Histone deacetylation of NIS promoter underlies BRAF V600E-promoted NIS silencing in thyroid cancer

Endocrine-Related Cancer

Volumn 21, Issue 2, 2014, Pages 161-173

  Zhang, Zongjing ^a,b   Liu, Dingxie ^a   Murugan, Avaniyapuram Kannan ^a   Liu, Zhimin ^b   Xing, Mingzhao ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

BRAF V600E mutation; Histone acetylation; Histone deacetylation; NIS gene; Radioiodine; Thyroid cancer

Indexed keywords

B RAF KINASE; HISTONE; LYSINE; SELUMETINIB; SODIUM IODIDE SYMPORTER; VEMURAFENIB; VORINOSTAT;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEACETYLATION; GENE MUTATION; GENE SILENCING; GENETIC TRANSFECTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; NONHUMAN; PROMOTER REGION; RAT; THYROID CANCER; THYROID CELL;

BRAF V600E MUTATION; HISTONE ACETYLATION; HISTONE DEACETYLATION; NIS GENE; RADIOIODINE; THYROID CANCER;

ACETYLATION; ANIMALS; CELL LINE; CELL LINE, TUMOR; GENE SILENCING; HISTONES; HUMANS; MUTATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS B-RAF; RATS; SYMPORTERS; THYROID NEOPLASMS;

EID: 84899844897     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-13-0399     Document Type: Article

References (34)

1. Barneda-Zahonero B & Parra M 2012 Histone deacetylases and cancer. Molecular Oncology 6 579-589. (doi:10.1016/j.molonc.2012.07.003)
2. Bjerling P, Silverstein RA, Thon G, Caudy A, Grewal S & Ekwall K 2002 Functional divergence between histone deacetylases in fission yeast by distinct cellular localization and in vivo specificity. Molecular and Cellular Biology 22 2170-2181. (doi:10.1128/MCB.22.7. 2170-2181.2002)
3. Chakravarty D, Santos E, Ryder M, Knauf JA, Liao XH, West BL, Bollag G, Kolesnick R, Thin TH, Rosen N et al. 2011 Small-molecule MAPK inhibitors restore radioiodine incorporation in mouse thyroid cancers with conditional BRAF activation. Journal of Clinical Investigation 121 4700-4711. (doi:10.1172/JCI46382)
4. Dhall A & Chatterjee C 2011 Chemical approaches to understand the language of histone modifications. ACS Chemical Biology 6 987-999. (doi:10.1021/cb200142c)
5. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G, Bonaldi T, Haydon C, Ropero S, Petrie K et al. 2005 Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nature Genetics 37 391-400. (doi:10.1038/ng1531)
6. Horikoshi M 2013 Histone acetylation: from code to web and router via intrinsically disordered regions. Current Pharmaceutical Design 19 5019-5042. (doi:10.2174/1381612811319280002)
7. Hou P, Liu D, Ji M, Liu Z, Engles JM, Wahl RL & Xing M 2009 Induction of thyroid gene expression and radioiodine uptake in melanoma cells: novel therapeutic implications. PLoS ONE 4 e6200. (doi:10.1371/journal.pone.0006200)
8. Hou P, Bojdani E & Xing M 2010 Induction of thyroid gene expression and radioiodine uptake in thyroid cancer cells by targeting major signaling pathways. Journal of Clinical Endocrinology and Metabolism 95 820-828. (doi:10.1210/jc.2009-1888)
9. Kim TH, Park YJ, Lim JA, Ahn HY, Lee EK, Lee YJ, Kim KW, Hahn SK, Youn YK, Kim KH et al. 2012 The association of the BRAF(V600E) mutation with prognostic factors and poor clinical outcome in papillary thyroid cancer: a meta-analysis. Cancer 118 1764-1773. (doi:10.1002/cncr.26500)
10. Kogai T, Taki K & Brent GA 2006 Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocrine-Related Cancer 13 797-826. (doi:10.1677/erc.1.01143)
11. Kuo MH, Brownell JE, Sobel RE, Ranalli TA, Cook RG, Edmondson DG, Roth SY & Allis CD 1996 Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383 269-272. (doi:10.1038/383269a0)
12. Li B, Carey M & Workman JL 2007 The role of chromatin during transcription. Cell 128 707-719. (doi:10.1016/j.cell.2007.01.015)
13. Liang G, Lin JC, Wei V, Yoo C, Cheng JC, Nguyen CT, Weisenberger DJ, Egger G, Takai D, Gonzales FA et al. 2004 Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. PNAS 101 7357-7362. (doi:10.1073/pnas.0401866101)
14. Liu D & Xing M 2008 Potent inhibition of thyroid cancer cells by the MEK inhibitor PD0325901 and its potentiation by suppression of the PI3K and NF-kB pathways. Thyroid 18 853-864. (doi:10.1089/thy.2007.0357)
15. Liu Z & Xing M 2012 Induction of sodium/iodide symporter (NIS) expression and radioiodine uptake in non-thyroid cancer cells. PLoS ONE 7 e31729. (doi:10.1371/journal.pone.0031729)
16. Liu D, Hu S, Hou P, Jiang D, Condouris S & Xing M 2007 Suppression of BRAF/MEK/MAP kinase pathway restores expression of iodide-metabolizing genes in thyroid cells expressing the V600E BRAF mutant. Clinical Cancer Research 13 1341-1349. (doi:10.1158/1078-0432. CCR-06-1753)
17. Momparler RL & Bovenzi V 2000 DNA methylation and cancer. Journal of Cellular Physiology 183 145-154. (doi:10.1002/(SICI) 1097-4652(200005)183:2!145: AID-JCP1O3.0.CO;2-V)
18. Pugliese M, Fortunati N, Germano A, Asioli S, Marano F, Palestini N, Frairia R, Boccuzzi G & Catalano MG 2013 Histone deacetylase inhibition affects sodium iodide symporter expression and induces (131)i cytotoxicity in anaplastic thyroid cancer cells. Thyroid 23 838-846. (doi:10.1089/thy.2012.0359)
19. Puppin C, D'Aurizio F, D'Elia AV, Cesaratto L, Tell G, Russo D, Filetti S, Ferretti E, Tosi E, Mattei T et al. 2005 Effects of histone acetylation on sodium iodide symporter promoter and expression of thyroid-specific transcription factors. Endocrinology 146 3967-3974. (doi:10.1210/en.2005-0128)
20. Puppin C, Passon N, Lavarone E, Di Loreto C, Frasca F, Vella V, Vigneri R & Damante G 2011 Levels of histone acetylation in thyroid tumors. Biochemical and Biophysical Research Communications 411 679-683. (doi:10.1016/j.bbrc.2011.06.182)
21. Puppin C, Passon N, Hershman J, Filetti S, Bulotta S, Celano M, Russo D & Giuseppe Damante G 2012 Cooperative effects of SAHA and VPA on NIS gene expression and proliferation of thyroid cancer cells. Journal of Molecular Endocrinology 48 217-227. (doi:10.1530/JME-11-0063)
22. Riesco-Eizaguirre G, Gutiérrez-Mart́inez P, Garćia-Cabezas MA, Nistal M & Santisteban P 2006 The oncogene BRAF V600E is associated with a high risk of recurrence and less differentiated papillary thyroid carcinoma due to the impairment of NaC/IK targeting to the membrane. Endocrine-Related Cancer 13 257-269. (doi:10.1677/erc.1.01119)
23. Ryu KY, Tong Q & Jhiang SM 1998 Promoter characterization of the human NaC/IK symporter. Journal of Clinical Endocrinology and Metabolism 83 3247-3251. (doi:10.1210/jc.83.9.3247)
24. Tong Q, Ryu KY & Jhiang SM 1997 Promoter characterization of the rat NaC/IK symporter gene. Biochemical and Biophysical Research Communications 239 34-41. (doi:10.1006/bbrc.1997.7432)
25. Vogelauer M, Wu J, Suka N & Grunstein M 2000 Global histone acetylation and deacetylation in yeast. Nature 408 495-498. (doi:10.1038/ 35044127)
26. Woo YH & Li WH 2012 Evolutionary conservation of histone modifications in mammals. Molecular Biology and Evolution 29 1757-1767. (doi:10.1093/molbev/mss022)
27. Xing M 2005 BRAF mutation in thyroid cancer. Endocrine-Related Cancer 12 245-262. (doi:10.1677/erc.1.0978)
28. Xing M 2007a BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocrine Reviews 28 742-762. (doi:10.1210/er.2007-0007)
29. Xing M 2007b Gene methylation in thyroid tumorigenesis. Endocrinology 148 948-953. (doi:10.1210/en.2006-0927)
30. Xing M 2013 Molecular pathogenesis and mechanisms of thyroid cancer. Nature Reviews. Cancer 13 184-199. (doi:10.1038/nrc3431)
31. Xing M, Westra WH, Tufano RP, Cohen Y, Rosenbaum E, Rhoden KJ, Carson KA, Vasko V, Larin A, Tallini G et al. 2005 BRAF mutation predicts a poorer clinical prognosis for papillary thyroid cancer. Journal of Clinical Endocrinology and Metabolism 90 6373-6379. (doi:10.1210/jc.2005-0987)
32. Xing M, Haugen BR & Schlumberger M 2013a Progress in molecular-based management of differentiated thyroid cancer. Lancet 381 1058-1069. (doi:10.1016/S0140-6736(13)60109-9)
33. Xing M, Alzahrani AS, Carson KA, Viola D, Elisei R, Bendlova B, Yip L, Mian C, Vianello F, Tuttle RM et al. 2013b Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. Journal of the American Medical Association 309 1493-1501. (doi:10.1001/jama.2013.3190)
34. Xu J & Hershman JM 2006 Histone deacetylase inhibitor depsipeptide represses nicotinamide N-methyltransferase and hepatocyte nuclear factor-1b gene expression in human papillary thyroid cancer cells. Thyroid 16 151-160. (doi:10.1089/thy.2006.16.151)