DNA methylation signatures identify biologically distinct thyroid cancer subtypes

Journal of Clinical Endocrinology and Metabolism

Volumn 98, Issue 7, 2013, Pages 2811-2821

  Rodriǵuez Rodero, Sandra ^a   Ferńandez, Agustín F ^a   Fernández Morera, Juan Luiś ^a   Castro Santos, Patricia ^a,e   Bayon, Gustavo F ^a   Ferrero, Cecilia ^a   Urdinguio, Rocio G ^a   Gonzalez Marquez, Rocío ^a   Suarez, Carlos ^a   Fernández Vega, Iván ^a   Forcelledo, Manuel Florentino Fresno ^a   Martińez Camblor, Pablo ^c   Mancikova, Veronika ^f,g   Castelblanco, Esmeralda ^h   Perez, Marco ⁱ   Marroń, Pablo Isidro ^b   Mendiola, Marta ^j   Hardisson, David ^k   Santisteban, Pilar ^l,m   Riesco Eizaguirre, Garcilaso ^k   Matiás Guiu, Xavier ^h   Carnero, Amancio ⁱ   Robledo, Mercedes ^f,g   Delgado Álvarez, Elías ^a,d   Meneńdez Torre, Edelmiro ^a   Fraga, Mario F ^a,n   more..

^a DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^b HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^c Oficina de Investigación Biosanitaria OIB de Asturias and Universidad Autonoma de Chile   (Spain)

^d UNIVERSITY OF OVIEDO   (Spain)

^e UNIVERSIDAD AUTÓNOMA DE CHILE   (Chile)

^f Centro Nacional de Investigaciones Oncológicas   (Spain)

^g CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^h HOSPITAL UNIVERSITARI ARNAU DE VILANOVA   (Spain)

ⁱ UNIVERSITY OF SEVILLE   (Spain)

^j HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^k HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^l INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^m UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

ⁿ CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR 54; HISTONE H3; NOTCH4 RECEPTOR; POLYCOMB REPRESSIVE COMPLEX 2;

ADAMTS8 GENE; ANAPLASTIC THYROID CANCER; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EMBRYO; GENE OVEREXPRESSION; HOXB4 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; KISS1R GENE; MAP17 GENE; MOLECULAR PATHOLOGY; ONCOGENE; ONCOGENE DPPA2; ONCOGENE INSL4; ONCOGENE TCL1B; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; THYROID CANCER; THYROID FOLLICULAR CARCINOMA; THYROID MEDULLARY CARCINOMA; THYROID PAPILLARY CARCINOMA; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; ZIC1 GENE;

ADENOCARCINOMA, FOLLICULAR; CARCINOMA; CARCINOMA, MEDULLARY; CARCINOMA, PAPILLARY; CELL LINE, TUMOR; COHORT STUDIES; DNA METHYLATION; DOWN-REGULATION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; THYROID GLAND; THYROID NEOPLASMS; TISSUE BANKS; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84879984996     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2012-3566     Document Type: Article

References (62)

1. Cohen EE. New approaches to thyroid cancer. Clin Adv Hematol Oncol. 2012;10:255-256.
2. DeVita VT, Samuel A, Wells J. Cancer of the endocrine system. In: Wilkins LW, ed. Principles and Practice of Oncology. 8th ed. Mexico City, Mexico: Wolters Kluwer Health Mexico; 2008
3. Boichard A, Croux L, Al Ghuzlan A, et al. Somatic RAS mutations occur in a large proportion of sporadic RET-negative medullary thyroid carcinomas and extend to a previously unidentified exon. J Clin Endocrinol Metab. 2012;97:E2031-E2035.
4. Li C, Lee KC, Schneider EB, Zeiger MA. BRAFV600E mutation and its association with clinicopathological features of papillary thyroid cancer: a meta-analysis. J Clin Endocrinol Metab. 2012;97:4559-4570.
5. Miyake Y, Aratake Y, Sakaguchi T, et al. Examination of CD26/DPPIV, p53, and PTEN expression in thyroid follicular adenoma. Diagn Cytopathol. 2012;40:1047-1053
6. Romei C, Elisei R. RET/PTC Translocations and Clinico-Pathological Features in Human Papillary Thyroid Carcinoma. Front Endocrinol (Lausanne). 2012;3:54.
7. A T, F S, G P, M B. Genetic Alterations in Medullary Thyroid Cancer: Diagnostic and Prognostic Markers. Curr Genom. 2011;12:618-625.
8. Smith JA, Fan CY, Zou C, Bodenner D, Kokoska MS. Methylation status of genes in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg. 2007;133:1006-1011. (Pubitemid 47607583)
9. -symporter gene methylation status. J Clin Endocrinol Metab. 1999;84:2449-2457.
10. Xing M, Usadel H, Cohen Y, et al. 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. (Pubitemid 36538643)
11. Stephen JK, Chitale D, Narra V, Chen KM, Sawhney R, Worsham MJ. DNA methylation in thyroid tumorigenesis. Cancers (Basel). 2011;3:1732-1743.
12. Anania MC, Sensi M, Radaelli E, et al. TIMP3 regulates migration, invasion and in vivo tumorigenicity of thyroid tumor cells. Oncogene. 2011;30:3011-3023.
13. Hu S, Liu D, Tufano RP, et al. Association of aberrant methylation of tumor suppressor genes with tumor aggressiveness and BRAF mutation in papillary thyroid cancer. Int J Cancer. 2006;119:2322-2329. (Pubitemid 44546951)
14. Xing M, Cohen Y, Mambo E, et al. Early occurrence of RASSF1A hypermethylation and its mutual exclusion with BRAF mutation in thyroid tumorigenesis. Cancer Res. 2004;64:1664-1668. (Pubitemid 38428687)
15. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
16. Giordano TJ, Kuick R, Thomas DG, et al. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene. 2005;24:6646-6656. (Pubitemid 41486795)
17. Lee TI, Jenner RG, Boyer LA, et al. Control of developmental regulators by polycomb in human embryonic stem cells. Cell. 2006;125:301-313. (Pubitemid 44313811)
18. Pan G, Tian S, Nie J, et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell. 2007;1:299-312. (Pubitemid 47355329)
19. Dunn JR, Reed JE, du Plessis DG, et al. Expression of ADAMTS-8, a secreted protease with antiangiogenic properties, is downregulated in brain tumours. Br J Cancer. 2006;94:1186-1193.
20. Fackler MJ, Umbricht CB, Williams D, et al. Genome-wide methylation analysis identifies genes specific to breast cancer hormone receptor status and risk of recurrence. Cancer Res. 2011;71:6195-6207.
21. Gan L, Chen S, Zhong J, et al. ZIC1 is downregulated through promoter hypermethylation, and functions as a tumor suppressor gene in colorectal cancer. PLoS One. 2011;6:e16916.
22. Ohtaki T, Shintani Y, Honda S, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature. 2001;411:613-617. (Pubitemid 32531412)
23. Brandt B, Kemming D, Packeisen J, et al. Expression of early placenta insulin-like growth factor in breast cancer cells provides an autocrine loop that predominantly enhances invasiveness and motility. Endocr Relat Cancer. 2005;12:823-837. (Pubitemid 41815778)
24. John T, Caballero OL, Svobodová SJ, et al. ECSA/DPPA2 is an embryo-cancer antigen that is coexpressed with cancer-testis antigens in non-small cell lung cancer. Clin Cancer Res. 2008;14:3291-3298.
25. Laine J, Künstle G, Obata T, Noguchi M. Differential regulation of Akt kinase isoforms by the members of the TCL1 oncogene family. J Biol Chem. 2002;277:3743-3751. (Pubitemid 34953249)
26. Xu K, Moghal N, Egan SE. Notch signaling in lung development and disease. Adv Exp Med Biol. 2012;727:89-98.
27. Guijarro MV, Leal JF, Blanco-Aparicio C, et al. MAP17 enhances the malignant behavior of tumor cells through ROS increase. Carcinogenesis. 2007;28:2096-2104. (Pubitemid 47543368)
28. Guijarro MV, Leal JF, Fominaya J, et al. MAP17 overexpression is a common characteristic of carcinomas. Carcinogenesis. 2007;28:1646-1652. (Pubitemid 47289025)
29. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8:286-298. (Pubitemid 46439286)
30. Calvisi DF, Ladu S, Gorden A, et al. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J Clin Invest. 2007;117:2713-2722. (Pubitemid 47494371)
31. Davidsson J, Lilljebjörn H, Andersson A, et al. The DNA methylome of pediatric acute lymphoblastic leukemia. Hum Mol Genet. 2009;18:4054-4065.
32. Omura N, Li CP, Li A, et al. Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol Ther. 2008;7:1146-1156.
33. Eze OP, Starker LF, Carling T. The role of epigenetic alterations in papillary thyroid carcinogenesis. J Thyroid Res. 2011;2011:895470.
34. Hou P, Ji M, Xing M. Association of PTEN gene methylation with genetic alterations in the phosphatidylinositol 3-kinase/AKT signaling pathway in thyroid tumors. Cancer. 2008;113:2440-2447.
35. Ishida E, Nakamura M, Shimada K, et al. DNA hypermethylation status of multiple genes in papillary thyroid carcinomas. Pathobiology. 2007;74:344-352. (Pubitemid 350273706)
36. Fernandez AF, Assenov Y, Martin-Subero JI, et al. A DNA methylation fingerprint of 1628 human samples. Genome Res. 2012;22:407-419.
37. Maldonado-Saldivia J, van den Bergen J, Krouskos M, et al. Dppa2 and Dppa4 are closely linked SAP motif genes restricted to pluripotent cells and the germ line. Stem Cells. 2007;25:19-28. (Pubitemid 46052971)
38. DeSmet C, Loriot A. DNAhypomethylation and activation of germline-specific genes in cancer. Adv Exp Med Biol. 2013;754:149- 166.
39. Neumann O, Kesselmeier M, Geffers R, et al. Methylome analysis and integrative profiling of human HCCs identify novel protumorigenic factors. Hepatology. 2012;56:1817-1827
40. Shen J, Wang S, Zhang YJ, et al. Genome-wide DNA methylation profiles in hepatocellular carcinoma. Hepatology. 2012;55:1799-1808.
41. Calvanese V, Fernández AF, Urdinguio RG, et al. A promoter DNA demethylation landscape of human hematopoietic differentiation. Nucleic Acids Res. 2011;40:116-131.
42. Gonzalez-Paz N, Chng WJ, McClure RF, et al. Tumor suppressor p16 methylation in multiple myeloma: biological and clinical implications. Blood. 2007;109:1228-1232. (Pubitemid 46220672)
43. Klug M, Heinz S, Gebhard C, et al. Active DNA demethylation in human postmitotic cells correlates with activating histone modifications, but not transcription levels. Genome Biol. 2010;11:R63.
44. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet. 2012;13:679-692.
45. Helman E, Naxerova K, Kohane IS. DNA hypermethylation in lung cancer is targeted at differentiation-associated genes. Oncogene. 2012;31:1181-1188.
46. Shen X, He Z, Li H, et al. Distinct functional patterns of gene promoter hypomethylation and hypermethylation in cancer genomes. PLoS One. 2012;7:e44822.
47. Ohm JE, Baylin SB. Stem cell chromatin patterns: an instructive mechanism for DNA hypermethylation? Cell Cycle. 2007;6:1040-1043. (Pubitemid 46708576)
48. Schlesinger Y, Straussman R, Keshet I, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet. 2007;39:232-236. (Pubitemid 46184355)
49. Widschwendter M, Fiegl H, Egle D, et al. Epigenetic stem cell signature in cancer. Nat Genet. 2007;39:157-158. (Pubitemid 46184343)
50. Boltze C, Zack S, Quednow C, Bettge S, Roessner A, Schneider-Stock R. Hypermethylation of the CDKN2/p16INK4A promotor in thyroid carcinogenesis. Pathol Res Pract. 2003;199:399-404. (Pubitemid 36974825)
51. Lam AK, Lo CY, Leung P, Lang BH, Chan WF, Luk JM. Clinicopathological roles of alterations of tumor suppressor gene p16 in papillary thyroid carcinoma. Ann Surg Oncol. 2007;14:1772-1779. (Pubitemid 46790989)
52. Nakamura N, Carney JA, Jin L, et al. RASSF1A and NORE1A methylation and BRAFV600E mutations in thyroid tumors. Lab Invest. 2005;85:1065-1075. (Pubitemid 43073981)
53. Zuo H, Gandhi M, Edreira MM, et al. Downregulation of Rap1GAP through epigenetic silencing and loss of heterozygosity promotes invasion and progression of thyroid tumors. Cancer Res. 2010;70:1389-1397.
54. Alvarez-Nuñez F, Bussaglia E, Mauricio D, et al. PTEN promoter methylation in sporadic thyroid carcinomas. Thyroid. 2006;16:17-23. (Pubitemid 43346499)
55. Ringel MD, Hardy E, Bernet VJ, et al. Metastin receptor is overexpressed in papillary thyroid cancer and activates MAP kinase in thyroid cancer cells. J Clin Endocrinol Metab. 2002;87:2399.
56. Gray S, Pandha HS, Michael A, Middleton G, Morgan R. HOX genes in pancreatic development and cancer. JOP. 2011;12:216-219.
57. Dunn JR, Panutsopulos D, Shaw MW, Het al. METH-2 silencing and promoter hypermethylation in NSCLC. Br J Cancer. 2004;91:1149-1154. (Pubitemid 39336255)
58. Strathdee G, Holyoake TL, Sim A, et al. Inactivation of HOXA genes by hypermethylation in myeloid and lymphoid malignancy is frequent and associated with poor prognosis. Clin Cancer Res. 2007;13:5048-5055. (Pubitemid 47502069)
59. Geers C, Colin IM, Gérard AC. Delta-like 4/Notch pathway is differentially regulated in benign and malignant thyroid tissues. Thyroid. 2011;21:1323-1330.
60. Ding LC, She L, Zheng DL, et al. Notch-4 contributes to the metastasis of salivary adenoid cystic carcinoma. Oncol Rep. 2010;24:363-368.
61. Yuille MR, Condie A, Stone EM, et al. TCL1 is activated by chromosomal rearrangement or by hypomethylation. Genes Chromosomes Cancer. 2001;30:336-341. (Pubitemid 32216324)
62. Bellet D, Lavaissiere L, Mock P, et al. Identification of pro-EPIL and EPIL peptides translated from insulin-like 4 (INSL4) mRNA in human placenta. J Clin Endocrinol Metab. 1997;82:3169-3172. (Pubitemid 27385694)