BRAF, p53 and SOX2 in anaplastic thyroid carcinoma: Evidence for multistep carcinogenesis

Pathology

Volumn 43, Issue 5, 2011, Pages 447-452

  Gauchotte, Guillaume ^a,b   Philippe, Christophe ^c   Lacomme, Stéphanie ^a   Léotard, Brigitte ^c   Wissler, Marie Pierre ^a   Allou, Lila ^c   Toussaint, Bruno ^a   Klein, Marc ^c   Vignaud, Jean Michel ^a,b   Bressenot, Aude ^a,b  

^a UNIVERSITY HOSPITAL OF NANCY   (France)

^b INSERM   (France)

^c CHU NANCY BRABOIS   (France)

Author keywords

1795 1797dup; Anaplastic thyroid carcinoma; BRAF; P53; Papillary thyroid carcinoma; SOX2; T1799A; T599dup; Tall cell variant; V600E

Indexed keywords

EID: 80052109496     PISSN: 00313025     EISSN: 14653931     Source Type: Journal    
DOI: 10.1097/PAT.0b013e3283486178     Document Type: Article

References (60)

1. Bongarzone I, Butti MG, Coronelli S, et al. Frequent activation of ret protooncogene by fusion with a new activating gene in papillary thyroid carcinomas. Cancer Res 1994; 54: 2979-85.
2. Bounacer A, Wicker R, Caillou B, et al. High prevalence of activating ret proto-oncogene rearrangements, in thyroid tumors from patients who had received external radiation. Oncogene 1997; 15: 1263-73.
3. Rabes HM, Demidchik EP, Sidorow JD, et al. Pattern of radiation-induced RET and NTRK1 rearrangements in 191 post-chernobyl papillary thyroid carcinomas: Biological, phenotypic, and clinical implications. Clin Cancer Res 2000; 6: 1093-103.
4. Bongarzone I, Vigneri P, Mariani L, et al. RET/NTRK1 rearrangements in thyroid gland tumors of the papillary carcinoma family: Correlation with clinicopathological features. Clin Cancer Res 1998; 4: 223-8.
5. Musholt TJ, Musholt PB, Khaladj N, et al. Prognostic significance of RET and NTRK1 rearrangements in sporadic papillary thyroid carcinoma. Surgery 2000; 128: 984-93.
6. Cohen Y, Xing M, Mambo E, et al. BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst 2003; 95: 625-7.
7. Kimura ET, Nikiforova MN, Zhu Z, et al. 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: 1454-7.
8. Xu X, Quiros RM, Gattuso P, et al. High prevalence of BRAF gene mutation in papillary thyroid carcinomas and thyroid tumor cell lines. Cancer Res 2003; 63: 4561-7.
9. Soares P, Trovisco V, Rocha AS, et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 2003; 22: 4578-80.
10. Xing M, Vasko V, Tallini G, et al. BRAF T1796A transversion mutation in various thyroid neoplasms. J Clin Endocrinol Metab 2004; 89: 1365-8.
11. Xing M, Westra WH, Tufano RP, et al. BRAF mutation predicts a poorer clinical prognosis for papillary thyroid cancer. J Clin Endocrinol Metab 2005; 90: 6373-9.
12. O'Neill CJ, Bullock M, Chou A, et al. BRAF(V600E) mutation is associated with an increased risk of nodal recurrence requiring reoperativesurgery in patients with papillary thyroid cancer. Surgery 2010; 148: 1139- 45; discussion 45-6.
13. Brzezianska E, Pastuszak-Lewandoska D, Wojciechowska K, et al. Investigation of V600E BRAF mutation in papillary thyroid carcinoma in the Polish population. Neuro Endocrinol Lett 2007; 28: 351-9.
14. Ciampi R, Knauf JA, Kerler R, et al. Oncogenic AKAP9-BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. J Clin Invest 2005; 115: 94-101.
15. Moretti S, Macchiarulo A, De Falco V, et al. Biochemical and molecular characterization of the novel BRAF(V599Ins) mutation detected in a classic papillary thyroid carcinoma. Oncogene 2006; 25: 4235-40.
16. Kitamura Y, Shimizu K, Tanaka S, et al. Allelotyping of anaplastic thyroid carcinoma: Frequent allelic losses on 1q, 9p, 11, 17, 19p, and 22q. Genes Chromosomes Cancer 2000; 27: 244-51.
17. Kleer CG, Bryant BR, Giordano TJ, et al. Genetic Changes in Chromosomes 1p and 17p in Thyroid Cancer Progression. Endocr Pathol 2000; 11: 137-43.
18. Wilkens L, Benten D, Tchinda J, et al. Aberrations of chromosomes 5 and 8 as recurrent cytogenetic events in anaplastic carcinoma of the thyroid as detected by fluorescence in situ hybridisation and comparative genomic hybridisation. Virchows Arch 2000; 436: 312-8.
19. Donghi R, Longoni A, Pilotti S, et al. Gene p53 mutations are restricted to poorly differentiated and undifferentiated carcinomas of the thyroid gland. J Clin Invest 1993; 91: 1753-60.
20. Gimm O, Perren A, Weng LP, et al. Differential nuclear and cytoplasmic expression of PTEN in normal thyroid tissue, and benign and malignant epithelial thyroid tumors. Am J Pathol 2000; 156: 1693-700.
21. Lee JJ, Au AY, Foukakis T, et al. Array-CGH identifies cyclin D1 and UBCH10 amplicons in anaplastic thyroid carcinoma. Endocr Relat Cancer 2008; 15: 801-15.
22. Quiros RM, Ding HG, Gattuso P, et al. Evidence that one subset of anaplastic thyroid carcinomas are derived from papillary carcinomas due to BRAF and p53 mutations. Cancer 2005; 103: 2261-8.
23. Nikiforova MN, Kimura ET, Gandhi M, et al. 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: 5399-404.
24. Hong H, Takahashi K, Ichisaka T, et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009; 460: 1132-5.
25. Wegner M. From head to toes: The multiple facets of Sox proteins. Nucleic Acids Res 1999; 27: 1409-20.
26. Sholl LM, Barletta JA, Yeap BY, et al. Sox2 protein expression is an independent poor prognostic indicator in stage I lung adenocarcinoma. Am J Surg Pathol 2010; 34: 1193-8.
27. Hussenet T, Dembele D, Martinet N, et al. An adult tissue-specific stem cell molecular phenotype is activated in epithelial cancer stem cells and correlated to patient outcome. Cell Cycle 2010; 9: 321-7.
28. Rodriguez-Pinilla SM, Sarrio D, Moreno-Bueno G, et al. Sox2: A possible driver of the basal-like phenotype in sporadic breast cancer. Mod Pathol 2007; 20: 474-81.
29. Ji J, Zheng PS. Expression of Sox2 in human cervical carcinogenesis. Hum Pathol 2010; 41: 1438-47.
30. DeLellis RA, Williams ED, LiVolsi VA, et al. Tumours of the thyroid and parathyroid. In: DeLellis RA, Lloyd RV, Heitz PU, Eng C, editors. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Endocrine Organs. Lyon: IARC Press, 2004; 49-133.
31. Namba H, Nakashima M, Hayashi T, et al. Clinical implication of hot spot BRAF mutation, V599E, in papillary thyroid cancers. J Clin Endocrinol Metab 2003; 88: 4393-7.
32. Hoque MO, Rosenbaum E, Westra WH, et al. Quantitative assessment of promoter methylation profiles in thyroid neoplasms. J Clin Endocrinol Metab 2005; 90: 4011-8.
33. Musholt PB, Musholt TJ, Morgenstern SC, et al. Follicular histotypes of oncocytic thyroid carcinomas do not carry mutations of the BRAF hot-spot. World J Surg 2008; 32: 722-8.
34. Proietti A, Giannini R, Ugolini C, et al. BRAF status of follicular variant of papillary thyroid carcinoma and its relationship to its clinical and cytological features. Thyroid 2010; 20: 1263-70.
35. Dibb NJ, Dilworth SM, Mol CD. Switching on kinases: Oncogenic activation of BRAF and the PDGFR family. Nat Rev Cancer 2004; 4: 718-27.
36. Knauf JA, Fagin JA. Role of MAPK pathway oncoproteins in thyroid cancer pathogenesis and as drug targets. Curr Opin Cell Biol 2009; 21: 296-303.
37. Carta C, Moretti S, Passeri L, et al. Genotyping of an Italian papillary thyroid carcinoma cohort revealed high prevalence of BRAF mutations, absence of RAS mutations and allowed the detection of a new mutation of BRAF oncoprotein (BRAF(V599lns)). Clin Endocrinol (Oxf) 2006; 64: 105-9.
38. Eisenhardt AE, Olbrich H, Roring M, et al. Functional characterization of a BRAF insertion mutant associated with pilocytic astrocytoma. Int J Cancer 2010; Dec 28: (Epub ahead of print).
39. Michels JJ, Jacques M, Henry-Amar M, et al. Prevalence and prognostic significance of tall cell variant of papillary thyroid carcinoma. Hum Pathol 2007; 38: 212-9.
40. Adeniran AJ, Zhu Z, Gandhi M, et al. Correlation between genetic alterations and microscopic features, clinical manifestations, and prognostic characteristics of thyroid papillary carcinomas. Am J Surg Pathol 2006; 30: 216-22.
41. Frasca F, Nucera C, Pellegriti G, et al. BRAF(V600E) mutation and the biology of papillary thyroid cancer. Endocr Relat Cancer 2008; 15: 191-205.
42. Lane DP. Benchimol S. p53: Oncogene or anti-oncogene? Genes Dev 1990; 4: 1-8.
43. Dobashi Y, Sakamoto A, Sugimura H, et al. Overexpression of p53 as a possible prognostic factor in human thyroid carcinoma. Am J Surg Pathol 1993; 17: 375-81.
44. Dobashi Y, Sugimura H, Sakamoto A, et al. Stepwise participation of p53 gene mutation during dedifferentiation of human thyroid carcinomas. Diagn Mol Pathol 1994; 3: 9-14.
45. Lam KY, Lo CY, Chan KW, et al. Insular and anaplastic carcinoma of the thyroid: A 45-year comparative study at a single institution and a review of the significance of p53 and p21. Ann Surg 2000; 231: 329-38.
46. Sarig R, Rivlin N, Brosh R, et al. Mutant p53 facilitates somatic cell reprogramming and augments the malignant potential of reprogrammed cells. J Exp Med 2010; 207: 2127-40.
47. Ellis P, Fagan BM, Magness ST, et al. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 2004; 26: 148-65.
48. Chew JL, Loh YH, Zhang W, et al. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 2005; 25: 6031-46.
49. Kamachi Y, Uchikawa M, Kondoh H. Pairing SOX off: With partners in the regulation of embryonic development. Trends Genet 2000; 16: 182-7.
50. Ishii Y, Rex M, Scotting PJ, et al. Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: Regulation by epithelialmesenchymal interactions. Dev Dyn 1998; 213: 464-75.
51. Boyer LA, Lee TI, Cole MF, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005; 122: 947-56.
52. Ben-Porath I, Thomson MW, Carey VJ, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
53. Gen Y, Yasui K, Zen Y, et al. SOX2 identified as a target gene for the amplification at 3q26 that is frequently detected in esophageal squamous cell carcinoma. Cancer Genet Cytogenet 2010; 202: 82-93.
54. Sholl LM, Long KB, Hornick JL. Sox2 expression in pulmonary non-small cell and neuroendocrine carcinomas. Appl Immunohistochem Mol Morphol 2010; 18: 55-61.
55. Lu Y, Futtner C, Rock JR, et al. Evidence that SOX2 overexpression is oncogenic in the lung. PLoS One 2010; 5: E11022.
56. Hussenet T, du Manoir S. SOX2 in squamous cell carcinoma: Amplifying a pleiotropic oncogene along carcinogenesis. Cell Cycle 2010; 9: 1480-6.
57. McCaughan F, Pole JC, Bankier AT, et al. Progressive 3q amplification consistently targets SOX2 in preinvasive squamous lung cancer. Am J Respir Crit Care Med 2010; 182: 83-91.
58. Hamm CA, Xie H, Costa FF, et al. Global demethylation of rat chondrosarcoma cells after treatment with 5-aza-20-deoxycytidine results in increased tumorigenicity. PLoS One 2009; 4: E8340.
59. Kashyap V, Rezende NC, Scotland KB, et al. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 2009; 18: 1093-108.
60. Zhang X, Yu H, Yang Y, et al. SOX2 in gastric carcinoma, but not Hath1, is related to patients' clinicopathological features and prognosis. J Gastrointest Surg 2010; 14: 1220-6.