Inverse agonist of estrogen-related receptor G enhances sodium iodide symporter function through mitogen-activated protein kinase signaling in anaplastic thyroid cancer cells

Journal of Nuclear Medicine

Volumn 56, Issue 11, 2015, Pages 1690-1696

  Singh, Thoudam Debraj ^a   Jeong, Shin Young ^a   Lee, Sang Woo ^a   Ha, Jeoung Hee ^a   Lee, In Kyu ^a   Kim, Seong Heon ^b   Kim, Jina ^b   Cho, Sung Jin ^b   Ahn, Byeong Cheol ^a   Lee, Jaetae ^a,b   Jeon, Young Hyun ^a,c  

^a Kyungpook National University School of Medicine   (South Korea)

^b Daegu Gyeongbuk Medical Innovation Foundation   (South Korea)

^c Kyungpook National University Hospital   (South Korea)

Author keywords

Anaplastic thyroid cancer; Estrogen related receptor gamma (ERR ); MAP kinase signaling; Radioiodide therapy; Sodium iodide symporter (NIS)

Indexed keywords

ESTROGEN RELATED RECEPTOR GAMMA; GSK 5182; HORMONE RECEPTOR STIMULATING AGENT; IODINE 131; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; SODIUM IODIDE SYMPORTER; STEROID RECEPTOR; UNCLASSIFIED DRUG; COTRANSPORTER; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR GAMMA; GSK5182; PROTEIN KINASE INHIBITOR; RADIOACTIVE IODINE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN;

ANAPLASTIC THYROID CANCER; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; THYROID CANCER CELL LINE; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; HUMAN; METABOLISM; THYROID CARCINOMA; THYROID TUMOR; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE, TUMOR; ESTROGEN RECEPTOR MODULATORS; HUMANS; IODINE RADIOISOTOPES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; RECEPTORS, ESTROGEN; SYMPORTERS; TAMOXIFEN; THYROID CARCINOMA, ANAPLASTIC; THYROID NEOPLASMS; TUMOR STEM CELL ASSAY;

EID: 84946606345     PISSN: 01615505     EISSN: 2159662X     Source Type: Journal    
DOI: 10.2967/jnumed.115.160366     Document Type: Article

References (36)

1. Fassnacht M, Kreissl MC, Weismann D, Allolio B. New targets and therapeutic approaches for endocrine malignancies. Pharmacol Ther. 2009;123:117-141.
2. Nagaiah G, Hossain A, Mooney CJ, Parmentier J, Remick SC. Anaplastic thyroid cancer: a review of epidemiology, pathogenesis, and treatment. J Oncol. 2011;2011:542358.
3. De Falco V, Guarino V, Avilla E, et al. Biological role and potential therapeutic targeting of the chemokine receptor CXCR4 in undifferentiated thyroid cancer. Cancer Res. 2007;67:11821-11829.
4. Busnardo B, Daniele O, Pelizzo MR, et al. A multimodality therapeutic approach in anaplastic thyroid carcinoma: study on 39 patients. J Endocrinol Invest. 2000;23:755-761.
5. Aldinger KA, Samaan NA, Ibanez M, Hill CS Jr. Anaplastic carcinoma of the thyroid: a review of 84 cases of spindle and giant cell carcinoma of the thyroid. Cancer. 1978;41:2267-2275.
6. Kim JH, Leeper RD. Treatment of locally advanced thyroid carcinoma with combination doxorubicin and radiation therapy. Cancer. 1987;60:2372-2375.
7. Tennvall J, Lundell G, Wahlberg P, et al. Anaplastic thyroid carcinoma: three protocols combining doxorubicin, hyperfractionated radiotherapy and surgery. Br J Cancer. 2002;86:1848-1853.
8. Chung JK. Sodium iodide symporter: its role in nuclear medicine. J Nucl Med. 2002;43:1188-1200.
9. Rosai J. Poorly differentiated thyroid carcinoma: introduction to the issue, its landmarks, and clinical impact. Endocr Pathol. 2004;15:293-296.
10. Patel KN, Shaha AR. Poorly differentiated and anaplastic thyroid cancer. Cancer Control. 2006;13:119-128.
11. Kogai T, Taki K, Brent GA. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer. 2006;13:797-826.
12. Lee YJ, Chung JK, Kang JH, Jeong JM, Lee DS, Lee MC. Wild-type p53 enhances the cytotoxic effect of radionuclide gene therapy using sodium iodide symporter in a murine anaplastic thyroid cancer model. Eur J Nucl Med Mol Imaging. 2010;37:235-241.
13. Lee YJ, Chung JK, Shin JH, et al. In vitro and in vivo properties of a human anaplastic thyroid carcinoma cell line transfected with the sodium iodide symporter gene. Thyroid. 2004;14:889-895.
14. 131I cytotoxicity in anaplastic thyroid cancer cells. Thyroid. 2013;23:838-846.
15. Tremblay AM, Giguere V. The NR3B subgroup: an ovERRview. Nucl Recept Signal. 2007;5:e009.
16. Heard DJ, Norby PL, Holloway J, Vissing H. Human ERRgamma, a third member of the estrogen receptor-related receptor (ERR) subfamily of orphan nuclear receptors: tissue-specific isoforms are expressed during development and in the adult. Mol Endocrinol. 2000;14:382-392.
17. Hong H, Yang L, Stallcup MR. Hormone-independent transcriptional activation and coactivator binding by novel orphan nuclear receptor ERR3. J Biol Chem. 1999;274:22618-22626.
18. Kim DK, Gang GT, Ryu D, et al. Inverse agonist of nuclear receptor ERRgamma mediates antidiabetic effect through inhibition of hepatic gluconeogenesis. Diabetes. 2013;62:3093-3102.
19. Kim DK, Ryu D, Koh M, et al. Orphan nuclear receptor estrogen-related receptor gamma (ERRgamma) is key regulator of hepatic gluconeogenesis. J Biol Chem. 2012;287:21628-21639.
20. Kim DK, Kim JR, Koh M, et al. Estrogen-related receptor gamma (ERRgamma) is a novel transcriptional regulator of phosphatidic acid phosphatase, LIPIN1, and inhibits hepatic insulin signaling. J Biol Chem. 2011;286:38035-38042.
21. Kim DK, Jeong JH, Lee JM, et al. Inverse agonist of estrogen-related receptor gamma controls Salmonella typhimurium infection by modulating host iron homeostasis. Nat Med. 2014;20:419-424.
22. Giguère V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev. 2008;29:677-696.
23. Chao EY, Collins JL, Gaillard S, et al. Structure-guided synthesis of tamoxifen analogs with improved selectivity for the orphan ERRgamma. Bioorg Med Chem Lett. 2006;16:821-824.
24. Kogai T, Schultz JJ, Johnson LS, Huang M, Brent GA. Retinoic acid induces sodium/iodide symporter gene expression and radioiodide uptake in the MCF-7 breast cancer cell line. Proc Natl Acad Sci USA. 2000;97:8519-8524.
25. Kogai T, Kanamoto Y, Che LH, et al. Systemic retinoic acid treatment induces sodium/iodide symporter expression and radioiodide uptake in mouse breast cancer models. Cancer Res. 2004;64:415-422.
26. Kwon DH, Eom GH, Kee HJ, et al. Estrogen-related receptor gamma induces cardiac hypertrophy by activating GATA4. J Mol Cell Cardiol. 2013;65:88-97.
27. Catalano MG, Fortunati N, Pugliese M, et al. Histone deacetylase inhibition modulates E-cadherin expression and suppresses migration and invasion of anaplastic thyroid cancer cells. J Clin Endocrinol Metab. 2012;97:E1150-E1159.
28. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature. 2001;410:37-40.
29. Samuvel DJ, Jayanthi LD, Bhat NR, Ramamoorthy S. A role for p38 mitogen-activated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression. J Neurosci. 2005;25:29-41.
30. Apparsundaram S, Sung U, Price RD, Blakely RD. Trafficking-dependent and -independent pathways of neurotransmitter transporter regulation differentially involving p38 mitogen-activated protein kinase revealed in studies of insulin modulation of norepinephrine transport in SK-N-SH cells. J Pharmacol Exp Ther. 2001;299:666-677.
31. Knostman KA, McCubrey JA, Morrison CD, Zhang Z, Capen CC, Jhiang SM. PI3K activation is associated with intracellular sodium/iodide symporter protein expression in breast cancer. BMC Cancer. 2007;7:137.
32. Zhang Z, Beyer S, Jhiang SM. MEK inhibition leads to lysosome-mediated Na+/I-symporter protein degradation in human breast cancer cells. Endocr Relat Cancer. 2013;20:241-250.
33. Riedel C, Levy O, Carrasco N. Post-transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem. 2001;276:21458-21463.
34. Arturi F, Ferretti E, Presta I, et al. Regulation of iodide uptake and sodium/iodide symporter expression in the mcf-7 human breast cancer cell line. J Clin Endocrinol Metab. 2005;90:2321-2326.
35. 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;86:3327-3335.
36. Ramamoorthy S, Blakely RD. Phosphorylation and sequestration of serotonin transporters differentially modulated by psychostimulants. Science. 1999;285:763-766.