DOI QR코드

DOI QR Code

Recent Progress of Genome Study for Anaplastic Thyroid Cancer

  • Lee, Jieun (Cancer Genomics Branch, Research Institute, National Cancer Center) ;
  • Hwang, Jung-Ah (Cancer Genomics Branch, Research Institute, National Cancer Center) ;
  • Lee, Eun Kyung (Center for Thyroid Cancer, National Cancer Center)
  • Received : 2013.05.01
  • Accepted : 2013.05.21
  • Published : 2013.06.30

Abstract

Anaplastic thyroid cancer (ATC) belongs to the most malignant and rapidly progressive human thyroid cancers and its prognosis is very poor. Also, it shows high resistance to cancer treatments, so that effective treatment for ATC has not been found to date, and virtually all patients terminate their life rapidly after diagnosis. Although targeted treatment of genetic alterations has emerged as an extremely promising approach to human cancers, such as BRAF in metastatic melanoma, it remains unclear that how commonly genomic alterations are influenced in ATC tumorigenesis. In recent years, genome wide approaches have been exploited to find genetic alterations associated with complex diseases, including cancer. Here, we reviewed the comprehensive genetic alterations in ATC and recent approaches in the context of identifying genomic alterations associated with ATC. Since surprisingly few reports have been published on the genome wide study of ATC, this review puts emphasis on the urgent needs of genomic research for the prevention and treatment of ATC.

Keywords

References

  1. Kilfoy BA, Zheng T, Holford TR, Han X, Ward MH, Sjodin A, et al. International patterns and trends in thyroid cancer incidence, 1973-2002. Cancer Causes Control 2009;20:525-531. https://doi.org/10.1007/s10552-008-9260-4
  2. Kondo T, Ezzat S, Asa SL. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 2006;6:292-306. https://doi.org/10.1038/nrc1836
  3. Xing M. Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer 2013;13:184-199. https://doi.org/10.1038/nrc3431
  4. Sherman SI. Thyroid carcinoma. Lancet 2003;361:501-511. https://doi.org/10.1016/S0140-6736(03)12488-9
  5. Nix PA, Nicolaides A, Coatesworth AP. Thyroid cancer review 3: management of medullary and undifferentiated thyroid cancer. Int J Clin Pract 2006;60:80-84.
  6. Ain KB. Anaplastic thyroid carcinoma: behavior, biology, and therapeutic approaches. Thyroid 1998;8:715-726. https://doi.org/10.1089/thy.1998.8.715
  7. Giuffrida D, Gharib H. Anaplastic thyroid carcinoma: current diagnosis and treatment. Ann Oncol 2000;11:1083-1089. https://doi.org/10.1023/A:1008322002520
  8. Smallridge RC, Marlow LA, Copland JA. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr Relat Cancer 2009;16:17-44.
  9. Murugan AK, Bojdani E, Xing M. Identification and functional characterization of isocitrate dehydrogenase 1 (IDH1) mutations in thyroid cancer. Biochem Biophys Res Commun 2010; 393:555-559. https://doi.org/10.1016/j.bbrc.2010.02.095
  10. Murugan AK, Xing M. Anaplastic thyroid cancers harbor novel oncogenic mutations of the ALK gene. Cancer Res 2011; 71:4403-4411. https://doi.org/10.1158/0008-5472.CAN-10-4041
  11. Liu Z, Hou P, Ji M, Guan H, Studeman K, Jensen K, et al. Highly prevalent genetic alterations in receptor tyrosine kinases and phosphatidylinositol 3-kinase/akt and mitogen-activated protein kinase pathways in anaplastic and follicular thyroid cancers. J Clin Endocrinol Metab 2008;93:3106-3116. https://doi.org/10.1210/jc.2008-0273
  12. Hemmer S, Wasenius VM, Knuutila S, Franssila K, Joensuu H. DNA copy number changes in thyroid carcinoma. Am J Pathol 1999;154:1539-1547. https://doi.org/10.1016/S0002-9440(10)65407-7
  13. Wreesmann VB, Ghossein RA, Patel SG, Harris CP, Schnaser EA, Shaha AR, et al. Genome-wide appraisal of thyroid cancer progression. Am J Pathol 2002;161:1549-1556. https://doi.org/10.1016/S0002-9440(10)64433-1
  14. Xing M. BRAF mutation in thyroid cancer. Endocr Relat Cancer 2005;12:245-262. https://doi.org/10.1677/erc.1.0978
  15. Fukushima T, Suzuki S, Mashiko M, Ohtake T, Endo Y, Takebayashi Y, et al. BRAF mutations in papillary carcinomas of the thyroid. Oncogene 2003;22:6455-6457. https://doi.org/10.1038/sj.onc.1206739
  16. Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA. High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res 2003;63:1454-1457.
  17. Soares P, Trovisco V, Rocha AS, Lima J, Castro P, Preto A, et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 2003; 22:4578-4580. https://doi.org/10.1038/sj.onc.1206706
  18. Xu X, Quiros RM, Gattuso P, Ain KB, Prinz RA. High prevalence of BRAF gene mutation in papillary thyroid carcinomas and thyroid tumor cell lines. Cancer Res 2003;63:4561-4567.
  19. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-954. https://doi.org/10.1038/nature00766
  20. Xing M, Westra WH, Tufano RP, Cohen Y, Rosenbaum E, Rhoden KJ, et al. BRAF mutation predicts a poorer clinical prognosis for papillary thyroid cancer. J Clin Endocrinol Metab 2005;90:6373-6379. https://doi.org/10.1210/jc.2005-0987
  21. Xing M. Prognostic utility of BRAF mutation in papillary thyroid cancer. Mol Cell Endocrinol 2010;321:86-93. https://doi.org/10.1016/j.mce.2009.10.012
  22. Donghi R, Longoni A, Pilotti S, Michieli P, Della Porta G, Pierotti MA. Gene p53 mutations are restricted to poorly differentiated and undifferentiated carcinomas of the thyroid gland. J Clin Invest 1993;91:1753-1760. https://doi.org/10.1172/JCI116385
  23. 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: 179-184. https://doi.org/10.1172/JCI116168
  24. Quiros RM, Ding HG, Gattuso P, Prinz RA, Xu X. Evidence that one subset of anaplastic thyroid carcinomas are derived from papillary carcinomas due to BRAF and p53 mutations. Cancer 2005;103:2261-2268. https://doi.org/10.1002/cncr.21073
  25. Capella G, Matias-Guiu X, Ampudia X, de Leiva A, Perucho M, Prat J. Ras oncogene mutations in thyroid tumors: polymerase chain reaction-restriction-fragment-length polymorphism analysis from paraffin-embedded tissues. Diagn Mol Pathol 1996;5:45-52. https://doi.org/10.1097/00019606-199603000-00008
  26. Garcia-Rostan G, Zhao H, Camp RL, Pollan M, Herrero A, Pardo J, et al. Ras mutations are associated with aggressive tumor phenotypes and poor prognosis in thyroid cancer. J Clin Oncol 2003;21:3226-3235. https://doi.org/10.1200/JCO.2003.10.130
  27. Nikiforova MN, Nikiforov YE. Molecular genetics of thyroid cancer: implications for diagnosis, treatment and prognosis. Expert Rev Mol Diagn 2008;8:83-95. https://doi.org/10.1586/14737159.8.1.83
  28. Crespo P, Leon J. Ras proteins in the control of the cell cycle and cell differentiation. Cell Mol Life Sci 2000;57:1613-1636. https://doi.org/10.1007/PL00000645
  29. Luo J, Manning BD, Cantley LC. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 2003;4:257-262. https://doi.org/10.1016/S1535-6108(03)00248-4
  30. Garcia-Rostan G, Costa AM, Pereira-Castro I, Salvatore G, Hernandez R, Hermsem MJ, et al. Mutation of the PIK3CA gene in anaplastic thyroid cancer. Cancer Res 2005;65:10199- 10207. https://doi.org/10.1158/0008-5472.CAN-04-4259
  31. Garcia-Rostan G, Camp RL, Herrero A, Carcangiu ML, Rimm DL, Tallini G. Beta-catenin dysregulation in thyroid neoplasms: down-regulation, aberrant nuclear expression, and CTNNB1 exon 3 mutations are markers for aggressive tumor phenotypes and poor prognosis. Am J Pathol 2001;158: 987-996. https://doi.org/10.1016/S0002-9440(10)64045-X
  32. Garcia-Rostan G, Tallini G, Herrero A, D'Aquila TG, Carcangiu ML, Rimm DL. Frequent mutation and nuclear localization of beta-catenin in anaplastic thyroid carcinoma. Cancer Res 1999;59:1811-1815.
  33. Kurihara T, Ikeda S, Ishizaki Y, Fujimori M, Tokumoto N, Hirata Y, et al. Immunohistochemical and sequencing analyses of the Wnt signaling components in Japanese anaplastic thyroid cancers. Thyroid 2004;14:1020-1029. https://doi.org/10.1089/thy.2004.14.1020
  34. Hemerly JP, Bastos AU, Cerutti JM. Identification of several novel non-p.R132 IDH1 variants in thyroid carcinomas. Eur J Endocrinol 2010;163:747-755. https://doi.org/10.1530/EJE-10-0473
  35. Morris SW, Kirstein MN, Valentine MB, Dittmer KG, Shapiro DN, Saltman DL, et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 1994;263:1281-1284. https://doi.org/10.1126/science.8122112
  36. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007;448: 561-566. https://doi.org/10.1038/nature05945
  37. Ma Z, Hill DA, Collins MH, Morris SW, Sumegi J, Zhou M, et al. Fusion of ALK to the Ran-binding protein 2 (RANBP2) gene in inflammatory myofibroblastic tumor. Genes Chromosomes Cancer 2003;37:98-105. https://doi.org/10.1002/gcc.10177
  38. Lange K, Uckert W, Blankenstein T, Nadrowitz R, Bittner C, Renauld JC, et al. Overexpression of NPM-ALK induces different types of malignant lymphomas in IL-9 transgenic mice. Oncogene 2003;22:517-527. https://doi.org/10.1038/sj.onc.1206076
  39. Wellmann A, Doseeva V, Butscher W, Raffeld M, Fukushima P, Stetler-Stevenson M, et al. The activated anaplastic lymphoma kinase increases cellular proliferation and oncogene up-regulation in rat 1a fibroblasts. FASEB J 1997;11:965-972.
  40. Rodrigues RF, Roque L, Rosa-Santos J, Cid O, Soares J. Chromosomal imbalances associated with anaplastic transformation of follicular thyroid carcinomas. Br J Cancer 2004; 90:492-496. https://doi.org/10.1038/sj.bjc.6601530
  41. Kitamura Y, Shimizu K, Tanaka S, Ito K, Emi M. Allelotyping of anaplastic thyroid carcinoma: frequent allelic losses on 1q, 9p, 11, 17, 19p, and 22q. Genes Chromosomes Cancer 2000;27: 244-251. https://doi.org/10.1002/(SICI)1098-2264(200003)27:3<244::AID-GCC4>3.0.CO;2-7
  42. Bond JA, Wyllie FS, Rowson J, Radulescu A, Wynford-Thomas D. In vitro reconstruction of tumour initiation in a human epithelium. Oncogene 1994;9:281-290.
  43. Hou P, Liu D, Shan Y, Hu S, Studeman K, Condouris S, et al. Genetic alterations and their relationship in the phosphatidylinositol 3-kinase/Akt pathway in thyroid cancer. Clin Cancer Res 2007;13:1161-1170. https://doi.org/10.1158/1078-0432.CCR-06-1125
  44. Marotta V, Guerra A, Sapio MR, Vitale M. RET/PTC rearrangement in benign and malignant thyroid diseases: a clinical standpoint. Eur J Endocrinol 2011;165:499-507. https://doi.org/10.1530/EJE-11-0499
  45. Onda M, Emi M, Yoshida A, Miyamoto S, Akaishi J, Asaka S, et al. Comprehensive gene expression profiling of anaplastic thyroid cancers with cDNA microarray of 25 344 genes. Endocr Relat Cancer 2004;11:843-854. https://doi.org/10.1677/erc.1.00818
  46. Passon N, Puppin C, Lavarone E, Bregant E, Franzoni A, Hershman JM, et al. Cyclic AMP-response element modulator inhibits the promoter activity of the sodium iodide symporter gene in thyroid cancer cells. Thyroid 2012;22:487-493. https://doi.org/10.1089/thy.2011.0360
  47. Montero-Conde C, Martin-Campos JM, Lerma E, Gimenez G, Martinez-Guitarte JL, Combalia N, et al. Molecular profiling related to poor prognosis in thyroid carcinoma. Combining gene expression data and biological information. Oncogene 2008;27:1554-1561. https://doi.org/10.1038/sj.onc.1210792
  48. Pallante P, Federico A, Berlingieri MT, Bianco M, Ferraro A, Forzati F, et al. Loss of the CBX7 gene expression correlates with a highly malignant phenotype in thyroid cancer. Cancer Res 2008;68:6770-6778. https://doi.org/10.1158/0008-5472.CAN-08-0695
  49. Salvatore G, Nappi TC, Salerno P, Jiang Y, Garbi C, Ugolini C, et al. A cell proliferation and chromosomal instability signature in anaplastic thyroid carcinoma. Cancer Res 2007; 67:10148-10158. https://doi.org/10.1158/0008-5472.CAN-07-1887
  50. Akaishi J, Onda M, Okamoto J, Miyamoto S, Nagahama M, Ito K, et al. Down-regulation of an inhibitor of cell growth, transmembrane protein 34 (TMEM34), in anaplastic thyroid cancer. J Cancer Res Clin Oncol 2007;133:213-218. https://doi.org/10.1007/s00432-006-0159-8
  51. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349: 2042-2054. https://doi.org/10.1056/NEJMra023075
  52. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;3:415-428.
  53. Hou P, Liu D, Xing M. Genome-wide alterations in gene methylation by the BRAF V600E mutation in papillary thyroid cancer cells. Endocr Relat Cancer 2011;18:687-697. https://doi.org/10.1530/ERC-11-0212
  54. Schagdarsurengin U, Gimm O, Dralle H, Hoang-Vu C, Dammann R. CpG island methylation of tumor-related promoters occurs preferentially in undifferentiated carcinoma. Thyroid 2006;16:633-642. https://doi.org/10.1089/thy.2006.16.633
  55. 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. https://doi.org/10.1002/cncr.23869
  56. Bruni P, Boccia A, Baldassarre G, Trapasso F, Santoro M, Chiappetta G, et al. PTEN expression is reduced in a subset of sporadic thyroid carcinomas: evidence that PTEN-growth suppressing activity in thyroid cancer cells mediated by p27kip1. Oncogene 2000;19:3146-3155. https://doi.org/10.1038/sj.onc.1203633
  57. Frisk T, Foukakis T, Dwight T, Lundberg J, Hoog A, Wallin G, et al. Silencing of the PTEN tumor-suppressor gene in anaplastic thyroid cancer. Genes Chromosomes Cancer 2002;35: 74-80. https://doi.org/10.1002/gcc.10098
  58. Visone R, Pallante P, Vecchione A, Cirombella R, Ferracin M, Ferraro A, et al. Specific microRNAs are downregulated in human thyroid anaplastic carcinomas. Oncogene 2007;26:7590- 7595. https://doi.org/10.1038/sj.onc.1210564
  59. Berlingieri MT, Pierantoni GM, Giancotti V, Santoro M, Fusco A. Thyroid cell transformation requires the expression of the HMGA1 proteins. Oncogene 2002;21:2971-2980. https://doi.org/10.1038/sj.onc.1205368
  60. Mitomo S, Maesawa C, Ogasawara S, Iwaya T, Shibazaki M, Yashima-Abo A, et al. Downregulation of miR-138 is associated with overexpression of human telomerase reverse transcriptase protein in human anaplastic thyroid carcinoma cell lines. Cancer Sci 2008;99:280-286. https://doi.org/10.1111/j.1349-7006.2007.00666.x
  61. Takakura S, Mitsutake N, Nakashima M, Namba H, Saenko VA, Rogounovitch TI, et al. Oncogenic role of miR-17-92 cluster in anaplastic thyroid cancer cells. Cancer Sci 2008;99: 1147-1154. https://doi.org/10.1111/j.1349-7006.2008.00800.x
  62. Kwon SM, Cho H, Choi JH, Jee BA, Jo Y, Woo HG. Perspectives of integrative cancer genomics in next generation sequencing era. Genomics Inform 2012;10:69-73. https://doi.org/10.5808/GI.2012.10.2.69

Cited by

  1. Autophagy: A potential target for thyroid cancer therapy (Review) vol.2, pp.5, 2014, https://doi.org/10.3892/mco.2014.305
  2. Update on Anaplastic Thyroid Carcinoma: Morphological, Molecular, and Genetic Features of the Most Aggressive Thyroid Cancer vol.2014, pp.1687-8345, 2014, https://doi.org/10.1155/2014/790834
  3. Anaplastic Thyroid Carcinoma: Current Treatments and Potential New Therapeutic Options with Emphasis on TfR1/CD71 vol.2014, pp.1687-8345, 2014, https://doi.org/10.1155/2014/685396
  4. Genomically Driven Precision Medicine to Improve Outcomes in Anaplastic Thyroid Cancer vol.2014, pp.1687-8469, 2014, https://doi.org/10.1155/2014/936285
  5. Anaplastic thyroid cancer vol.22, pp.5, 2015, https://doi.org/10.1097/MED.0000000000000189
  6. c-Met-mediated reactivation of PI3K/AKT signaling contributes to insensitivity of BRAF(V600E) mutant thyroid cancer to BRAF inhibition vol.55, pp.11, 2015, https://doi.org/10.1002/mc.22418
  7. Anaplastic thyroid carcinoma: from clinicopathology to genetics and advanced therapies vol.13, pp.11, 2017, https://doi.org/10.1038/nrendo.2017.76