Assessing the utility of a mutational assay for B-RAF as an adjunct to conventional fine needle aspiration of the thyroid gland

Advances in Anatomic Pathology

Volumn 13, Issue 5, 2006, Pages 228-237

  Tetzlaff, Michael T ^a   LiVolsi, Virginia ^a   Baloch, Zubair W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

B RAF; Fine needle aspiration; Prognosis; Thyroid carcinoma

Indexed keywords

A RAF KINASE; B RAF KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RAF PROTEIN; RAS PROTEIN; SODIUM IODIDE SYMPORTER; THYROGLOBULIN; THYROID PEROXIDASE; TRANSCRIPTION FACTOR PAX8;

ANAPLASTIC CARCINOMA; ASPIRATION BIOPSY; CYTODIAGNOSIS; ENZYME ACTIVITY; GENE MUTATION; HUMAN; MUTATIONAL ANALYSIS; ONCOCYTOMA; ONCOGENE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; THYROID CARCINOMA; THYROID FOLLICULAR CARCINOMA; THYROID MEDULLARY CARCINOMA; THYROID PAPILLARY CARCINOMA;

ADOLESCENT; ADULT; AGE FACTORS; BIOPSY, FINE-NEEDLE; DNA MUTATIONAL ANALYSIS; HUMANS; MIDDLE AGED; MUTATION; PROTO-ONCOGENE PROTEINS B-RAF; RISK FACTORS; THYROID GLAND; THYROID NEOPLASMS;

EID: 33748959570     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/01.pap.0000213044.23823.d3     Document Type: Review

References (87)

1. Hundahl SA, Fleming ID, Fremgen AM, et al. 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.
2. Baloch ZW, LiVolsi VA. Fine-needle aspiration of thyroid nodules: past, present, and future. Endocr Pract. 2004;10:234-241.
3. Soares P, Trovisco V, Rocha AS, et al. 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.
4. 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;63:4561-4567.
5. Xing M. BRAF mutation in thyroid cancer. Endocr Relat Cancer. 2005;12:245-262.
6. Soares P, Trovisco V, Rocha AS, et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene. 2003;22:4578-4580.
7. 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;88:5399-5404.
8. 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;88:4393-4397.
9. 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;63:1454-1457.
10. Fukushima T, Suzuki S, Mashiko M, et al. BRAF mutations in papillary carcinomas of the thyroid. Oncogene. 2003;22:6455-6457.
11. Cohen Y, Xing M, Mambo E, et al. BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst. 2003;95:625-627.
12. Begum S, Rosenbaum E, Henrique R, et al. BRAF mutations in anaplastic thyroid carcinoma: implications for tumor origin, diagnosis and treatment. Mod Pathol. 2004;17:1359-1363.
13. Chen Z, Gibson TB, Robinson F, et al. MAP kinases. Chem Rev. 2001;101:2449-2476.
14. Hubbard SR. Oncogenic mutations in B-Raf: some losses yield gains. Cell. 2004;116:764-766.
15. Hoshino R, Chatani Y, Yamori T, et al. Constitutive activation of the 41-/43-kDa mitogen-activated protein kinase signaling pathway in human tumors. Oncogene. 1999;18:813-822.
16. Bos JL. Ras oncogenes in human cancer: a review. Cancer Res. 1989;49:4682-4689.
17. Davies H, Bignell GR, Cox C, et al. Mutations of the BRAF gene in human cancer. Nature. 2002;417:949-954.
18. Rajagopalan H, Bardelli A, Lengauer C, et al. Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature. 2002;418:934.
19. Brose MS, Volpe P, Feldman M, et al. BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res. 2002;62:6997-7000.
20. Rapp UR, Goldsborough MD, Mark GE, et al. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc Natl Acad Sci U S A. 1983;80:4218-4222.
21. Huebner K, ar-Rushdi A, Griffin CA, et al. Actively transcribed genes in the raf oncogene group, located on the X chromosome in mouse and human. Proc Natl Acad Sci U S A. 1986;83:3934-3938.
22. Jansen HW, Lurz R, Bister K, et al. Homologous cell-derived oncogenes in avian carcinoma virus MH2 and murine sarcoma virus 3611. Nature. 1984;307:281-284.
23. Daum G, Eisenmann-Tappe I, Fries HW, et al. The ins and outs of Raf kinases. Trends Biochem Sci. 1994;19:474-480.
24. Chong H, Vikis HG, Guan KL. Mechanisms of regulating the Raf kinase family. Cell Signal. 2003;15:463-469.
25. Mercer KE, Pritchard CA. Raf proteins and cancer: B-Raf is identified as a mutational target. Biochim Biophys Acta. 2003;1653:25-40.
26. Wan PT, Garnett MJ, Roe SM, et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell. 2004;116:855-867.
27. Yamamori B, Kuroda S, Shimizu K, et al. Purification of a Ras-dependent mitogen-activated protein kinase kinase kinase from bovine brain cytosol and its identification as a complex of B-Raf and 14-3-3 proteins. J Biol Chem. 1995;270:11723-11726.
28. Zhang BH, Guan KL. Activation of B-Raf kinase requires phosphorylation of the conserved residues Thr598 and Ser601. Embo J. 2000;19:5429-5439.
29. Garnett MJ, Marais R. Guilty as charged: B-RAF is a human oncogene. Cancer Cell. 2004;6:313-319.
30. Wellbrock C, Ogilvie L, Hedley D, et al. V599EB-RAF is an oncogene in melanocytes. Cancer Res. 2004;64:2338-2342.
31. Hingorani SR, Jacobetz MA, Robertson GP, et al. Suppression of BRAF(V599E) in human melanoma abrogates transformation. Cancer Res. 2003;63:5198-5202.
32. Nikiforova MN, Biddinger PW, Caudill CM, et al. PAX8-PPARgamma rearrangement in thyroid tumors: RT-PCR and immunohistochemical analyses. Am J Surg Pathol. 2002;26:1016-1023.
33. Marques AR, Espadinha C, Catarino AL, et al. Expression of PAX8-PPAR gamma 1 rearrangements in both follicular thyroid carcinomas and adenomas. J Clin Endocrinol Metab. 2002;87:3947-3952.
34. Kroll TG, Sarraf P, Pecciarini L, et al. PAX8-PPARgamma1 fusion oncogene in human thyroid carcinoma [corrected]. Science. 2000;289:1357-1360.
35. Dwight T, Thoppe SR, Foukakis T, et al. Involvement of the PAX8/peroxisome proliferator-activated receptor gamma rearrangement in follicular thyroid tumors. J Clin Endocrinol Metab. 2003;88:4440-4445.
36. Cheung L, Messina M, Gill A, et al. Detection of the PAX8-PPAR gamma fusion oncogene in both follicular thyroid carcinomas and adenomas. J Clin Endocrinol Metab. 2003;88:354-357.
37. Zhu Z, Gandhi M, Nikiforova MN, et al. Molecular profile and clinical-pathologic features of the follicular variant of papillary thyroid carcinoma. An unusually high prevalence of ras mutations. Am J Clin Pathol. 2003;120:71-77.
38. Vasko V, Ferrand M, Di Cristofaro J, et al. Specific pattern of RAS oncogene mutations in follicular thyroid tumors. J Clin Endocrinol Metab. 2003;88:2745-2752.
39. Suarez HG. Genetic alterations in human epithelial thyroid tumours. Clin Endocrinol (Oxford). 1998;48:531-546.
40. Namba H, Rubin SA, Fagin JA. Point mutations of ras oncogenes are an early event in thyroid tumorigenesis. Mol Endocrinol. 1990;4:1474-1479.
41. Lemoine NR, Mayall ES, Wyllie FS, et al. High frequency of ras oncogene activation in all stages of human thyroid tumorigenesis. Oncogene. 1989;4:159-164.
42. Esapa CT, Johnson SJ, Kendall-Taylor P, et al. Prevalence of Ras mutations in thyroid neoplasia. Clin Endocrinol (Oxford). 1999;50:529-535.
43. Tallini G, Santoro M, Helie M, et al. 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.
44. Santoro M, Carlomagno F, Hay ID, et al. Ret oncogene activation in human thyroid neoplasms is restricted to the papillary cancer subtype. J Clin Invest. 1992;89:1517-1522.
45. Sadetzki S, Calderon-Margalit R, Modan B, et al. Ret/PTC activation in benign and malignant thyroid tumors arising in a population exposed to low-dose external-beam irradiation in childhood. J Clin Endocrinol Metab. 2004;89:2281-2289.
46. Nikiforova MN, Caudill CM, Biddinger P, et al. Prevalence of RET/PTC rearrangements in Hashimoto's thyroiditis and papillary thyroid carcinomas. Int J Surg Pathol. 2002;10:15-22.
47. Elisei R, Romei C, Vorontsova T, et al. 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. 2001;86:3211-3216.
48. Cinti R, Yin L, Ilc K, et al. RET rearrangements in papillary thyroid carcinomas and adenomas detected by interphase FISH. Cytogenet Cell Genet. 2000;88:56-61.
49. 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;15:1263-1273.
50. Trovisco V, Vieira de Castro I, Soares P, et al. BRAF mutations are associated with some histological types of papillary thyroid carcinoma. J Pathol. 2004;202:247-251.
51. Pollock PM, Harper UL, Hansen KS, et al. High frequency of BRAF mutations in nevi. Nat Genet. 2003;33:19-20.
52. 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;30:216-222.
53. Mitsutake N, Knauf JA, Mitsutake S, et al. Conditional BRAFV600E expression induces DNA synthesis, apoptosis, dedifferentiation, and chromosomal instability in thyroid PCCL3 cells. Cancer Res. 2005;65:2465-2473.
54. Knauf JA, Ma X, Smith EP, et al. Targeted expression of BRAFV600E in thyroid cells of transgenic mice results in papillary thyroid cancers that undergo dedifferentiation. Cancer Res. 2005;65:4238-4245.
55. Missero C, Pirro MT, Di Lauro R. Multiple ras downstream pathways mediate functional repression of the homeobox gene product TTF-1. Mol Cell Biol. 2000;20:2783-2793.
56. Giordano TJ, Kuick R, Thomas DG, et al. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene. 2005;24:6646-6656.
57. Porra V, Ferraro-Peyret C, Durand C, et al. Silencing of the tumor suppressor gene SLC5A8 is associated with BRAF mutations in classical papillary thyroid carcinomas. J Clin Endocrinol Metab. 2005;90:3028-3035.
58. Kim N, Lavertu P. Evaluation of a thyroid nodule. Otolaryngol Clin North Am. 2003;36:17-33.
59. Baloch ZW, Sack MJ, Yu GH, et al. Fine-needle aspiration of thyroid: an institutional experience. Thyroid. 1998;8:565-569.
60. Logani S, Gupta PK, LiVolsi VA, et al. Thyroid nodules with FNA cytology suspicious for follicular variant of papillary thyroid carcinoma: follow-up and management. Diagn Cytopathol. 2000;23:380-385.
61. Kesmodel SB, Terhune KP, Canter RJ, et al. The diagnostic dilemma of follicular variant of papillary thyroid carcinoma. Surgery. 2003;134:1005-1112; discussion 1012.
62. Wilson DB, Staren ED, Prinz RA. Thyroid reoperations: indications and risks. Am Surg. 1998;64:674-668; discussion 678-679.
63. Cohen Y, Rosenbaum E, Clark DP, et al. 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. 2004;10:2761-2765.
64. Xing M, Vasko V, Tallini G, et al. BRAF T1796A transversion mutation in various thyroid neoplasms. J Clin Endocrinol Metab. 2004;89:1365-1368.
65. Xing M, Tufano RP, Tufaro AP, et al. Detection of BRAF mutation on fine needle aspiration biopsy specimens: a new diagnostic tool for papillary thyroid cancer. J Clin Endocrinol Metab. 2004;89:2867-2872.
66. Salvatore G, Giannini R, Faviana P, et al. Analysis of BRAF point mutation and RET/PTC rearrangement refines the fine-needle aspiration diagnosis of papillary thyroid carcinoma. J Clin Endocrinol Metab. 2004;89:5175-5180.
67. Puxeddu E, Moretti S, Elisei R, et al. BRAF(V599E) mutation is the leading genetic event in adult sporadic papillary thyroid carcinomas. J Clin Endocrinol Metab. 2004;89:2414-2420.
68. Fugazzola L, Mannavola D, Cirello V, et al. BRAF mutations in an Italian cohort of thyroid cancers. Clin Endocrinol (Oxford). 2004;61:239-243.
69. Trovisco V, Soares P, Preto A, et al. 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.
70. Trovisco V, Soares P, Soares R, et al. A new BRAF gene mutation detected in a case of a solid variant of papillary thyroid carcinoma. Hum Pathol. 2005;36:694-697.
71. Wirtschafter A, Schmidt R, Rosen D, et al. Expression of the RET/PTC fusion gene as a marker for papillary carcinoma in Hashimoto's thyroiditis. Laryngoscope. 1997;107:95-100.
72. Sheils OM, O'Eary JJ, Uhlmann V, et al. ret/PTC-1 Activation in Hashimoto Thyroiditis. Int J Surg Pathol. 2000;8:185-189.
73. Ishizaka Y, Kobayashi S, Ushijima T, et al. Detection of retTPC/PTC transcripts in thyroid adenomas and adenomatous goiter by an RT-PCR method. Oncogene. 1991;6:1667-1672.
74. Schlumberger MJ. Papillary and follicular thyroid carcinoma. N Engl J Med. 1998;338:297-306.
75. LiVolsi VA, Fadda G, Baloch ZW. Prognostic factors in well-differentiated thyroid cancer. Rays. 2000;25:163-175.
76. Hay ID, Bergstralh EJ, Goellner JR, et al. Predicting outcome in papillary thyroid carcinoma: development of a reliable prognostic scoring system in a cohort of 1779 patients surgically treated at one institution during 1940 through 1989. Surgery. 1993;114:1050-1107; discussion 1057-1058.
77. Gilliland FD, Hunt WC, Morris DM, et al. Prognostic factors for thyroid carcinoma. A population-based study of 15,698 cases from the Surveillance, Epidemiology and End Results (SEER) program 1973-1991. Cancer. 1997;79:564-573.
78. Xing M, Westra WH, Tufano RP, et al. BRAF mutation predicts a poorer clinical prognosis for papillary thyroid cancer. J Clin Endocrinol Metab. 2005;90:6373-6379.
79. Kim TY, Kim WB, Song JY, et al. The BRAF mutation is not associated with poor prognostic factors in Korean patients with conventional papillary thyroid microcarcinoma. Clin Endocrinol (Oxford). 2005;63:588-593.
80. Lyons JF, Wilhelm S, Hibner B, et al. Discovery of a novel Raf kinase inhibitor. Endocr Relat Cancer. 2001;8:219-225.
81. Wilhelm SM, Carter C, Tang L, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 2004;64:7099-7109.
82. Strumberg D, Richly H, Hilger RA, et al. Phase I clinical and pharmacokinetic study of the Novel Raf kinase and vascular endothelial growth factor receptor inhibitor BAY 43-9006 in patients with advanced refractory solid tumors. J Clin Oncol. 2005;23:965-972.
83. Siu LL, Awada A, Takimoto CH, et al. Phase I trial of sorafenib and gemcitabine in advanced solid tumors with an expanded cohort in advanced pancreatic cancer. Clin Cancer Res. 2006;12:144-151.
84. Richly H, Henning BF, Kupsch P, et al. Results of a Phase I trial of sorafenib (BAY 43-9006) in combination with doxorubicin in patients with refractory solid tumors. Ann Oncol. 2006;17:866-873.
85. Clark JW, Eder JP, Ryan D, et al. Safety and pharmacokinetics of the dual action Raf kinase and vascular endothelial growth factor receptor inhibitor, BAY 43-9006, in patients with advanced, refractory solid tumors. Clin Cancer Res. 2005;11:5472-5480.
86. Niculescu-Duvaz I, Roman E, Whittaker SR, et al. Novel inhibitors of B-RAF based on a disubstituted pyrazine scaffold. Generation of a nanomolar lead. J Med Chem. 2006;49:407-416.
87. Solit DB, Garraway LA, Pratilas CA, et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature. 2006;439:358-362.