Molecular biology of thyroid cancer initiation

Clinical and Translational Oncology

Volumn 9, Issue 11, 2007, Pages 686-693

  Riesco Eizaguirre, G ^a,b   Santisteban, P ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

Author keywords

MAPK and PI3K pathway; Molecular classification; Thyroid cancer genetics; Tumour initiation

Indexed keywords

B RAF KINASE; BIOLOGICAL MARKER; HYBRID PROTEIN; IODINE 131; MITOGEN ACTIVATED PROTEIN KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA TRANSCRIPTION FACTOR PAX8; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN P53; PROTEIN RET; RADIOACTIVE IODINE; RAS PROTEIN; SODIUM IODIDE SYMPORTER; THYROGLOBULIN; TRANSCRIPTION FACTOR PAX8;

ANAPLASTIC CARCINOMA; CANCER GROWTH; CARCINOGENESIS; CELL DIFFERENTIATION; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENE REARRANGEMENT; GENETIC PREDISPOSITION; HUMAN; MALIGNANT TRANSFORMATION; METASTASIS; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; RADIATION CARCINOGENESIS; REVIEW; SIGNAL TRANSDUCTION; THYROID FOLLICLE CELL; THYROID FOLLICULAR CARCINOMA; THYROID PAPILLARY CARCINOMA; THYROID UNDIFFERENTIATED CARCINOMA; CELL TRANSFORMATION; CLASSIFICATION; GENETICS; PATHOLOGY; THYROID TUMOR;

CELL TRANSFORMATION, NEOPLASTIC; HUMANS; MOLECULAR BIOLOGY; THYROID NEOPLASMS;

EID: 39749101645     PISSN: 1699048X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12094-007-0125-1     Document Type: Review

References (81)

1. Schlumberger MJ, Filetti S, Hay ID (2003) Nontoxic goiter and thyroid neoplasia. In: Larsen PR, Kronenberg HM, Melmed S et al (eds) Williams textbook of endocrinology, 13th Edn. Saunders, Philadelphia, pp 457-491
2. AJCC (2002) Thyroid. In Greene FL, Page DL, Fleming ID et al (eds) AJCC Cancer Staging Handbook, 6th Edn, Springer, New York, pp 89-98
3. Schlumberger M, Pacini F (2003) Tumeurs de la thyroïde. Editions Nucléon. Paris
4. Xing M (2005) BRAF mutation in thyroid cancer. Endocr Relat Cancer 12:245-262
5. Nikiforova MN, Kimura ET, Gandhi M et al (2003) BRAF mutations in thyroid tumours are restricted to papillary carcinomas and anaplastic or poorly differentiated carcinomas arising from papillary carcinomas. J Clin Endocrinol Metab 88:5399-5404
6. Begum S, Rosenbaum E, Henrique R et al (2004) BRAF mutations in anaplastic thyroid carcinoma: Implications for tumour origin, diagnosis and treatment. Mod Pathol 17:1359-1363
7. Namba H, Nakashima M, Hayashi T et al (2003) Clinical implication of hot spot BRAF mutation, V599E, in papillary thyroid cancers. J Clin Endocrinol Metab 88:4393-4397
8. Quiros RM, Ding HG, Gattuso P et al (2005) Evidence that one subset of anaplastic thyroid carcinomas are derived from papillary carcinomas due to BRAF and p53 mutations. Cancer 103:2261-2268
9. Soares P, Trovisco V, Rocha AS et al (2004) BRAF mutations typical of papillary thyroid carcinoma are more frequently detected in undifferentiated than in insular and insular-like poorly differentiated carcinomas. Virchows Arch 444:572-576
10. Xing M, Vasko V, Tallini G et al (2004) BRAF T1796A transversion mutation in various thyroid neoplasms. J Clin Endocrinol Metab 89:1365-1368
11. Knauf JA, Ma X, Smith EP et al (2005) Targeted expression of BRAFV600E in thyroid cells of transgenic mice results in papillary thyroid cancers that undergo dedifferentiation. Cancer Res 65:4238-4245
12. Cohen Y, Rosenbaum E, Clark DP et al (2004) Mutational analysis of BRAF in fine needle aspiration biopsies of the thyroid: A potential application for the preoperative assessment of thyroid nodules. Clin Cancer Res 10:2761-2765
13. Xing M, Tufano RP, Tufaro AP et al (2004) Detection of BRAF mutation on fine needle aspiration biopsy specimens: A new diagnostic tool for papillary thyroid cancer. J Clin Endocrinol Metab 89:2867-2872
14. Riesco-Eizaguirre G, Gutiérrez-Martínez P, García-Cabezas MA et al (2006) The oncogene BRAF V600E is associated with a high risk of recurrence and less differentiated papillary thyroid carcinoma due to the impairment of Na+/I-targeting to the membrane. Endocr Relat Cancer 13:257-269
15. Xing M, Westra WH, Tufano RP et al (2005) BRAF mutation predicts a poorer clinical prognosis for papillary thyroid cancer. J Clin Endocrinol Metab 90:6373-6379
16. Klugbauer S, Lengfelder E, Demidchik EP, Rabes HM (1995) High prevalence of RET rearrangement in thyroid tumours of children from Belarus after the Chernobyl reactor accident. Oncogene 11:2459-2467
17. Fugazzola L, Pilotti S, Pinchera A et al (1995) Oncogenic rearrangements of the RET proto-oncogene in papillary thyroid carcinomas from children exposed to the Chernobyl nuclear accident. Cancer Res 55:5617-5620
18. Nikiforov YE, Rowland JM, Bove KE et al (1997) Distinct pattern of ret oncogene rearrangements in morphological variants of radiation-induced and sporadic thyroid papillary carcinomas in children. Cancer Res 57:1690-1694
19. Santoro M, Carlomagno F, Hay ID et al (1992) Ret oncogene activation in human thyroid neoplasms is restricted to the papillary cancer subtype. J Clin Invest 89:1517-1522
20. Bounacer A, Wicker R, Caillou B et al (1997) High prevalence of activating ret proto-oncogene rearrangements, in thyroid tumours from patients who had received external radiation. Oncogene 15:1263-1273
21. Bongarzone I, Fugazzola L, Vigneri P et al (1996) Age-related activation of the tyrosine kinase receptor protooncogenes RET and NTRK1 in papillary thyroid carcinoma. J Clin Endocrinol Metab 81:2006-2009
22. Ito T, Seyama T, Iwamoto KS et al (1994) Activated RET oncogene in thyroid cancers of children from areas contaminated by Chernobyl accident. Lancet 344:259
23. Elisei R, Romei C, Vorontsova T et al (2001) RET/PTC rearrangements in thyroid nodules: Studies in irradiated and not irradiated, malignant and benign thyroid lesions in children and adults. J Clin Endocrinol Metab 86:3211-3216
24. Ishizaka Y, Kobayashi S, Ushijima T et al (1991) Detection of retTPC/PTC transcripts in thyroid adenomas and adenomatous goiter by an RTPCR method. Oncogene 6:1667-1672
25. Nikiforova MN, Caudill CM, Biddinger P, Nikiforov YE (2002) Prevalence of RET/PTC rearrangements in Hashimoto's thyroiditis and papillary thyroid carcinomas. Int J Surg Pathol 10:15-22
26. Nikiforov YE (2002) RET/PTC rearrangement in thyroid tumours. Endocr Pathol 13:3-16
27. Zhu Z, Ciampi R, Nikiforova MN et al (2006) Prevalence of RET/PTC rearrangements in thyroid papillary carcinomas: Effects of the detection methods and genetic heterogeneity. J Clin Endocrinol Metab 91:3603-3610
28. Jhiang SM, Sagartz JE, Tong Q et al (1996) Targeted expression of the ret/PTC1 oncogene induces papillary thyroid carcinomas. Endocrinology 137:375-378
29. Santoro M, Chiappetta G, Cerrato A et al (1996) Development of thyroid papillary carcinomas secondary to tissue-specific expression of the RET/ PTC1 oncogene in transgenic mice. Oncogene 12:1821-1826
30. Powell DJ Jr, Russell J, Nibu K et al (1998) The RET/PTC3 oncogene: metastatic solid-type papillary carcinomas in murine thyroids. Cancer Res 58:5523-5528
31. Ito T, Seyama T, Iwamoto KS et al (1993) In vitro irradiation is able to cause RET oncogene rearrangement. Cancer Res 53:2940-2943
32. Carlomagno F, Vitagliano D, Guida T et al (2002) ZD6474, an orally available inhibitor of KDR tyrosine kinase activity, efficiently blocks oncogenic RET kinases. Cancer Res 62:7284-7290
33. Carlomagno F, Vitagliano D, Guida T et al (2003) Efficient inhibition of RET/papillary thyroid carcinoma oncogenic kinases by 4-amino-5-(4-chloro-phenyl)-7-(t-butyl)pyrazolo[3,4-d]pyrimidine (PP2). J Clin Endocrinol Metab 88:1897-1902
34. Lanzi C, Cassinelli G, Cuccuru G et al (2003) Inactivation of Ret/Ptc1 oncoprotein and inhibition of papillary thyroid carcinoma cell proliferation by indolinone RPI-1. Cell Mol Life Sci 60: 1449-1459
35. Strock CJ, Park JI, Rosen M et al (2003) CEP-701 and CEP-751 inhibit constitutively activated RET tyrosine kinase activity and block medullary thyroid carcinoma cell growth. Cancer Res 63:5559-5563
36. Challeton C, Bounacer A, Du Villard JA et al (1995) Pattern of ras and gsp oncogene mutations in radiation-associated human thyroid tumours. Oncogene 11:601-603
37. Suarez HG, du Villard JA, Severino M et al (1990) Presence of mutations in all three ras genes in human thyroid tumours. Oncogene 5: 565-570
38. Wright PA, Lemoine NR, Mayall ES et al (1989) Papillary and follicular thyroid carcinomas show a different pattern of ras oncogene mutation. Br J Cancer 60:576-577
39. García-Rostan G, Zhao H, Camp RL et al (2003) ras mutations are associated with aggressive tumour phenotypes and poor prognosis in thyroid cancer. J Clin Oncol 21:3226-3235
40. Lemoine NR, Mayall ES, Wyllie FS et al (1988) Activated ras oncogenes in human thyroid cancers. Cancer Res 48:4459-4463
41. Namba H, Rubin SA, Fagin JA (1990) Point mutations of ras oncogenes are an early event in thyroid tumorigenesis. Mol Endocrinol 4:1474-1479
42. Vitagliano D, Portella G, Troncone G et al (2006) Thyroid targeting of the N-ras(Gln61Lys) oncogene in transgenic mice results in follicular tumours that progress to poorly differentiated carcinomas. Oncogene 25:5467-5474
43. Eng C (1998) Genetics of Cowden syndrome: Through the looking glass of oncology. Int J Oncol 12:701-710
44. Halachmi N, Halachmi S, Evron E et al (1998) Somatic mutations of the PTEN tumour suppressor gene in sporadic follicular thyroid tumours. Genes Chromosomes Cancer 23:239-243
45. Bruni P, Boccia A, Baldassarre G et al (2000) 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 19:3146-3155
46. Gimm O, Perren A, Weng LP et al (2000) Differential nuclear and cytoplasmic expression of PTEN in normal thyroid tissue, and benign and malignant epithelial thyroid tumours. Am J Pathol 156:1693-1700
47. Vasko V, Saji M, Hardy E et al (2004) Akt activation and localisation correlate with tumour invasion and oncogene expression in thyroid cancer. J Med Genet 41:161-170
48. Ringel MD, Hayre N, Saito J et al (2001) Overexpression and overactivation of Akt in thyroid carcinoma. Cancer Res 61:6105-6111
49. Yeager N, Klein-Szanto A, Kimura S, Di Cristofano A (2007) Pten loss in the mouse thyroid causes goiter and follicular adenomas: Insights into thyroid function and Cowden disease pathogenesis. Cancer Res 67:959-966
50. García-Rostan G, Costa AM, Pereira-Castro I et al (2005) Mutation of the PIK3CA gene in anaplastic thyroid cancer. Cancer Res 65:10199-10207
51. Wu G, Mambo E, Guo Z et al (2005) Uncommon mutation, but common amplifications, of the PIK3CA gene in thyroid tumours. J Clin Endocrinol Metab 90:4688-4693
52. Wang Y, Hou P, Yu H et al (2007) High prevalence and mutual exclusivity of genetic alterations in the phosphatidylinositol-3-kinase/akt pathway in thyroid tumours. J Clin Endocrinol Metab 92:2387-2390
53. Hou P, Liu D, Shan Y et al (2007) Genetic alterations and their relationship in the phosphatidylinositol 3-kinase/Akt pathway in thyroid cancer. Clin Cancer Res 13:1161-1170
54. Osaki M, Oshimura M, Ito H (2004) PI3K-Akt pathway: Its functions and alterations in human cancer. Apoptosis 9:667-676
55. Kroll TG, Sarraf P, Pecciarini L et al (2000) PAX8-PPARgamma1 fusion oncogene in human thyroid carcinoma [corrected]. Science 289: 1357-1360
56. Marques AR, Espadinha C, Catarino AL et al (2002) Expression of PAX8-PPAR gamma 1 rearrangements in both follicular thyroid carcinomas and adenomas. J Clin Endocrinol Metab 87:3947-3952
57. Castro P, Rebocho AP, Soares RJ et al (2006) PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 91: 213-220
58. French CA, Alexander EK, Cibas ES et al (2003) Genetic and biological subgroups of low-stage follicular thyroid cancer. Am J Pathol 162: 1053-1060
59. Nikiforova MN, Biddinger PW, Caudill CM et al (2002) PAX8-PPARgamma rearrangement in thyroid tumours: RT-PCR and immunohistochemical analyses. Am J Surg Pathol 26:1016-1023
60. Nikiforova MN, Lynch RA, Biddinger PW et al (2003) RAS point mutations and PAX8-PPAR gamma rearrangement in thyroid tumours: Evidence for distinct molecular pathways in thyroid follicular carcinoma. J Clin Endocrinol Metab 88:2318-2326
61. Martelli ML, Iuliano R, Le Pera I et al (2002) Inhibitory effects of peroxisome poliferator-activated receptor gamma on thyroid carcinoma cell growth. J Clin Endocrinol Metab 87:4728-4735
62. Au AY, McBride C, Wilhelm KG Jr et al (2006) PAX8-peroxisome proliferator-activated receptor gamma (PPARgamma) disrupts normal PAX8 or PPARgamma transcriptional function and stimulates follicular thyroid cell growth. Endocrinology 147:367-376
63. Ito T, Seyama T, Mizuno T et al (1992) Unique association of p53 mutations with undifferentiated but not with differentiated carcinomas of the thyroid gland. Cancer Res 52:1369-1371
64. Fagin JA, Matsuo K, Karmakar A et al (1993) High prevalence of mutations of the p53 gene in poorly differentiated human thyroid carcinomas. J Clin Invest 91:179-184
65. Battista S, Martelli ML, Fedele M et al (1995) A mutated p53 gene alters thyroid cell differentiation. Oncogene 11:2029-2037
66. Fagin JA, Tang SH, Zeki K et al (1996) Reexpression of thyroid peroxidase in a derivative of an undifferentiated thyroid carcinoma cell line by introduction of wild-type p53. Cancer Res 56:765-771
67. Moretti F, Farsetti A, Soddu S et al (1997) p53 re-expression inhibits proliferation and restores differentiation of human thyroid anaplastic carcinoma cells. Oncogene 14:729-740
68. Medina DL, Santisteban P (2000) Thyrotropin-dependent proliferation of in vitro rat thyroid cell systems. Eur J Endocrinol 143:161-178
69. Kimura T, Van Keymeulen A, Golstein J et al (2001) Regulation of thyroid cell proliferation by TSH and other factors: A critical evaluation of in vitro models. Endocr Rev 22:631-656
70. Parma J, Duprez L, Van Sande J et al (1993) Somatic mutations in the thyrotropin receptor gene cause hyperfunctioning thyroid adenomas. Nature 365:649-651
71. 2+ cascades. Mol Endocrinol 9:725-733
72. Porcellini A, Ciullo I, Laviola L et al (1994) Novel mutations of thyrotropin receptor gene in thyroid hyperfunctioning adenomas. Rapid identification by fine needle aspiration biopsy. J Clin Endocrinol Metab 79:657-661
73. O'sullivan C, Barton CM, Staddon SL et al (1991) Activating point mutations of the gsp oncogene in human thyroid adenomas. Mol Carcinog 4:345-349
74. Lyons J, Landis CA, Harsh G et al (1990) Two G protein oncogenes in human endocrine tumours. Science 249:655-659
75. Melillo RM, Castellone MD, Guarino V et al (2005) The RET/PTC-RAS-BRAF linear signalling cascade mediates the motile and mitogenic phenotype of thyroid cancer cells. J Clin Invest 115:1068-1081
76. Finley DJ, Arora N, Zhu B et al (2004) Molecular profiling distinguishes papillary carcinoma from benign thyroid nodules. J Clin Endocrinol Metab 89:3214-3223
77. Jarzab B, Gubala E, Lange D (2005) [DNA microarrays and papillary thyroid carcinoma gene expression profile]. Endokrynol Pol 56:293-301
78. Huang Y, Prasad M, Lemon WJ et al (2001) Gene expression in papillary thyroid carcinoma reveals highly consistent profiles. Proc Natl Acad Sci U S A 98:15044-15049
79. Wasenius VM, Hemmer S, Kettunen E et al (2003) Hepatocyte growth factor receptor, matrix metalloproteinase-11, tissue inhibitor of metalloproteinase-1, and fibronectin are up-regulated in papillary thyroid carcinoma: A cDNA and tissue microarray study. Clin Cancer Res 9:68-75
80. Giordano TJ, Kuick R, Thomas DG et al (2005) Molecular classification of papillary thyroid carcinoma: Distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene 24:6646-6656
81. Mesa C Jr, Mirza M, Mitsutake N et al (2006) Conditional activation of RET/PTC3 and BRAFV600E in thyroid cells is associated with gene expression profiles that predict a preferential role of BRAF in extracellular matrix remodeling. Cancer Res 66:6521-6529