Hypermethylation of a new distal sodium/iodide symporter (NIS) enhancer (NDE) Is associated with reduced nis expression in thyroid tumors

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 6, 2014, Pages

  Galrão, Ana Luiza ^a   Camargo, Rosalinda Y ^a   Friguglietti, Celso U ^b   Moraes, Lais ^c   Cerutti, Janete Maria ^c   Serrano Nascimento, Caroline ^a   Suzuki, Miriam F ^d   Medeiros Neto, Geraldo ^a   Rubio, Ileana G S ^c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b HOSPITAL SANTA CATARINA   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d INSTITUTO DE PESQUISAS ENERGÉTICAS E NUCLEARES   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BISULFITE; IODINE 125; MESSENGER RNA; SODIUM IODIDE SYMPORTER;

5' UNTRANSLATED REGION; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; CORRELATIONAL STUDY; CPG ISLAND; DNA METHYLATION; EMBRYO; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION; GENE FUNCTION; GENETIC IDENTIFICATION; GENETIC REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NIS GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; THYROID CANCER; THYROID TUMOR; TUMOR CELL CULTURE; WESTERN BLOTTING;

AZACITIDINE; CARCINOMA, PAPILLARY, FOLLICULAR; CPG ISLANDS; DNA METHYLATION; DOWN-REGULATION; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; SYMPORTERS; THYROID NEOPLASMS;

EID: 84902309987     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-1450     Document Type: Article

References (40)

1. National Cancer Institute. Thyroid cancer. http://www.cancer.gov/ cancertopics/types/thyroid.
2. Kondo T, Ezzat S, Asa SL. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer. 2006;6:292-306.
3. Ricarte-Filho JC, Ryder M, Chitale DA, et al. Mutational profile of advanced pr imary and metastatic radioactive iodine-refractory thyroid cancers reveals distinct pathogenetic roles for BRAF, PIK3CA, and AKT1. Cancer Res. 2009;69:4885-4893.
4. Elisei R, Romei C, Vorontsova T, et al. RET/PTC rearrangements in thyroid nodules: studies in irradiated and not irradiated, malignant and benign thyroid lesions in children and adults. J Clin Endocrinol Metab. 2001;86:3211-3216.
5. Mitsutake N, Knauf JA, Mitsutake S, Mesa C Jr., Zhang L, Fagin JA. Conditional BRAFV600E expression induces DNA synthesis, apoptosis, dedifferentiation, and chromosomal instability in thyroid PCCL3 cells. Cancer Res. 2005;65:2465-2473.
6. Carrasco N. Iodide transport in the thyroid gland. Biochim Biophys Acta. 1993;1154:65-82.
7. Dohán O,De la Vieja A,Paroder V,et al The sodium/iodide symporter (NIS): characterization, regulation, and medical significance Endocr Rev. 2003 24 48-77.
8. Sodré AK, Rubio IG, Galrao AL, et al. Association of low sodiumiodide symporter messenger ribonucleic acid expression in malignant thyroid nodules with increased intracellular protein staining. J Clin Endocrinol Metab. 2008;93:4141-4145.
9. Trouttet-Masson S, Selmi-Ruby S, Bernier-Valentin F, et al. Evidence for transcriptional and posttranscriptional alterations of the sodium/iodide symporter expression in hypofunctioning benign and malignant thyroid tumors. Am J Pathol. 2004;165:25-34.
10. Spitzweg C, Morris JC. Genetics and phenomics of hypothyroidism and goiter due to NIS mutations. Mol Cell Endocrinol. 2010;322: 56-63.
11. Razin A, Cedar H. DNA methylation and gene expression. Microbiol Rev. 1991;55:451-458.
12. Lister R, Pelizzola M, Dowen RH, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315-322.
13. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001;293:1068-1070.
14. Irizarry RA, Ladd-Acosta C, Wen B, et al. The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41:178-186.
15. Kondo T, Asa SL, Ezzat S. Epigenetic dysregulation in thyroid neoplasia. Endocrinol Metab Clin North Am. 2008;37:389-400, ix.
16. Stephen JK, Chitale D, Narra V, Chen KM, Sawhney R, Worsham MJ. DNA methylation in thyroid tumorigenesis. Cancers. 2011;3: 1732-1743.
17. Smith JA, Fan CY, Zo u C, Bodenner D, Kokoska MS. Methylation status of genes in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg. 2007;133:1006-1011.
18. Galra o AL, Sodré AK, Camargo RY, et al. Methylation levels of sodium-iodide symporter (NIS) promoter in benign and malignant thyroid tumors with reduced NIS expression. Endocrine. 2013;43: 225-229.
19. Venkataraman GM, Yatin M, Marcinek R, Ain KB. Restoration of iodide uptake in dedifferentiated thyroid carcinoma: relationship to humanNa-/I-symporter gene methylation status. J Clin Endocrinol Metab. 1999;84:2449-2457.
20. Neumann S, Schuchardt K, Reske A, Reske A, Emmrich P, Paschke R. Lack of correlation for sodium iodide symporter mRNA and protein expression and analysis of sodium iodide symporter promoter methylation in benign cold thyroid nodules. Thyroid. 2004; 14:99-111.
21. Xing M, Usadel H, Cohen Y, et al. Methylation of the thyroidstimulating hormone receptor gene in epithelial thyroid tumors: a marker of malign ancy and a cause of gene silencing. Cancer Res. 2003;63:2316-2321.
22. Kondo T, Nakazawa T, Ma D, et al. Epigenetic silencing of TTF-1/NKX2-1 through DNA hypermethylation and histone H3 modulatio n in thyroid carcinomas. Lab Invest. 2009;89:791-799.
23. Riesco-Eizaguirre G, Rodrí guez I, De la Vieja A, et al. The BRAFV600E oncogene induces transforming growth factor-secretion leading to so dium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Res. 2009;69:8317-8325.
24. Hutter B, Paulsen M, Helms V. Identifying CpG islands by different computational techniques. Omics. 2009;13:153-164.
25. Herman JG, Graff JR, My öhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA. 1996;93:9821-9826.
26. Graham FL, van der Eb AJ. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973;52:456-467.
27. Nicola JP, Reyna-Neyra A, Carrasco N, Masini-RepisoAM.Dietary iodide controls its own absorption through post-transcriptional regulation of the intestinal Na-/I-symporter. J Physiol. 2012;590: 6013-6026.
28. Rodríguez-Paredes M,Esteller M Cancer epigenetics reaches mainstream oncology Nat Med. 2011 17 330-339.
29. Wang S, Dorsey TH, Terunuma A, Kittles RA, Ambs S, Kwabi-Ad do B. Relationship between tumor DNA methylation status and patient characteristics in African-American and European-American women with breast cancer. PLoS One. 2012;7:e37928.
30. Lou W, Krill D, D hir R, et al. Methylation of the CD44 metastasis suppressor gene in human prostate cancer. Cancer Res. 1999;59: 2329-2331.
31. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128: 683-692.
32. Xing M. Gene methylation in thyroid tumorigenesis. Endocrinology. 2007;148:948-953.
33. XingM,Tokumaru Y,WuG, WestraWB,Ladenson PW, Sidransky D. Hypermethylation of the Pendred syndrome gene SLC26A4 is an early event in thyroid tumorigenesis. Cancer Res. 2003;63:2312-2315.
34. Ohno M, Zannini M, Levy O, Carrasco N, di Lauro R. The paireddomain transcription factor Pax8 binds to the upstream enhancer of the rat sodium/iodide symporter gene and participates in both thyroid-specific and cycl ic-AMP-dependent transcription. Mol Cell Biol. 1999;19:2051-2060.
35. Ryu KY, Tong Q, Jhiang SM. Promoter characterization of the human Na-/I-symporter. J Clin Endocrinol Metab. 1998;83:3247-3251.
36. Wiench M, John S, Baek S, et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J. 2011;30:3028-3039.
37. Shore A, K aramitri A, Kemp P, Speakman JR, Lomax MA. Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue. Diabetologia. 2010;53:1164-1173.
38. Schmitt TL, Espinoza CR, Loos U. Characterization of a thyroidspecific and cyclic adenosine monophosphate-responsive enhancer far upstream from the human sodium iodide symporter gene. Thyroid. 2002;12:273-279.
39. Ong CT, Corces VG. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat Rev Genet. 2011;12: 283-293.
40. Morari EC, Marcello MA, Guilh en AC, et al. Use of sodium iodide symporter expression in differentiated thyroid carcinomas. Clin Endocrinol (Oxf). 2011;75:247-254.