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[Cancer Research 63, 1454-1457, April 1, 2003]
© 2003 American Association for Cancer Research

Advances in Brief

High Prevalence of BRAF Mutations in Thyroid Cancer

Genetic Evidence for Constitutive Activation of the RET/PTC-RAS-BRAF Signaling Pathway in Papillary Thyroid Carcinoma1

Edna T. Kimura, Marina N. Nikiforova, Zhaowen Zhu, Jeffrey A. Knauf, Yuri E. Nikiforov and James A. Fagin2

Division of Endocrinology and Metabolism [E. T. K., J. A. K., J. A. F.] and Department of Pathology [M. N. N., Z. Z., Y. E. N.], University of Cincinnati College of Medicine, Cincinnati, Ohio 45267

Thyroid papillary cancers (PTCs) are associated with activating mutations of genes coding for RET or TRK tyrosine kinase receptors, as well as of RAS genes. Activating mutations of BRAF were reported recently in most melanomas and a small proportion of colorectal tumors. Here we show that a somatic mutation of BRAF, V599E, is the most common genetic change in PTCs (28 of 78; 35.8%). BRAFV599E mutations were unique to PTCs, and not found in any of the other types of differentiated follicular neoplasms arising from the same cell type (0 of 46). Moreover, there was no overlap between PTC with RET/PTC, BRAF, or RAS mutations, which altogether were present in 66% of cases. The lack of concordance for these mutations was highly unlikely to be a chance occurrence. Because these signaling proteins function along the same pathway in thyroid cells, this represents a unique paradigm of human tumorigenesis through mutation of three signaling effectors lying in tandem.




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Endocr. Relat. Cancer, September 1, 2006; 13(3): 797 - 826.
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C. C. Lubitz, S. K. Ugras, J. J. Kazam, B. Zhu, T. Scognamiglio, Y.-T. Chen, and T. J. Fahey III
Microarray Analysis of Thyroid Nodule Fine-Needle Aspirates Accurately Classifies Benign and Malignant Lesions
J. Mol. Diagn., September 1, 2006; 8(4): 490 - 498.
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S. Matsukuma, M. Yoshihara, F. Kasai, A. Kato, A. Yoshida, M. Akaike, O. Kobayashi, H. Nakayama, Y. Sakuma, T. Yoshida, et al.
Rapid and Simple Detection of Hot Spot Point Mutations of Epidermal Growth Factor Receptor, BRAF, and NRAS in Cancers Using the Loop-Hybrid Mobility Shift Assay
J. Mol. Diagn., September 1, 2006; 8(4): 504 - 512.
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F. Weber, R. E. Teresi, C. E. Broelsch, A. Frilling, and C. Eng
A Limited Set of Human MicroRNA Is Deregulated in Follicular Thyroid Carcinoma
J. Clin. Endocrinol. Metab., September 1, 2006; 91(9): 3584 - 3591.
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M. R. James, T. Dumeni, M. S. Stark, D. L. Duffy, G. W. Montgomery, N. G. Martin, and N. K. Hayward
Rapid Screening of 4000 Individuals for Germ-line Variations in the BRAF Gene
Clin. Chem., September 1, 2006; 52(9): 1675 - 1678.
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C. Mesa Jr., M. Mirza, N. Mitsutake, M. Sartor, M. Medvedovic, C. Tomlinson, J. A Knauf, G. F. Weber, and J. A. Fagin
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., July 1, 2006; 66(13): 6521 - 6529.
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L Fugazzola, E Puxeddu, N Avenia, C Romei, V Cirello, A Cavaliere, P Faviana, D Mannavola, S Moretti, S Rossi, et al.
Correlation between B-RAFV600E mutation and clinico-pathologic parameters in papillary thyroid carcinoma: data from a multicentric Italian study and review of the literature.
Endocr. Relat. Cancer, June 1, 2006; 13(2): 455 - 464.
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A Bakhsh, G Kirov, J W Gregory, E D Williams, and M Ludgate
A new form of familial multi-nodular goitre with progression to differentiated thyroid cancer.
Endocr. Relat. Cancer, June 1, 2006; 13(2): 475 - 483.
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K. J. Rhoden, K. Unger, G. Salvatore, Y. Yilmaz, V. Vovk, G. Chiappetta, M. B. Qumsiyeh, J. L. Rothstein, A. Fusco, M. Santoro, et al.
RET/Papillary Thyroid Cancer Rearrangement in Nonneoplastic Thyrocytes: Follicular Cells of Hashimoto's Thyroiditis Share Low-Level Recombination Events with a Subset of Papillary Carcinoma
J. Clin. Endocrinol. Metab., June 1, 2006; 91(6): 2414 - 2423.
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M. Eszlinger, M. Wiench, B. Jarzab, K. Krohn, M. Beck, J. Lauter, E. Gubala, K. Fujarewicz, A. Swierniak, and R. Paschke
Meta- and Reanalysis of Gene Expression Profiles of Hot and Cold Thyroid Nodules and Papillary Thyroid Carcinoma for Gene Groups
J. Clin. Endocrinol. Metab., May 1, 2006; 91(5): 1934 - 1942.
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R. P. McCarthy, M. Wang, T. D. Jones, R. W. Strate, and L. Cheng
Molecular Evidence for the Same Clonal Origin of Multifocal Papillary Thyroid Carcinomas
Clin. Cancer Res., April 15, 2006; 12(8): 2414 - 2418.
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T. J. Giordano, A. Y.M. Au, R. Kuick, D. G. Thomas, D. R. Rhodes, K. G. Wilhelm Jr., M. Vinco, D. E. Misek, D. Sanders, Z. Zhu, et al.
Delineation, Functional Validation, and Bioinformatic Evaluation of Gene Expression in Thyroid Follicular Carcinomas with the PAX8-PPARG Translocation.
Clin. Cancer Res., April 1, 2006; 12(7): 1983 - 1993.
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A. Chiloeches and R. Marais
Is BRAF the Achilles' Heel of Thyroid Cancer?
Clin. Cancer Res., March 15, 2006; 12(6): 1661 - 1664.
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B. Ouyang, J. A. Knauf, E. P. Smith, L. Zhang, T. Ramsey, N. Yusuff, D. Batt, and J. A. Fagin
Inhibitors of Raf Kinase Activity Block Growth of Thyroid Cancer Cells with RET/PTC or BRAF Mutations In vitro and In vivo.
Clin. Cancer Res., March 15, 2006; 12(6): 1785 - 1793.
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 Am J EpidemiolHome page
A. J. Canchola, P. L. Horn-Ross, and D. M. Purdie
Risk of Second Primary Malignancies in Women with Papillary Thyroid Cancer
Am. J. Epidemiol., March 15, 2006; 163(6): 521 - 527.
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G. Salvatore, V. De Falco, P. Salerno, T. C. Nappi, S. Pepe, G. Troncone, F. Carlomagno, R. M. Melillo, S. M. Wilhelm, and M. Santoro
BRAF Is a Therapeutic Target in Aggressive Thyroid Carcinoma
Clin. Cancer Res., March 1, 2006; 12(5): 1623 - 1629.
[Abstract] [Full Text] [PDF]

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 Eur J EndocrinolHome page
M. R. Sapio, D. Posca, G. Troncone, G. Pettinato, L. Palombini, G. Rossi, G. Fenzi, and M. Vitale
Detection of BRAF mutation in thyroid papillary carcinomas by mutant allele-specific PCR amplification (MASA)
Eur. J. Endocrinol., February 1, 2006; 154(2): 341 - 348.
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D. J. Panka, W. Wang, M. B. Atkins, and J. W. Mier
The Raf Inhibitor BAY 43-9006 (Sorafenib) Induces Caspase-Independent Apoptosis in Melanoma Cells
Cancer Res., February 1, 2006; 66(3): 1611 - 1619.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
N. Mitsutake, M. Miyagishi, S. Mitsutake, N. Akeno, C. Mesa Jr, J. A. Knauf, L. Zhang, K. Taira, and J. A. Fagin
BRAF Mediates RET/PTC-Induced Mitogen-Activated Protein Kinase Activation in Thyroid Cells: Functional Support for Requirement of the RET/PTC-RAS-BRAF Pathway in Papillary Thyroid Carcinogenesis
Endocrinology, February 1, 2006; 147(2): 1014 - 1019.
[Abstract] [Full Text] [PDF]

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P. Castro, A. P. Rebocho, R. J. Soares, J. Magalhaes, L. Roque, V. Trovisco, I. Vieira de Castro, M. Cardoso-de-Oliveira, E. Fonseca, P. Soares, et al.
PAX8-PPAR{gamma} Rearrangement Is Frequently Detected in the Follicular Variant of Papillary Thyroid Carcinoma
J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 213 - 220.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. Y. M. Au, C. McBride, K. G. Wilhelm Jr., R. J. Koenig, B. Speller, L. Cheung, M. Messina, J. Wentworth, V. Tasevski, D. Learoyd, et al.
PAX8-Peroxisome Proliferator-Activated Receptor {gamma} (PPAR{gamma}) Disrupts Normal PAX8 or PPAR{gamma} Transcriptional Function and Stimulates Follicular Thyroid Cell Growth
Endocrinology, January 1, 2006; 147(1): 367 - 376.
[Abstract] [Full Text] [PDF]

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H. He, K. Jazdzewski, W. Li, S. Liyanarachchi, R. Nagy, S. Volinia, G. A. Calin, C.-g. Liu, K. Franssila, S. Suster, et al.
The role of microRNA genes in papillary thyroid carcinoma
PNAS, December 27, 2005; 102(52): 19075 - 19080.
[Abstract] [Full Text] [PDF]

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K. Mercer, S. Giblett, S. Green, D. Lloyd, S. DaRocha Dias, M. Plumb, R. Marais, and C. Pritchard
Expression of Endogenous Oncogenic V600EB-raf Induces Proliferation and Developmental Defects in Mice and Transformation of Primary Fibroblasts
Cancer Res., December 15, 2005; 65(24): 11493 - 11500.
[Abstract] [Full Text] [PDF]

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B Jarzab, D Handkiewicz-Junak, and J Wloch
Juvenile differentiated thyroid carcinoma and the role of radioiodine in its treatment: a qualitative review
Endocr. Relat. Cancer, December 1, 2005; 12(4): 773 - 803.
[Abstract] [Full Text] [PDF]

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M. Xing, W. H. Westra, R. P. Tufano, Y. Cohen, E. Rosenbaum, K. J. Rhoden, K. A. Carson, V. Vasko, A. Larin, G. Tallini, et al.
BRAF Mutation Predicts a Poorer Clinical Prognosis for Papillary Thyroid Cancer
J. Clin. Endocrinol. Metab., December 1, 2005; 90(12): 6373 - 6379.
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G. Garcia-Rostan, A. M. Costa, I. Pereira-Castro, G. Salvatore, R. Hernandez, M. J.A. Hermsem, A. Herrero, A. Fusco, J. Cameselle-Teijeiro, and M. Santoro
Mutation of the PIK3CA Gene in Anaplastic Thyroid Cancer
Cancer Res., November 15, 2005; 65(22): 10199 - 10207.
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M. G. Borrello, L. Alberti, A. Fischer, D. Degl'Innocenti, C. Ferrario, M. Gariboldi, F. Marchesi, P. Allavena, A. Greco, P. Collini, et al.
Induction of a proinflammatory program in normal human thyrocytes by the RET/PTC1 oncogene
PNAS, October 11, 2005; 102(41): 14825 - 14830.
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M. Beeram, A. Patnaik, and E. K. Rowinsky
Raf: A Strategic Target for Therapeutic Development Against Cancer
J. Clin. Oncol., September 20, 2005; 23(27): 6771 - 6790.
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 GutHome page
A B Hassan and C Paraskeva
Colorectal cancer prognosis: is it all mutation, mutation, mutation?
Gut, September 1, 2005; 54(9): 1209 - 1211.
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V. Guarino, P. Faviana, G. Salvatore, M. D. Castellone, A. M. Cirafici, V. De Falco, A. Celetti, R. Giannini, F. Basolo, R. M. Melillo, et al.
Osteopontin Is Overexpressed in Human Papillary Thyroid Carcinomas and Enhances Thyroid Carcinoma Cell Invasiveness
J. Clin. Endocrinol. Metab., September 1, 2005; 90(9): 5270 - 5278.
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V. Vasko, S. Hu, G. Wu, J. C. Xing, A. Larin, V. Savchenko, B. Trink, and M. Xing
High Prevalence and Possible de Novo Formation of BRAF Mutation in Metastasized Papillary Thyroid Cancer in Lymph Nodes
J. Clin. Endocrinol. Metab., September 1, 2005; 90(9): 5265 - 5269.
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Y.-Z. Feng, T. Shiozawa, T. Miyamoto, H. Kashima, M. Kurai, A. Suzuki, and I. Konishi
BRAF Mutation in Endometrial Carcinoma and Hyperplasia: Correlation with KRAS and p53 Mutations and Mismatch Repair Protein Expression
Clin. Cancer Res., September 1, 2005; 11(17): 6133 - 6138.
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 Epidemiol RevHome page
M. Hatch, E. Ron, A. Bouville, L. Zablotska, and G. Howe
The Chernobyl Disaster: Cancer following the Accident at the Chernobyl Nuclear Power Plant
Epidemiol. Rev., July 1, 2005; 27(1): 56 - 66.
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M. O. Hoque, E. Rosenbaum, W. H. Westra, M. Xing, P. Ladenson, M. A. Zeiger, D. Sidransky, and C. B. Umbricht
Quantitative Assessment of Promoter Methylation Profiles in Thyroid Neoplasms
J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 4011 - 4018.
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 NEJMHome page
T. M. Shattuck, W. H. Westra, P. W. Ladenson, and A. Arnold
Independent Clonal Origins of Distinct Tumor Foci in Multifocal Papillary Thyroid Carcinoma
N. Engl. J. Med., June 9, 2005; 352(23): 2406 - 2412.
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M Xing
BRAF mutation in thyroid cancer
Endocr. Relat. Cancer, June 1, 2005; 12(2): 245 - 262.
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S Rossi, L Fugazzola, L De Pasquale, P Braidotti, V Cirello, P Beck-Peccoz, S Bosari, and A Bastagli
Medullary and papillary carcinoma of the thyroid gland occurring as a collision tumour: report of three cases with molecular analysis and review of the literature
Endocr. Relat. Cancer, June 1, 2005; 12(2): 281 - 289.
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