin Investig. 2011;121(12):4700–11.PubMedPubMedCentralCrossRef

89.

Ho AL, Grewal RK, Leboeuf R, Sherman EJ, Pfister DG, Deandreis D, Pentlow KS, Zanzonico PB, Haque S, Gavane S, Ghossein RA, Ricarte JC, Dominguez JM, Shen RL, Tuttle RM, Larson SM, Fagin JA. Selumetinib-enhanced radioiodine uptake in advanced thyroid cancer. N Engl J Med. 2013;368(7):623–32.PubMedPubMedCentralCrossRef

90.

Hou P, Bojdani E, Xing MZ. Induction of thyroid gene expression and radioiodine uptake in thyroid cancer cells by targeting major signaling pathways. J Clin Endocrinol Metab. 2010;95(2):820–8.PubMedCrossRef

91.

Rothenberg SM, McFadden DG, Palmer EL, Daniels GH, Wirth LJ. Redifferentiation of iodine-refractory BRAF V600E-mutant metastatic papillary thyroid cancer with dabrafenib. Clin Cancer Res. 2015;21(5):1028–35.PubMedCrossRef

92.

Ruan MM, Liu M, Dong QG, Chen LB. Iodide- and glucose-handling gene expression regulated by sorafenib or cabozantinib in papillary thyroid cancer. J Clin Endocrinol Metab. 2015;100(5):1771–9.PubMedCrossRef

93.

Jaber T, Waguespack SG, Cabanillas ME, Elbanan M, Vu T, Dadu R, Sherman SI, Amit M, Santos EB, Zafereo M, Busaidy NL. Targeted therapy in advanced thyroid cancer to resensitize tumors to radioactive iodine. J Clin Endocrinol Metab. 2018;103(10):3698–705.PubMedPubMedCentralCrossRef

94.

Dunn LA, Sherman EJ, Baxi SS, Tchekmedyian V, Grewal RK, Larson SM, Pentlow KS, Haque S, Tuttle RM, Sabra MM, Fish S, Boucai L, Walters J, Ghossein RA, Seshan VE, Ni A, Li D, Knauf JA, Pfister DG, Fagin JA, Ho AL. Vemurafenib redifferentiation of BRAFmutant, RAI-refractory thyroid cancers. J Clin Endocrinol Metabol. 2019;104(5):1417–28.CrossRef

95.

Rothenberg SM, Daniels GH, Wirth LJ. Redifferentiation of iodine-refractory BRAF V600E-mutant metastatic papillary thyroid cancer with Dabrafenib—response. Clin Cancer Res. 2015;21(24):5640–1.PubMedCrossRef

96.

Ho AL, Grewal RK, Leboeuf R, Sherman EJ, Pfister DG, Deandreis D, Pentlow KS, Zanzonico PB, Haque S, Gavane S, Ghossein RA, Ricarte-Filho JC, Dominguez JM, Shen R, Tuttle RM, Larson SM, Fagin JA. Selumetinib-enhanced radioiodine uptake in advanced thyroid cancer. N Engl J Med. 2013;368(7):623–32.PubMedPubMedCentralCrossRef

97.

Brown SR, Hall A, Buckley HL, Flanagan L, Gonzalez de Castro D, Farnell K, Moss L, Gregory R, Newbold K, Du Y, Flux G, Wadsley J. Investigating the potential clinical beneit of Selumetinib in resensitising advanced iodine refractory differentiated thyroid cancer to radioiodine therapy (SEL-I-METRY): protocol for a multicentre UK single arm phase II trial. BMC Cancer. 2019;19(1):582.PubMedPubMedCentralCrossRef

98.

Saqcena M, Leandro-Garcia LJ, Maag JLV, Tchekmedyian V, Krishnamoorthy GP, Tamarapu PP, Tiedje V, Reuter V, Knauf JA, de Stanchina E, Xu B, Liao X-H, Refetof S, Ghossein R, Chi P, Ho AL, Koche RP, Fagin JA. SWI/SNF complex mutations promote thyroid tumor progression and insensitivity to redifferentiation therapies. Cancer Discov. 2020;11(5):1158–75.PubMedCrossRefPubMedCentral

99.

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(2):243–52.PubMedCrossRef

100.

Liu YY, Zhang XL, Ringel MD, Jhiang SM. Modulation of sodium iodide symporter expression and function by LY294002, Akti-1/2 and Rapamycin in thyroid cells. Endocr Relat Cancer. 2012;19(3):291–304.PubMedPubMedCentralCrossRef

101.

Plantinga TS, Heinhuis B, Gerrits D, Netea MG, Joosten LA, Hermus AR, Oyen WJ, Schweppe RE, Haugen BR, Boerman OC, Smit JW, Netea-Maier RT. mTOR Inhibition promotes TTF1-dependent redifferentiation and restores iodine uptake in thyroid carcinoma cell lines. J Clin Endocrinol Metab. 2014;99(7):E1368-1375.PubMedPubMedCentralCrossRef

102.

Hanna GJ, Busaidy NL, Chau NG, Wirth LJ, Barletta JA, Calles A, Haddad RI, Kraft S, Cabanillas ME, Rabinowits G, O’Neill A, Limaye SA, Alexander EK, Moore FD, Misiwkeiwicz K, Thomas T, Nehs M, Marqusee E, Lee SL, Jänne PA, Lorch JH. Genomic correlates of response to everolimus in aggressive radioiodine-refractory thyroid cancer: a phase II study. Clin Cancer Res. 2018;24(7):1546–53.PubMedCrossRef

103.

Borson-Chazot F, Dantony E, Illouz F, Lopez J, Niccoli P, Wassermann J, Do Cao C, Leboulleux S, Klein M, Tabarin A, Eberle M-C, Benisvy D, de la Fouchardière C, Bournaud C, Lasolle H, Delahaye A, Rabilloud M, Lapras V, Decaussin-Petrucci M, Schlumberger M. Effect of buparlisib, a pan-class I PI3K inhibitor, in refractory follicular and poorly differentiated thyroid cancer. Thyroid. 2018;28(9):1174–9.PubMedCrossRef

104.

Alexander EK, Larsen PR. Radioiodine for thyroid cancer - is less more? N Engl J Med. 2012;366(18):1732–3.PubMedCrossRef

105.

Tavares C, Coelho MJ, Eloy C, Melo M, da Rocha AG, Pestana A, Batista R, Ferreira LB, Rios E, Selmi-Ruby S, Cavadas B, Pereira L, Simoes MS, Soares P. NIS expression in thyroid tumors, relation with prognosis clinicopathological and molecular features. Endocr Connect. 2018;7(1):78–90.PubMedCrossRef

106.

Dohan O, Baloch Z, Banrevi Z, Livolsi V, Carrasco N. Rapid communication: predominant intracellular overexpression of the Na(+)/I(-) symporter (NIS) in a large sampling of thyroid cancer cases. J Clin Endocrinol Metab. 2001;86(6):2697–700.PubMed

107.

Kollecker I, von Wasielewski R, Langner C, Muller JA, Spitzweg C, Kreipe H, Brabant G. Subcellular distribution of the sodium iodide symporter in benign and malignant thyroid tissues. Thyroid. 2012;22(5):529–35.PubMedCrossRef

108.

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 Investig. 1998;101(7):1296–300.PubMedPubMedCentralCrossRef

Titel: Mechanisms of regulating NIS transport to the cell membrane and redifferentiation therapy in thyroid cancer
verfasst von: X. Cai
R. Wang
J. Tan
Z. Meng
N. Li
Publikationsdatum: 08.06.2021
Verlag: Springer International Publishing
Erschienen in: Clinical and Translational Oncology / Ausgabe 12/2021
Print ISSN: 1699-048X
Elektronische ISSN: 1699-3055
DOI: https://doi.org/10.1007/s12094-021-02655-0

Springer Medizin

Mechanisms of regulating NIS transport to the cell membrane and redifferentiation therapy in thyroid cancer

Abstract

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Springer Medizin

Abstract

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