Hypermethylation, but not LOH, is associated with the low expression of MT1G and CRABP1 in papillary thyroid carcinoma

International Journal of Cancer

Volumn 104, Issue 6, 2003, Pages 735-744

  Huang, Ying ^a   De la Chapelle, Albert ^a   Pellegata, Natalia S ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

DNA methylation; DNA microarray; Loss of heterozygosity; Papillary thyroid cancer; Tumor suppressor gene

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA METHYLTRANSFERASE; GENOMIC DNA; TRICHOSTATIN A;

ADULT; AGED; ARTICLE; CANCER CELL; CLINICAL ARTICLE; CPG ISLAND; CRABP1 GENE; DNA METHYLATION; DNA MICROARRAY; FEMALE; GENE; GENE EXPRESSION; HETEROZYGOSITY LOSS; HUMAN; HUMAN TISSUE; MALE; MT1G GENE; NUCLEOTIDE SEQUENCE; ONCOGENE RET; PRIORITY JOURNAL; THYROID CARCINOMA; THYROID PAPILLARY CARCINOMA; TUMOR SUPPRESSOR GENE;

ADENOCARCINOMA, PAPILLARY; ADULT; AGED; AZACITIDINE; BASE SEQUENCE; CPG ISLANDS; DNA METHYLATION; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HUMANS; HYDROXAMIC ACIDS; LOSS OF HETEROZYGOSITY; MALE; METALLOTHIONEIN; MICROSATELLITE REPEATS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; O(6)-METHYLGUANINE-DNA METHYLTRANSFERASE; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); RECEPTORS, RETINOIC ACID; THYROID NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 0037431507     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.11006     Document Type: Article

References (50)

1. Mazzaferri EL. Thyroid carcinoma: papillary and follicular. In: Mazzaferri EL, Samaan N, eds. Endocrine tumors Cambridge, England: Blackwell Scientific Publications Inc., 1993. 278.
2. Tallini G, Asa SL. RET oncogene activation in papillary thyroid carcinoma. Adv Anat Pathol 2001;8:345-54.
3. Moretti F, Nanni S, Pontecorvi A. Molecular pathogenesis of thyroid nodules and cancer. Baillieres Best Pract Res Clin Endocrinol Metab 2000;14:517-39.
4. Jhiang SM. The RET proto-oncogene in human cancers. Oncogene 2000;19:5590-7.
5. Gillespie JW, Nasir A, Kaiser HE. Loss of heterozygosity in papillary and follicular thyroid carcinoma: a mini review. In Vivo 2000;14: 139-40.
6. Ward LS, Brenta G, Medvedovic M, Fagin JA. Studies of allelic loss in thyroid tumors reveal major differences in chromosomal instability between papillary and follicular carcinomas. J Clin Endocrinol Metab 1998;83:525-30.
7. Oriola J, Halperin I, Mallofre C, Muntane J, Angel M, Rivera-Fillat F. Screening of selected genomic areas potentially involved in thyroid neoplasms. Eur J Cancer 2001;37:2470-4.
8. Califano JA, Johns MM, 3rd, Westra WH, Lango MN, Eisele D, Saji M, Zeiger MA, Udelsman R, Koch WM, Sidransky D. An allelotype of papillary thyroid cancer. Int J Cancer 1996;69:442-4.
9. Costello JF, Plass C. Methylation matters. J Med Genet 2001;38:285-303.
10. Matsuo K, Tang SH, Zeki K, Gutman RA, Fagin JA. Aberrant deoxyribonucleic acid methylation in human thyroid tumors. J Clin Endocrinol Metab 1993;77:991-5.
11. Venkataraman GM, Yatin M, Marcinek R, Ain KB. Restoration of iodide uptake in dedifferentiated thyroid carcinoma: relationship to human Na+/I-symporter gene methylation status. J Clin Endocrinol Metab 1999;84:2449-57.
12. Graff JR, Greenberg VE, Herman JG, Westra WH, Boghaert ER. Ain KB, Saji M, Zeiger MA, Zimmer SG, Baylin SB. Distinct patterns of E-cadherin CpG island methylation in papillary, follicular, Hurthle's cell, and poorly differentiated human thyroid carcinoma. Cancer Res 1998;58:2063-6.
13. Rocha AS, Soares P, Seruca R, Maximo V, Matias-Guiu X. Cameselle-Teijeiro J, Sobrinho-Simoes M. Abnormalities of the E-cadherin/catenin adhesion complex in classical papillary thyroid carcinoma and in its diffuse sclerosing variant. J Pathol 2001;194:358-66.
14. Elisei R, Shiohara M, Koeffler HP, Fagin JA. Genetic and epigenetic alterations of the cyclin-dependent kinase inhibitors p15INK4b and p16INK4a in human thyroid carcinoma cell lines and primary thyroid carcinomas. Cancer 1998;83:2185-93.
15. Huang Y, Prasad M, Lemon WJ, Hampel H, Wright FA, Kornacker K, LiVolsi V, Frankel W, Kloos RT, Eng C, Pellegata NS, de la Chapelle A. Gene expression in papillary thyroid carcinoma reveals highly consistent profiles. Proc Natl Acad Sci USA 2001;98:15044-9.
16. Fagin JA, Matsuo K, Karmakar A, Chen DL, Tang SH, Koeffler HP. High prevalence of mutations of the p53 gene in poorly differentiated human thyroid carcinomas. J Clin Invest 1993;91:179-84.
17. Jones CJ, Shaw JJ, Wyllie FS, Gaillard N, Schlumberger M, Wynford-Thomas D. High frequency deletion of the tumour suppressor gene P16INK4a (MTS1) in human thyroid cancer cell lines. Mol Cell Endocrinol 1996;116:115-9.
18. Mullenbach R, Lagoda PJ, Welter C. An efficient salt-chloroform extraction of DNA from blood and tissues. Trends Genet 1989;5:391.
19. Ge K, Minhas F, Duhadaway J, Mao NC, Wilson D, Buccafusca R, Sakamuro D, Nelson P, Malkowicz SB, Tomaszewski J, Prendergast GC. Loss of heterozygosity and tumor suppressor activity of Bin1 in prostate carcinoma. Int J Cancer 2000;86:155-61.
20. Canzian F, Salovaara R, Hemminki A, Kristo P, Chadwick RB, Aaltonen LA, de la Chapelle A. Semiautomated assessment of loss of heterozygosity and replication error in tumors. Cancer Res 1996;56: 3331-7.
21. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 1997;25:2532-4.
22. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 1992;89:1827-31.
23. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996;93:9821-6.
24. Simpson DJ, Hibberts NA, McNicol AM, Clayton RN, Farrell WE. Loss of pRb expression in pituitary adenomas is associated with methylation of the RB1 CpG island. Cancer Res 2000;60:1211-6.
25. Kitamura Y, Shimizu K, Tanaka S, Ito K, Emi M. Association of allelic loss on 1q, 4p, 7q, 9p, 9q, and 16q with postoperative death in papillary thyroid carcinoma. Clin Cancer Res 2000;6:1819-25.
26. Smit JW, Van Zelderen-Bhola S, Merx R, De Leeuw W, Wessels H, Vink R, Morreau H. A novel chromosomal translocation t(3;5)(q12; p15.3) and loss of heterozygosity on chromosome 22 in a multifocal follicular variant of papillary thyroid carcinoma presenting with skin metastases. Clin Endocrinol 2001;55:543-8.
27. McKay JD, Lesueur F, Jonard L, Pastore A, Williamson J, Hoffman L, Burgess J, Duffield A, Papotti M, Stark M, Sobol H, Maes B, et al. Localization of a susceptibility gene for familial nonmedullary thyroid carcinoma to chromosome 2q21. Am J Hum Genet 2001;69:440-6.
28. Canzian F, Amati P, Harach HR, Kraimps JL, Lesueur F, Barbier J, Levillain P, Romeo G, Bonneau D. A gene predisposing to familial thyroid tumors with cell oxyphilia maps to chromosome 19p13.2. Am J Hum Genet 1998;63:1743-8.
29. Yang X, Shen P, Yao K, Mi Z, Liu S, Zhang H, Wang D, Liu C, Liu H. High frequency loss of heterozygosity in the region of the DBH locus in bladder cancer. Chin Med J 2000;113:117-9.
30. Li W, Wang D, Wang X, Hao X, Wu M. [Loss of heterozygosity microsatellite DNA on chromosome loci 3, 5, 7, 9 and 18 in human pancreatic cancer]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 1998;15: 274-7.
31. Takita J, Hayashi Y, Kohno T, Yamaguchi N, Hanada R, Yamamoto K, Yokota J. Deletion map of chromosome 9 and p16 (CDKN2A) gene alterations in neuroblastoma. Cancer Res 1997;57:907-12.
32. Hedvat CV, Irving SG. The isolation and characterization of MINOR, a novel mitogen-inducible nuclear orphan receptor. Mol Endocrinol 1995;9:1692-700.
33. Foster R, Jahroudi N, Varshney U, Gedamu L. Structure and expression of the human metallothionein-IG gene. Differential promoter activity of two linked metallothionein-I genes in response to heavy metals. J Biol Chem 1988;263:11528-35.
34. Coyle P, Philcox JC, Carey LC, Rofe AM. Metallothionein: the multipurpose protein. Cell Mol Life Sci 2002;59:627-47.
35. Nartey N, Cherian MG, Banerjee D. Immunohistochemical localization of metallothionein in human thyroid tumors. Am J Pathol 1987; 129:177-82.
36. Deng DX, Chakrabarti S, Waalkes MP, Cherian MG. Metallothionein and apoptosis in primary human hepatocellular carcinoma and metastatic adenocarcinoma. Histopathology 1998;32:340-7.
37. Stenram U, Ohlsson B, Tranberg KG. Immunohistochemical expression of metallothionein in resected hepatic primary tumors and colorectal carcinoma metastases. Apmis 1999;107:420-4.
38. Ghoshal K, Majumder S, Li Z, Dong X, Jacob ST. Suppression of metallothionein gene expression in a rat hepatoma because of promoter-specific DNA methylation. J Biol Chem 2000;275:539-47.
39. Waalkes MP, Diwan BA, Rehm S, Ward JM, Moussa M, Cherian MG, Goyer RA. Down-regulation of metallothionein expression in human and murine hepatocellular tumors: association with the tumor-necrotizing and antineoplastic effects of cadmium in mice. J Pharmacol Exp Ther 1996;277:1026-33.
40. Wei LN, Lee CH. Demethylation in the 5′-flanking region of mouse cellular retinoic acid binding protein-I gene is associated with its high level of expression in mouse embryos and facilitates its induction by retinoic acid in P19 embryonal carcinoma cells. Dev Dyn 1994;201: 1-10.
41. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987;196:261-82.
42. Donovan M, Olofsson B, Gustafson AL, Dencker L, Eriksson U. The cellular retinoic acid binding proteins. J Steroid Biochem Mol Biol 1995;53:459-65.
43. Boylan JF, Gudas LJ. The level of CRABP-I expression influences the amounts and types of all-trans-retinoic acid metabolites in F9 teratocarcinoma stem cells. J Biol Chem 1992;267:21486-91.
44. Anwar F, Emond MJ, Schmidt RA, Hwang HC, Bronner MP. Retinoblastoma expression in thyroid neoplasms. Mod Pathol 2000;13: 562-9.
45. Soda G, Antonaci A, Bosco D, Nardoni S, Melis M. Expression of bcl-2, c-erbB-2, p53, and p21 (waf1-cip1) protein in thyroid carcinomas. J Exp Clin Cancer Res 1999;18:363-7.
46. Zou M, Shi Y, Farid NR, al-Sedairy ST, Paterson MC. FHIT gene abnormalities in both benign and malignant thyroid tumours. Eur J Cancer 1999;35:467-72.
47. Del Sal G, Collavin L, Ruaro ME, Edomi P, Saccone S, Valle GD, Schneider C. Structure, function, and chromosome mapping of the growth-suppressing human homologue of the murine gas1 gene. Proc Natl Acad Sci U S A 1994;91:1848-52.
48. Unoki M, Nakamura Y. Growth-suppressive effects of BPOZ and EGR2, two genes involved in the PTEN signaling pathway. Oncogene 2001;20:4457-65.
49. Nagatake M, Osada H, Kondo M, Uchida K, Nishio M, Shimokata K, Takahashi T, Takahashi T. Aberrant hypermethylation at the bcl-2 locus at 18q21 in human lung cancers. Cancer Res 1996;56:1886-91.
50. Zochbauer-Muller S, Fong KM, Maitra A, Lam S, Geradts J, Ashfaq R, Virmani AK, Milchgrub S, Gazdar AF, Minna JD. 5′ CpG island methylation of the FHIT gene is correlated with loss of gene expression in lung and breast cancer. Cancer Res 2001;61:3581-5.