Genetic alterations in poorly differentiated and undifferentiated thyroid carcinomas

Current Genomics

Volumn 12, Issue 8, 2011, Pages 609-617

  Soares, Paula ^a,b   Lima, Jorge ^a,b   Preto, Ana ^a,c   Castro, Patricia ^a,b   Vinagre, João ^a,b   Celestino, Ricardo ^a,b   Couto, Joana P ^a,b   Prazeres, Hugo ^a,b,e   Eloy, Catarina ^a,b,d   Máximo, Valdemar ^a,b   Sobrinho Simoes M ^a,b,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b University of Porto   (Portugal)

^c UNIVERSITY OF MINHO   (Portugal)

^d HOSPITAL DE SÃO JOÃO   (Portugal)

^e EPE   (Portugal)

Author keywords

catenin; BRAF; P53; PI3K; Poorly differentiated thyroid carcinoma; RAS; Telomerase; Undifferentiated thyroid carcinoma

Indexed keywords

B RAF KINASE; BETA CATENIN; HYBRID PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN P53; PROTEIN RET; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR PAX8; TYROSINE KINASE RECEPTOR; UVOMORULIN; WNT PROTEIN;

ARTICLE; CELL DEDIFFERENTIATION; CELL PROLIFERATION; DIFFERENTIATED THYROID CANCER; ENZYME ACTIVATION; ENZYME ACTIVITY; EPIGENETICS; GENE MUTATION; GENE REARRANGEMENT; HUMAN; ONCOGENE N RAS; POLYMERASE CHAIN REACTION; POORLY DIFFERENTIATED THYROID CANCER; PROGNOSIS; TELOMERIC REPEAT AMPLIFICATION PROTOCOL; THYROID CARCINOMA; UNDIFFERENTIATED CARCINOMA; UNDIFFERENTIATED THYROID CARCINOMA;

EID: 82055176819     PISSN: 13892029     EISSN: 18755488     Source Type: Journal    
DOI: 10.2174/138920211798120853     Document Type: Article

References (102)

1. Carcangiu, M. L.; Zampi, G.; Rosai, J. Poorly differentiated (insular) thyroid carcinoma. A reinterpretation of Langhans' wuchernde Struma. Am. J. Surg. Pathol., 1984, 8, 655-668.
2. DeLellis, R.A.; Lloyd L. R., Heitz, P.U.; Eng, C. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Endocrine Glands. IARC Press: Lyon, 2004.
3. Hundahl, S. A.; Fleming, I. D.; Fremgen, A. M.; Menck, H. R. A National Cancer Data Base report on 53.856 cases of thyroid carcinoma treated in the U.S., 1985-1995 [see comments]. Cancer, 1998, 83, 2638-2648.
4. Wiseman, S. M.; Masoudi, H.; Niblock, P.; Turbin, D.; Rajput, A.; Hay, J.; Bugis, S.; Filipenko, D.; Huntsman, D.; Gilks, B. Anaplastic thyroid carcinoma: expression profile of targets for therapy offers new insights for disease treatment. Ann. Surg. Oncol., 2007, 14, 719-729.
5. Ashfaq, R.; Vuitch, F.; Delgado, R.; Albores-Saavedra, J. Papillary and follicular thyroid carcinomas with an insular component. Cancer, 1994, 73, 416-423.
6. Pilotti, S.; Collini, P.; Mariani, L.; Placucci, M.; Bongarzone, I.; Vigneri, P.; Cipriani, S.; Falcetta, F.; Miceli, R.; Pierotti, M. A.; Rilke, F. Insular carcinoma: a distinct de novo entity among follicular carcinomas of the thyroid gland. Am. J. Surg. Pathol., 1997, 21, 1466-1473.
7. Garcia-Rostan, G.; Sobrinho-Simões, M. Poorly differentiated thyroid carcinoma: an evolving entity. Diagn. Histopathol., 2011, 17, 114-123.
8. Sobrinho-Simoes, M.; Sambade, C.; Fonseca, E.; Soares, P. Poorly differentiated carcinomas of the thyroid gland: a review of the clinicopathologic features of a series of 28 cases of a heterogeneous, clinically aggressive group of thyroid tumors. Int. J. Surg. Pathol., 2002, 10, 123-131.
9. Volante, M.; Rapa, I.; Gandhi, M.; Bussolati, G.; Giachino, D.; Papotti, M.; Nikiforov, Y. E. RAS mutations are the predominant molecular alteration in poorly differentiated thyroid carcinomas and bear prognostic impact. J. Clin. Endocrinol. Metab., 2009, 94, 4735-4741.
10. Volante, M.; Collini, P.; Nikiforov, Y. E.; Sakamoto, A.; Kakudo, K.; Katoh, R.; Lloyd, R. V.; LiVolsi, V. A.; Papotti, M.; Sobrinho- Simoes, M.; Bussolati, G.; Rosai, J. Poorly differentiated thyroid carcinoma: the Turin proposal for the use of uniform diagnostic criteria and an algorithmic diagnostic approach. Am. J. Surg. Pathol., 2007, 31, 1256-1264.
11. Sobrinho-Simoes, M.; Maximo, V.; Rocha, A. S.; Trovisco, V.; Castro, P.; Preto, A.; Lima, J.; Soares, P. Intragenic mutations in thyroid cancer. Endocrinol. Metab. Clin. North. Am., 2008, 37, 333-362, viii.
12. Chong, H.; Guan, K. L. Regulation of Raf through phosphorylation and N terminus-C terminus interaction. J. Biol.Chem., 2003, 278, 36269-36276.
13. Davies, H.; Bignell, G. R.; Cox, C.; Stephens, P.; Edkins, S.; Clegg, S.; Teague, J.; Woffendin, H.; Garnett, M. J.; Bottomley, W.; Davis, N.; Dicks, E.; Ewing, R.; Floyd, Y.; Gray, K.; Hall, S.; Hawes, R.; Hughes, J.; Kosmidou, V.; Menzies, A.; Mould, C.; Parker, A.; Stevens, C.; Watt, S.; Hooper, S.; Wilson, R.; Jayatilake, H.; Gusterson, B. A.; Cooper, C.; Shipley, J.; Hargrave, D.; Pritchard-Jones, K.; Maitland, N.; Chenevix-Trench, G.; Riggins, G. J.; Bigner, D. D.; Palmieri, G.; Cossu, A.; Flanagan, A.; Nicholson, A.; Ho, J. W.; Leung, S. Y.; Yuen, S. T.; Weber, B. L.; Seigler, H. F.; Darrow, T. L.; Paterson, H.; Marais, R.; Marshall, C. J.; Wooster, R.; Stratton, M. R.; Futreal, P. A. Mutations of the BRAF gene in human cancer. Nature, 2002, 417, 949-954.
14. Nikiforova, M. N.; Kimura, E. T.; Gandhi, M.; Biddinger, P. W.; Knauf, J. A.; Basolo, F.; Zhu, Z.; Giannini, R.; Salvatore, G.; Fusco, A.; Santoro, M.; Fagin, J. A.; Nikiforov, Y. E. BRAF Mutations in Thyroid Tumors Are Restricted to Papillary Carcinomas and Anaplastic or Poorly Differentiated Carcinomas Arising from Papillary Carcinomas. J. Clin. Endocrinol. Metab., 2003, 88, 5399-5404.
15. Cohen, Y.; Xing, M.; Mambo, E.; Guo, Z.; Wu, G.; Trink, B.; Beller, U.; Westra, W. H.; Ladenson, P. W.; Sidransky, D. BRAF Mutation in Papillary Thyroid Carcinoma. JNCI Cancer Spectrum 2003, 95, 625-627.
16. Kimura, E. T.; Nikiforova, M. N.; Zhu, Z.; Knauf, J. A.; Nikiforov, Y. E.; Fagin, J. A. 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. Xu, X.; Quiros, R. M.; Gattuso, P.; Ain, K. B.; Prinz, R. A. High Prevalence of BRAF Gene Mutation in Papillary Thyroid Carcinomas and Thyroid Tumor Cell Lines. Cancer Res., 2003, 63, 4561-4567.
18. Soares, P.; Trovisco, V.; Rocha, A. S.; Lima, J.; Castro, P.; Preto, A.; Maximo, V.; Botelho, T.; Seruca, R.; Sobrinho-Simoes, M. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene, 2003, 22, 4578-4580.
19. Trovisco, V.; Soares, P.; Preto, A.; de Castro, I. V.; Lima, J.; Castro, P.; Maximo, V.; Botelho, T.; Moreira, S.; Meireles, A. M.; Magalhaes, J.; Abrosimov, A.; Cameselle-Teijeiro, J.; Sobrinho- Simoes, M. Type and prevalence of BRAF mutations are closely associated with papillary thyroid carcinoma histotype and patients' age but not with tumour aggressiveness. Virchows Arch., 2005, 446, 589-595.
20. Espinosa, A.V.; Porchia, L.; Ringel, M. D. Targeting BRAF in thyroid cancer. Br. J. Cancer, 2007, 96, 16-20.
21. Mitsiades, C. S.; Negri, J.; McMullan, C.; McMillin, D. W.; Sozopoulos, E.; Fanourakis, G.; Voutsinas, G.; Tseleni-Balafouta, S.; Poulaki, V.; Batt, D.; Mitsiades, N. Targeting BRAFV600E in thyroid carcinoma: therapeutic implications. Mol. Cancer Ther., 2007, 6, 1070-1078.
22. Ricarte-Filho, J. C.; Ryder, M.; Chitale, D. A.; Rivera, M.; Heguy, A.; Ladanyi, M.; Janakiraman, M.; Solit, D.; Knauf, J. A.; Tuttle, R. M.; Ghossein, R. A.; Fagin, J. A. Mutational profile of advanced primary and metastatic radioactive iodine-refractory thyroid cancers reveals distinct pathogenetic roles for BRAF, PIK3CA, and AKT1. Cancer Res., 2009, 69, 4885-4893.
23. Durante, C.; Puxeddu, E.; Ferretti, E.; Morisi, R.; Moretti, S.; Bruno, R.; Barbi, F.; Avenia, N.; Scipioni, A.; Verrienti, A.; Tosi, E.; Cavaliere, A.; Gulino, A.; Filetti, S.; Russo, D. BRAF mutations in papillary thyroid carcinomas inhibit genes involved in iodine metabolism. J. Clin. Endocrinol. Metab., 2007, 92, 2840-2843.
24. Soares, P.; Trovisco, V.; Rocha, A. S.; Feijao, T.; Rebocho, A. P.; Fonseca, E.; Vieira, d. C. I.; Cameselle-Teijeiro, J.; Cardoso- Oliveira, M.; Sobrinho-Simoes, M. BRAF mutations typical of papillary thyroid carcinoma are more frequently detected in undifferentiated than in insular and insular-like poorly differentiated carcinomas. Virchows Arch., 2004, 444, 572-576.
25. Romei, C.; Ciampi, R.; Faviana, P.; Agate, L.; Molinaro, E.; Bottici, V.; Basolo, F.; Miccoli, P.; Pacini, F.; Pinchera, A.; Elisei, R. BRAFV600E mutation, but not RET/PTC rearrangements, is correlated with a lower expression of both thyroperoxidase and sodium iodide symporter genes in papillary thyroid cancer. Endocr. Relat. Cancer, 2008, 15, 511-520.
26. Xing, M. Identifying genetic alterations in poorly differentiated thyroid cancer: a rewarding pursuit. J. Clin. Endocrinol. Metab., 2009, 94, 4661-4664.
27. Xing, M. BRAF mutation in thyroid cancer. Endocr. Relat. Cancer, 2005, 12, 245-262.
28. Manenti, G.; Pilotti, S.; Re, F. C.; Della Porta, G.; Pierotti, M. A. Selective activation of ras oncogenes in follicular and undifferentiated thyroid carcinomas. Eur. J. Cancer, 1994, 30A, 987-993.
29. Basolo, F.; Pisaturo, F.; Pollina, L. E.; Fontanini, G.; Elisei, R.; Molinaro, E.; Iacconi, P.; Miccoli, P.; Pacini, F. N-ras mutation in poorly differentiated thyroid carcinomas: correlation with bone metastases and inverse correlation to thyroglobulin expression. Thyroid, 2000, 10, 19-23.
30. Garcia-Rostan, G.; Zhao, H.; Camp, R. L.; Pollan, M.; Herrero, A.; Pardo, J.; Wu, R.; Carcangiu, M. L.; Costa, J.; Tallini, G. Ras mutations are associated with aggressive tumor phenotypes and poor prognosis in thyroid cancer. J. Clin. Oncol., 2003, 21, 3226-3235.
31. Fukushima, T.; Takenoshita, S. Roles of RAS and BRAF mutations in thyroid carcinogenesis. Fukushima J. Med. Sci., 2005, 51, 67-75.
32. Quiros, R. M.; Ding, H. G.; Gattuso, P.; Prinz, R. A.; 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.
33. Volante, M.; Papotti, M.; Gugliotta, P.; Migheli, A.; Bussolati, G. Extensive DNA fragmentation in oxyphilic cell lesions of the thyroid. J. Histochem. Cytochem., 2001, 49, 1003-1011.
34. Wang, Y.; Hou, P.; Yu, H.; Wang, W.; Ji, M.; Zhao, S.; Yan, S.; Sun, X.; Liu, D.; Shi, B.; Zhu, G.; Condouris, S.; Xing, M. High prevalence and mutual exclusivity of genetic alterations in the phosphatidylinositol-3-kinase/akt pathway in thyroid tumors. J. Clin. Endocrinol. Metab., 2007, 92, 2387-2390.
35. Hou, P.; Liu, D.; Shan, Y.; Hu, S.; Studeman, K.; Condouris, S.; Wang, Y.; Trink, A.; El-Naggar, A. K.; Tallini, G.; Vasko, V.; Xing, M. Genetic alterations and their relationship in the phosphatidylinositol 3-kinase/Akt pathway in thyroid cancer. Clin. Cancer Res., 2007, 13, 1161-1170.
36. Wright, P. A.; Lemoine, N. R.; Goretzki, P. E.; Wyllie, F. S.; Bond, J.; Hughes, C.; Roher, H. D.; Williams, E. D.; Wynford-Thomas, D. Mutation of the p53 gene in a differentiated human thyroid carcinoma cell line, but not in primary thyroid tumours. Oncogene, 1991, 6, 1693-1697.
37. Ito, T.; Seyama, T.; Mizuno, T.; Tsuyama, N.; Hayashi, T.; Hayashi, Y.; Dohi, K.; Nakamura, N.; Akiyama, M. Unique association of p53 mutations with undifferentiated but not with differentiated carcinomas of the thyroid gland. Cancer Res., 1992, 52, 1369-1371.
38. Donghi, R.; Longoni, A.; Pilotti, S.; Michieli, P.; Della Porta, G.; Pierotti, M. A. Gene p53 mutations are restricted to poorly differentiated and undifferentiated carcinomas of the thyroid gland. J. Clin. Invest., 1993, 91, 1753-1760.
39. Fagin, J. A.; Matsuo, K.; Karmakar, A.; Chen, D. L.; Tang, S. H.; Koeffler, H. P. High prevalence of mutations of the p53 gene in poorly differentiated human thyroid carcinomas. J. Clin. Invest., 1993, 91, 179-184.
40. Park, K. Y.; Koh, J. M.; Kim, Y. I.; Park, H. J.; Gong, G.; Hong, S. J.; Ahn, I. M. Prevalences of Gs alpha, ras, p53 mutations and ret/PTC rearrangement in differentiated thyroid tumours in a Korean population. Clin. Endocrinol. (Oxf), 1998, 49, 317-323.
41. Arends, J. W. Molecular interactions in the Vogelstein model of colorectal carcinoma. J. Pathol., 2000, 190, 412-416.
42. Zou, M.; Shi, Y.; Farid, N. R. P53 mutations in all stages of thyroid carcinomas. J. Clin. Endocrinol. Metab., 1993, 77, 1054-1058.
43. Soares, P.; Cameselle-Teijeiro, J.; Sobrinho-Simoes, M. Immunohistochemical detection of p53 in differentiated, poorly differentiated and undifferentiated carcinomas of the thyroid. Histopathology, 1994, 24, 205-210.
44. Saltman, B.; Singh, B.; Hedvat, C. V.; Wreesmann, V. B.; Ghossein, R. Patterns of expression of cell cycle/apoptosis genes along the spectrum of thyroid carcinoma progression. Surgery, 2006, 140, 899-905.
45. Ito, T.; Seyama, T.; Mizuno, T.; Tsuyama, N.; Hayashi, Y.; Dohi, K.; Nakamura, N.; Akiyama, M. Genetic alterations in thyroid tumor progression: association with p53 gene mutations. Jpn. J. Cancer Res., 1993, 84, 526-531.
46. Dobashi, Y.; Sakamoto, A.; Sugimura, H.; Mernyei, M.; Mori, M.; Oyama, T.; Machinami, R. Overexpression of p53 as a possible prognostic factor in human thyroid carcinoma. Am. J. Surg. Pathol., 1993, 17, 375-381.
47. Farid, P.; Gomb, S. Z.; Peter, I.; Szende, B. Bcl2, p53 and bax in thyroid tumors and their relation to apoptosis. Neoplasma, 2001, 48, 299-301.
48. Wynford-Thomas, D. Proliferative lifespan checkpoints: cell-type specificity and influence on tumour biology. Eur. J. Cancer, 1997, 33, 716-726.
49. Wynford-Thomas, D.; Blaydes, J. The influence of cell context on the selection pressure for p53 mutation in human cancer. Carcinogenesis, 1998, 19, 29-36.
50. Rodrigues, R. F.; 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.
51. Rodrigues, R. F.; Roque, L.; Krug, T.; Leite, V. Poorly differentiated and anaplastic thyroid carcinomas: chromosomal and oligo-array profile of five new cell lines. Br. J. Cancer, 2007, 96, 1237-1245.
52. Wreesmann, V. B.; Ghossein, R. A.; Patel, S. G.; Harris, C. P.; Schnaser, E. A.; Shaha, A. R.; Tuttle, R. M.; Shah, J. P.; Rao, P. H.; Singh, B. Genome-wide appraisal of thyroid cancer progression. Am. J. Pathol., 2002, 161, 1549-1556.
53. Miura, D.; Wada, N.; Chin, K.; Magrane, G. G.; Wong, M.; Duh, Q. Y.; Clark, O. H. Anaplastic thyroid cancer: cytogenetic patterns by comparative genomic hybridization. Thyroid, 2003, 13, 283-290.
54. Tung, W. S.; Shevlin, D. W.; Bartsch, D.; Norton, J. A.; Wells, S. A., Jr.; Goodfellow, P. J. Infrequent CDKN2 mutation in human differentiated thyroid cancers. Mol. Carcinog., 1996, 15, 5-10.
55. Garcia-Rostan, G.; Costa, A. M.; Pereira-Castro, I.; Salvatore, G.; Hernandez, R.; Hermsem, M. J.; Herrero, A.; Fusco, A.; Cameselle-Teijeiro, J.; Santoro, M. Mutation of the PIK3CA gene in anaplastic thyroid cancer. Cancer Res., 2005, 65, 10199-10207.
56. Preto, A.; Reis-Filho, J. S.; Ricardo, S.; Soares, P. P63 expression in papillary and anaplastic carcinomas of the thyroid gland: lack of an oncogenetic role in tumorigenesis and progression. Pathol. Res. Pract., 2002, 198, 449-454.
57. Santoro, M.; Papotti, M.; Chiappetta, G.; Garcia-Rostan, G.; Volante, M.; Johnson, C.; Camp, R. L.; Pentimalli, F.; Monaco, C.; Herrero, A.; Carcangiu, M. L.; Fusco, A.; Tallini, G. RET activation and clinicopathologic features in poorly differentiated thyroid tumors. J. Clin. Endocrinol. Metab., 2002, 87, 370-379.
58. Tallini, G.; Santoro, M.; Helie, M.; Carlomagno, F.; Salvatore, G.; Chiappetta, G.; Carcangiu, M. L.; Fusco, A. RET/PTC oncogene activation defines a subset of papillary thyroid carcinomas lacking evidence of progression to poorly differentiated or undifferentiated tumor phenotypes. Clin. Cancer Res., 1998, 4, 287-294.
59. Mochizuki, K.; Kondo, T.; Nakazawa, T.; Iwashina, M.; Kawasaki, T.; Nakamura, N.; Yamane, T.; Murata, S.; Ito, K.; Kameyama, K.; Kobayashi, M.; Katoh, R. RET rearrangements and BRAF mutation in undifferentiated thyroid carcinomas having papillary carcinoma components. Histopathology, 2010, 57, 444-450.
60. Kroll, T. G.; Sarraf, P.; Pecciarini, L.; Chen, C. J.; Mueller, E.; Spiegelman, B. M.; Fletcher, J. A. PAX8-PPARgamma1 fusion oncogene in human thyroid carcinoma [corrected]. Science, 2000, 289, 1357-1360.
61. Marques, A. R.; Espadinha, C.; Catarino, A. L.; Moniz, S.; Pereira, T.; Sobrinho, L. G.; Leite, V. Expression of PAX8-PPAR gamma 1 rearrangements in both follicular thyroid carcinomas and adenomas. J. Clin. Endocrinol. Metab., 2002, 87, 3947-3952.
62. Castro, P.; Rebocho, A. P.; Soares, R. J.; Magalhaes, J.; Roque, L.; Trovisco, V.; Vieira de Castro, I.; Cardoso-de-Oliveira, M.; Fonseca, E.; Soares, P.; Sobrinho-Simoes, M. PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J. Clin. Endocrinol. Metab., 2006, 91, 213-220.
63. Nikiforova, M. N.; Biddinger, P. W.; Caudill, C. M.; Kroll, T. G.; Nikiforov, Y. E. PAX8-PPARgamma rearrangement in thyroid tumors: RT-PCR and immunohistochemical analyses. Am. J. Surg. Pathol., 2002, 26, 1016-1023.
64. Garcia-Rostan, G.; Camp, R. L.; Herrero, A.; Carcangiu, M. L.; Rimm, D. L.; 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.
65. Garcia-Rostan, G.; Tallini, G.; Herrero, A.; D'Aquila, T. G.; Carcangiu, M. L.; Rimm, D. L. Frequent mutation and nuclear localization of beta-catenin in anaplastic thyroid carcinoma. Cancer Res., 1999, 59, 1811-1815.
66. Kim, W. B.; Lewis, C. J.; McCall, K. D.; Malgor, R.; Kohn, A. D.; Moon, R. T.; Kohn, L. D. Overexpression of Wnt-1 in thyrocytes enhances cellular growth but suppresses transcription of the thyroperoxidase gene via different signaling mechanisms. J. Endocrinol., 2007, 193, 93-106.
67. Rocha, A. S.; Soares, P.; Fonseca, E.; Cameselle-Teijeiro, J.; Oliveira, M. C.; Sobrinho-Simoes, M. E-cadherin loss rather than beta-catenin alterations is a common feature of poorly differentiated thyroid carcinomas. Histopathology, 2003, 42, 580-587.
68. Kurihara, T.; Ikeda, S.; Ishizaki, Y.; Fujimori, M.; Tokumoto, N.; Hirata, Y.; Ozaki, S.; Okajima, M.; Sugino, K.; Asahara, T. Immunohistochemical and sequencing analyses of the Wnt signaling components in Japanese anaplastic thyroid cancers. Thyroid, 2004, 14, 1020-1029.
69. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer. Cell, 2000, 100, 57-70.
70. Kim, N. W.; Piatyszek, M. A.; Prowse, K. R.; Harley, C. B.; West, M. D.; Ho, P. L.; Coviello, G. M.; Wright, W. E.; Weinrich, S. L.; Shay, J. W. Specific association of human telomerase activity with immortal cells and cancer [see comments]. Science, 1994, 266, 2011-2015.
71. Shay, J. W.; Bacchetti, S. A survey of telomerase activity in human cancer. Eur. J. Cancer, 1997, 33, 787-791.
72. Bryan, T. M.; Englezou, A.; Dalla-Pozza, L.; Dunham, M. A.; Reddel, R. R. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med., 1997, 3, 1271-1274.
73. Bryan, T. M.; Englezou, A.; Gupta, J.; Bacchetti, S.; Reddel, R. R. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J., 1995, 14, 4240-4248.
74. Dumont, J. E.; Maenhaut, C.; Pirson, I.; Baptist, M.; Roger, P. P. Growth factors controlling the thyroid gland. Baillieres Clin. Endocrinol. Metab., 1991, 5, 727-754.
75. Preto, A.; Cameselle-Teijeiro, J.; Moldes-Boullosa, J.; Soares, P.; Cameselle-Teijeiro, J. F.; Silva, P.; Reis-Filho, J. S.; Reyes-Santias, R. M.; Alfonsin-Barreiro, N.; Forteza, J.; Sobrinho-Simoes, M. Telomerase expression and proliferative activity suggest a stem cell role for thyroid solid cell nests. Mod. Pathol., 2004, 17, 819-826.
76. Matthews, P.; Jones, C. J.; Skinner, J.; Haughton, M.; de Micco, C.; Wynford-Thomas, D. Telomerase activity and telomere length in thyroid neoplasia: biological and clinical implications. J. Pathol., 2001, 194, 183-193.
77. Hoang-Vu, C.; Boltze, C.; Gimm, O.; Poremba, C.; Dockhorn- Dworniczak, B.; Kohrle, J.; Rath, F. W.; Dralle, H. Expression of telomerase genes in thyroid carcinoma. Int. J. Oncol., 2002, 21, 265-272.
78. Takano, T.; Ito, Y.; Matsuzuka, F.; Miya, A.; Kobayashi, K.; Yoshida, H.; Miyauchi, A. Quantitative measurement of telomerase reverse transcriptase, thyroglobulin and thyroid transcription factor 1 mRNAs in anaplastic thyroid carcinoma tissues and cell lines. Oncol. Rep., 2007, 18, 715-720.
79. Brousset, P.; Chaouche, N.; Leprat, F.; Branet-Brousset, F.; Trouette, H.; Zenou, R. C.; Merlio, J. P.; Delsol, G. Telomerase activity in human thyroid carcinomas originating from the follicular cells. J. Clin. Endocrinol. Metab., 1997, 82, 4214-4216.
80. Saji, M.; Xydas, S.; Westra, W. H.; Liang, C. K.; Clark, D. P.; Udelsman, R.; Umbricht, C. B.; Sukumar, S.; Zeiger, M. A. Human telomerase reverse transcriptase (hTERT) gene expression in thyroid neoplasms. Clin. Cancer Res., 1999, 5, 1483-1489.
81. Aogi, K.; Kitahara, K.; Urquidi, V.; Tarin, D.; Goodison, S. Comparison of telomerase and CD44 expression as diagnostic tumor markers in lesions of the thyroid. Clin. Cancer Res., 1999, 5, 2790-2797.
82. Onoda, N.; Ishikawa, T.; Yoshikawa, K.; Sugano, S.; Kato, Y.; Sowa, M.; Hirakawa-Yong Suk Chung, K. Telomerase activity in thyroid tumors. Oncol. Rep., 1998, 5, 1447-1450.
83. Umbricht, C. B.; Saji, M.; Westra, W. H.; Udelsman, R.; Zeiger, M. A.; Sukumar, S. Telomerase activity: a marker to distinguish follicular thyroid adenoma from carcinoma. Cancer Res., 1997, 57, 2144-2147.
84. Okayasu, I.; Osakabe, T.; Fujiwara, M.; Fukuda, H.; Kato, M.; Oshimura, M. Significant correlation of telomerase activity in thyroid papillary carcinomas with cell differentiation, proliferation and extrathyroidal extension. Jpn. J. Cancer Res., 1997, 88, 965-970.
85. Liu, Z.; Hou, P.; Ji, M.; Guan, H.; Studeman, K.; Jensen, K.; Vasko, V.; El-Naggar, A. K.; Xing, M. 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.
86. Murugan, A. K.; Xing, M. Anaplastic Thyroid Cancers Harbor Novel Oncogenic Mutations of the ALK Gene. Cancer Res., 2011, 71, 4403-4411.
87. Prazeres, H.; Torres, J.; Rodrigues, F.; Pinto, M.; Pastoriza, M. C.; Gomes, D.; Cameselle-Teijeiro, J.; Vidal, A.; Martins, T. C.; Sobrinho-Simoes, M.; Soares, P. Chromosomal, epigenetic and microRNA-mediated inactivation of LRP1B, a modulator of the extracellular environment of thyroid cancer cells. Oncogene, 2011, 30, 1302-1317.
88. Visone, R.; Pallante, P.; Vecchione, A.; Cirombella, R.; Ferracin, M.; Ferraro, A.; Volinia, S.; Coluzzi, S.; Leone, V.; Borbone, E.; Liu, C. G.; Petrocca, F.; Troncone, G.; Calin, G. A.; Scarpa, A.; Colato, C.; Tallini, G.; Santoro, M.; Croce, C. M.; Fusco, A. Specific microRNAs are downregulated in human thyroid anaplastic carcinomas. Oncogene, 2007, 26, 7590-7595.
89. Schwertheim, S.; Sheu, S. Y.; Worm, K.; Grabellus, F.; Schmid, K. W. Analysis of deregulated miRNAs is helpful to distinguish poorly differentiated thyroid carcinoma from papillary thyroid carcinoma. Horm. Metab. Res., 2009, 41, 475-481.
90. Braun, J.; Hoang-Vu, C.; Dralle, H.; Huttelmaier, S. Downregulation of microRNAs directs the EMT and invasive potential of anaplastic thyroid carcinomas. Oncogene, 2010, 29, 4237-4244.
91. Murugan, A. K.; 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.
92. Saji, M.; Westra, W. H.; Chen, H.; Umbricht, C. B.; Tuttle, R. M.; Box, M. F.; Udelsman, R.; Sukumar, S.; Zeiger, M. A. Telomerase activity in the differential diagnosis of papillary carcinoma of the thyroid. Surgery, 1997, 122, 1137-1140.
93. Aogi, K.; Kitahara, K.; Buley, I.; Backdahl, M.; Tahara, H.; Sugino, T.; Tarin, D.; Goodison, S. Telomerase activity in lesions of the thyroid: application to diagnosis of clinical samples including fine-needle aspirates. Clin. Cancer Res., 1998, 4, 1965-1970.
94. Yashima, K.; Vuitch, F.; Gazdar, A. F.; Fahey, T. J., 3rd Telomerase activity in benign and malignant thyroid diseases. Surgery, 1997, 122, 1141-1145; discussion 1145-1146.
95. Cheng, A. J.; Lin, J. D.; Chang, T.; Wang, T. C. Telomerase activity in benign and malignant human thyroid tissues. Br. J. Cancer, 1998, 77, 2177-2180.
96. De Deken, X.; Vilain, C.; Van Sande, J.; Dumont, J. E.; Miot, F. Decrease of telomere length in thyroid adenomas without telomerase activity. J. Clin. Endocrinol. Metab., 1998, 83, 4368-4372.
97. Haugen, B. R.; Nawaz, S.; Markham, N.; Hashizumi, T.; Shroyer, A. L.; Werness, B.; Shroyer, K. R. Telomerase activity in benign and malignant thyroid tumors. Thyroid, 1997, 7, 337-342.
98. Lo, C. Y.; Lam, K. Y.; Chan, K. T.; Luk, J. M. Telomerase activity in thyroid malignancy. Thyroid, 1999, 9, 1215-1220.
99. Onoda, N.; Ishikawa, T.; Yoshikawa, K.; Sugano, S.; Kato, Y.; Sowa, M.; Hirakawa-Yong Suk Chung, K. Telomerase activity in thyroid tumors. Oncol. Rep., 1998, 5, 1447-1450.
100. Kammori, M.; Takubo, K.; Nakamura, K.; Furugouri, E.; Endo, H.; Kanauchi, H.; Mimura, Y.; Kaminishi, M. Telomerase activity and telomere length in benign and malignant human thyroid tissues. Cancer Lett., 2000, 159, 175-181.
101. Sebesta, J.; Brown, T.; Williard, W.; Dehart, M. J.; Aldous, W.; Kavolius, J.; Azarow, K. Does telomerase activity add to the value of fine needle aspirations in evaluating thyroid nodules? Am. J. Surg., 2001, 181, 420-422.
102. Matthews, P.; Jones, C. J.; Skinner, J.; Haughton, M.; de Micco, C.; Wynford-Thomas, D. Telomerase activity and telomere length in thyroid neoplasia: biological and clinical implications. J. Pathol., 2001, 194, 183-193.