Tyrosine kinase activating mutations in human malignancies: Implications for diagnostic pathology

Experimental and Molecular Pathology

Volumn 85, Issue 1, 2008, Pages 68-75

  Holden, Joseph A ^a,b   Willmore Payne, Carlynn ^a,b   Layfield, Lester J ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b ARUP INSTITUTE FOR CLINICAL AND EXPERIMENTAL PATHOLOGY   (United States)

Author keywords

BRAF mutations; c kit mutations; DNA melting analysis; Gastrointestinal stromal tumors; Tyrosine kinase activation

Indexed keywords

ANTINEOPLASTIC AGENT; B RAF KINASE; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; GEFITINIB; GENOMIC DNA; IMATINIB; PLACEBO; PROTEIN TYROSINE KINASE; STEM CELL FACTOR RECEPTOR;

CANCER DIAGNOSIS; CANCER THERAPY; CELL PROLIFERATION; CLINICAL TRIAL; COLORECTAL CARCINOMA; COMBINATION CHEMOTHERAPY; DNA DENATURATION; DRUG INHIBITION; DRUG RESPONSE; ENZYME ACTIVATION; GASTROINTESTINAL STROMAL TUMOR; GENE AMPLIFICATION; GENE MUTATION; HUMAN; LUNG NON SMALL CELL CANCER; MELANOMA; MUTATIONAL ANALYSIS; NEOPLASM; PROSTATE CANCER; RECOMMENDED DRUG DOSE; REVIEW; THYROID CANCER; TUMOR REGRESSION;

COLONIC NEOPLASMS; DNA; DNA MUTATIONAL ANALYSIS; FEMALE; GASTROINTESTINAL STROMAL TUMORS; GENES, ERBB-2; HUMANS; MALE; MELANOMA; MUTATION; NEOPLASMS; NUCLEIC ACID DENATURATION; PROSTATIC NEOPLASMS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, EPIDERMAL GROWTH FACTOR; THYROID NEOPLASMS;

EID: 46749158639     PISSN: 00144800     EISSN: 10960945     Source Type: Journal    
DOI: 10.1016/j.yexmp.2008.03.010     Document Type: Review

References (94)

1. Alexeev V., and Yoon K. Distinctive role of the cKit receptor tyrosine kinase signaling in mammalian melanocytes. J. Invest. Dermatol. 126 (2006) 1102-1110
2. Antonescu C.R., Busam K.J., Francone T.D., et al. L576P KIT mutation in anal melanomas correlates with KIT protein expression and is sensitive to specific kinase inhibition. Int. J. Cancer 121 (2007) 257-264
3. Baselga J. Targeting tyrosine kinases in cancer: the second wave. Science 312 (2006) 1175-1178
4. Blume-Jensen P., and Hunter T. Oncogenic kinase signalling. Nature 411 (2001) 355-365
5. Bock-Axelsen J., Lotem J., Sachs L., et al. Genes overexpressed in different human solid cancers exhibit different tissue-specific expression profiles. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 13122-13127
6. Bublil E.M., and Yarden Y. The EGF receptor family: spearheading a merger of signaling and therapeutics. Curr. Opin. Cell Biol. 19 (2007) 124-134
7. Bukowski R., Cella D., Gondek K., et al. Sorafenib TARGETs Clinical Trial Group. Effects of sorafenib on symptoms and quality of life: results from a large randomized placebo-controlled study in renal cancer. Am. J. Clin. Oncol. 30 (2007) 220-227
8. Chirieac L.R., Trent J.C., Steinert D.M., et al. Correlation of immunophenotype with progression-free survival in patients with gastrointestinal stromal tumors treated with imatinib mesylate. Cancer 107 (2006) 2237-2244
9. Cho N.Y., Choi M., Kim B.H., Cho Y.M., Moon K.C., and Kang G.H. BRAF and KRAS mutations in prostatic adenocarcinoma. Int. J. Cancer 119 (2006) 1858-1862
10. ClinicalTrials.gov (NCT00424515) Imatinib in Patients with Mucosal or Acral/Lentiginous Melanoma.
11. ClinicalTrials.gov. (NCT00470470) Imatinib Mesylate in Treating Patients with Stage III or Stage IV Melanoma That Cannot Be Removed by Surgery.
12. Corless C.L., Fletcher J.A., and Heinrich M.C. Biology of gastrointestinal stromal tumors. J. Clin. Oncol. 22 (2004) 3813-3825
13. Corless C.L., Schroeder A., Griffith D., et al. PDGFRA mutations in gastrointestinal stromal tumors: frequency, spectrum and in vitro sensitivity to imatinib. J. Clin. Oncol. 23 (2005) 5357-5364
14. Curtin J.A., Fridlyand J., Kageshita T., et al. Distinct sets of genetic alterations in melanoma. N. Engl. J. Med. 353 (2005) 2135-2147
15. Curtin J.A., Busam K., Pinkel D., and Bastian B.C. Somatic activation of KIT in distinct subtypes of melanoma. J. Clin. Oncol. 24 (2006) 4340-4346
16. Dave S.S. Gene expression signatures and outcome prediction in mature B-cell malignancies. Curr. Treatm. Opt. Oncol. 4 (2006) 261-269
17. Davies H., Bignell G.R., Cox C., et al. Mutations of the BRAF gene in human cancer. Nature 417 (2002) 949-954
18. Debiec-Rychter M., Sciot R., Le C.A., et al. KIT mutations and dose selection for imatinib in patients with advanced gastrointestinal stromal tumours. Eur. J. Cancer 42 (2006) 1093-1103
19. Dhomen N., and Marais R. New insight into BRAF mutations in cancer. Curr. Opin. Genet. Dev. 17 (2007) 31-39
20. Druker B.J., Talpaz M., Resta D.J., Peng B., Buchdunger E., Ford J.M., Lydon N.B., Kantarjian H., Capdeville R., Ohno-Jones S., and Sawyers C.L. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 344 (2001) 1031-1037
21. Eisen T., Ahmad T., Flaherty K.T., et al. Sorafenib in advanced melanoma: a Phase II randomised discontinuation trial analysis. Br. J. Cancer 95 (2006) 581-586
22. Escudier B., Lassau N., Angevin E., et al. Phase I trial of sorafenib in combination with IFN alpha-2a in patients with unresectable and/or metastatic renal cell carcinoma or malignant melanoma. Clin. Cancer Res. 13 (2007) 1801-1809
23. Espinosa A.V., Porchia L., and Ringel M.D. Targeting BRAF in thyroid cancer. Br. J. Cancer 96 (2007) 16-20
24. Fan C., Oh D.S., Wessels L., Weigelt B., et al. Concordance among gene-expression-based predictors for breast cancer. N. Engl. J. Med. 355 (2006) 560-569
25. Fehrmann R.S., Li X.Y., van der Zee A.G., et al. Profiling studies in ovarian cancer: a review. Oncologist (2007) 2960-2966
26. Garnett M.J., and Marais R. Guilty as charged: B-RAF is a human oncogene. Cancer Cells 6 (2004) 313-319
27. Giuliani F., and Colucci G. Cetuximab in colon cancer. Int. J. Biol. Markers 22 1 Suppl 4 (2007) S62-S70 (Jan-Mar)
28. Grichnik J.M., Burch J.A., Burchette J., and Shea C.R. The SCF/KIT pathway plays a critical role in the control of normal human melanocyte homeostasis. J. Invest. Dermatol. 111 (1998) 233-238
29. Guo T., Agaram N.P., Wong G.C., et al. Sorafenib inhibits the imatinib-resistant KIT T670I gatekeeper mutation in gastrointestinal stromal tumor. Clin. Cancer Res. 13 (2007) 4874-4881
30. Haller F., Happel N., Schulten H.J., et al. Site-dependent differential KIT and PDGFRA expression in gastric and intestinal gastrointestinal stromal tumors. Mod. Pathol. (2007) (Aug 3; [Electronic publication ahead of print])
31. Hann C.L., and Brahmer J.R. Who should receive epidermal growth factor receptor inhibitors for non-small cell lung cancer and when?. Curr. Treatm. Opt. Oncol. 8 (2007) 28-37
32. Haqq C., Nosrati M., Sudilovsky D., et al. The gene expression signatures of melanoma progression. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6092-6097
33. Hart S., Isozaki K., Moriyama Y., et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279 (1998) 577-580
34. Heinrich M.C., Griffith D.J., Druker B.J., et al. Inhibition of c-kit receptor tyrosine kinase activity by STI 571, a selective tyrosine kinase inhibitor. Blood 96 (2000) 925-932
35. Heinrich M.C., Corless C.L., Duensing A., et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299 (2003) 708-710
36. Heinrich M.C., Corless C.L., Demetri G.D., et al. Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J. Clin. Oncol. 21 (2003) 4342-4349
37. Hernández S., López-Knowles E., Lloreta J., et al. Prospective study of FGFR3 mutations as a prognostic factor in nonmuscle invasive urothelial bladder carcinomas. J. Clin. Oncol. 24 (2006) 3664-3671
38. Herrmann M.G., Durtschi J.D., Bromley L.K., et al. Amplicon DNA melting analysis for mutation scanning and genotyping: cross-platform comparison of instruments and dyes. Clin. Chem. 53 (2007) 150-152
39. Hingorani S.R., Jacobetz M.A., Robertson G.P., et al. Suppression of BRAF(V599E) in human melanoma abrogates transformation. Cancer Res. 63 (2003) 5198-5202
40. Hirota S., and Isozaki K. Pathology of gastrointestinal stromal tumors. Pathol. Int. 56 (2006) 1-9
41. Hirsch F.R., Varella-Garcia M., McCoy J., et al. Increased epidermal growth factor receptor gene copy number detected by fluorescence in situ hybridization associates with increased sensitivity to gefitinib in patients with bronchioloalveolar carcinoma subtypes: a Southwest Oncology Group Study. J. Clin. Oncol. 23 (2005) 6838-6845
42. Hirsch F.R., Varella-Garcia M., Bunn Jr. P.A., et al. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small-cell lung cancer. J. Clin. Oncol. 24 (2006) 5034-5042
43. Hoeflich K.P., Gray D.C., Eby M.T., et al. Oncogenic BRAF is required for tumor growth and maintenance in melanoma models. Cancer Res. 66 (2006) 999-1006
44. Hornick J.L., and Fletcher C.D. Immunohistochemical staining for KIT (CD117) in soft tissue sarcomas is very limited in distribution. Am. J. Clin. Pathol. (2002) 117188-117193
45. Hornick J.L., and Fletcher C.D. The role of KIT in the management of patients with gastrointestinal stromal tumors. Human Pathol. 38 (2007) 679-687
46. Huang S., Jean D., Luca M., Tainsky M.A., and Bar-Eli M. Loss of AP-2 results in downregulation of c-KIT and enhancement of melanoma tumorigenicity and metastasis. EMBO J. 17 (1998) 4358-4369
47. Hudis C.A. Trastuzumab-mechanism of action and use in clinical practice. N. Engl. J. Med. 357 1 (2007) 39-51 (Jul 5)
48. Joensuu H., Roberts P.J., Sarlomo-Rikala M., et al. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N. Engl. J. Med. 344 (2001) 1052-1056
49. Lanzilotta S.G., Grammatica L., Paradiso A., and Simone G. BRAF in papillary thyroid carcinoma. Cell Oncol. 29 (2007) 269-277
50. Laskin J.J., and Sandler A.B. Epidermal growth factor receptor: a promising target in solid tumours. Cancer Treat. Rev. 30 (2004) 1-17
51. Lasota J., Stachura J., and Miettinen M. GISTs with PDGFRA exon 14 mutations represent subset of clinically favorable gastric tumors with epithelioid morphology. Lab. Invest. 86 (2006) 94-100
52. Lee J.H., Lee E.S., and Kim Y.S. Clinicopathologic significance of BRAF V600E mutation in papillary carcinomas of the thyroid: a meta-analysis. Cancer 110 (2007) 38-46
53. Liu R., Wang X., Chen G.Y., et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N. Engl. J. Med. 356 (2007) 217-226
54. Lucas D.R., al-Abbadi M., Tabaczka P., et al. c-Kit expression in desmoid fibromatosis. Comparative immunohistochemical evaluation of two commercial antibodies. Am. J. Clin. Pathol. 119 (2003) 39-45
55. Lynch T.J., Bell D.W., Sordella R., et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350 (2004) 2129-2139
56. Lyons J.F., Wilhelm S., Hibner B., et al. Discovery of a novel Raf kinase inhibitor. Endocr.-Relat. Cancer 8 (2001) 219-225
57. Miettinen M., and Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl. Immunohistochem. Mol. Morphol. 13 (2005) 205-220
58. Miettinen M., Sarlomo-Rikala M., et al. Gastrointestinal stromal tumors and leiomyosarcomas in the colon: a clinicopathologic, immunohistochemical, and molecular genetic study of 44 cases. Am. J. Surg. Pathol. 24 (2000) 1339-1352
59. Mol C.D., Dougan D.R., Schneider T.R., et al. Structural basis for the autoinhibition and STI-571 inhibition of c-Kit tyrosine kinase. J. Biol. Chem. 279 (2004) 31655-31663
60. Paez J.G., Jänne P.A., Lee J.C., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304 (2004) 1497-1500
61. Paik S., Shak S., Tang G., et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351 (2004) 2817-2826
62. Pizzolanti G., Russo L., Richiusa P., et al. Fine-needle aspiration molecular analysis for the diagnosis of papillary thyroid carcinoma through BRAF(V600E) mutation and RET/PTC rearrangement. Thyroid (2007) (Aug 30; [Electronic publication ahead of print])
63. Pollock P.M., Gartside M.G., Dejeza L.C., et al. Frequent activating FGFR2 mutations in endometrial carcinomas parallel germline mutations associated with craniosynostosis and skeletal dysplasia syndromes. Oncogene (2007) (May 21; [Electronic publication ahead of print])
64. Pugh T.J., Bebb G., Barclay L., et al. Correlations of EGFR mutations and increases in EGFR and HER2 copy number to gefitinib response in a retrospective analysis of lung cancer patients. BMC Cancer 7 (2007) 128-139
65. Ramaswamy S., and Golub T.R. DNA microarrays in clinical oncology. J. Clin. Oncol. 20 (2002) 1932-1941
66. Reed G.H., Kent J.O., and Wittwer C.T. High-resolution DNA melting analysis for simple and efficient molecular diagnostics. Pharmacogenomics 8 (2007) 597-608
67. Riely G.J., Politi K.A., Miller V.A., and Pao W. Update on epidermal growth factor receptor mutations in non-small cell lung cancer. Clin. Cancer Res. 12 (2006) 7232-7241
68. Rowe L.R., Bentz B.G., and Bentz J.S. Utility of BRAF V600E mutation detection in cytologically indeterminate thyroid nodules. Cyto J. 3 (2006) 10
69. Rubin B.P., Heinrich M.C., and Corless C.L. Gastrointestinal stromal tumour. Lancet 369 (2007) 1731-1741
70. Samowitz W.S., Sweeney C., Herrick J., et al. Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res. 65 (2005) 6063-6069
71. Sequist L.V., and Lynch T.J. EGFR tyrosine kinase inhibitors in lung cancer: an evolving story. Annu. Rev. Med. (2007) (Aug 20; [Electronic publication ahead of print])
72. Shigematsu H., Lin L., Takahashi T., et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J. Natl. Cancer Inst. 97 (2005) 339-346
73. Shigematsu H., Takahashi T., Nomura M., et al. Somatic mutations of the HER2 kinase domain in lung adenocarcinomas. Cancer Res. 65 (2005) 1642-1646
74. Siddiqui M.A., and Scott L.J. Imatinib: a review of its use in the management of gastrointestinal stromal tumours. Drugs 67 (2007) 805-820
75. Solit D.B., Garraway L.A., Pratilas C.A., et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 439 (2006) 358-362
76. Sordella R., Bell D.W., Haber D.A., and Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 305 (2004) 1163-1167
77. Sotiriou C., and Piccart M.J. Taking gene-expression profiling to the clinic: when will molecular signatures become relevant to patient care?. Nat. Rev., Cancer 7 (2007) 545-553
78. Steeghs N., Nortier J.W., and Gelderblom H. Small molecule tyrosine kinase inhibitors in the treatment of solid tumors: an update of recent developments. Ann. Surg. Oncol. 14 (2007) 942-953
79. Stephens P., Hunter C., Bignell G., et al. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature 431 (2004) 525-526
80. Sumimoto H., Miyagishi M., Miyoshi H., et al. Inhibition of growth and invasive ability of melanoma by inactivation of mutated BRAF with lentivirus-mediated RNA interference. Oncogene 23 (2004) 6031-6039
81. Sumimoto H., Hirata K., Yamagata S., et al. Effective inhibition of cell growth and invasion of melanoma by combined suppression of BRAF (V599E) and Skp2 with lentiviral RNAi. Int. J. Cancer 118 (2006) 472-476
82. Takano T., Ohe Y., Sakamoto H., et al. Epidermal growth factor receptor gene mutations and increased copy numbers predict gefitinib sensitivity in patients with recurrent non-small-cell lung cancer. J. Clin. Oncol. 23 (2005) 6829-6837
83. Tarn C., and Godwin A.K. Molecular research directions in the management of gastrointestinal stromal tumors. Curr. Treatm. Opt. Oncol. 6 (2005) 473-486
84. Ugurel S., Hildenbrand R., Zimpfer A., et al. Lack of clinical efficacy of imatinib in metastatic melanoma. Br. J. Cancer 92 (2005) 1398-1405
85. Ullrich A., and Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell 61 (1990) 203-212
86. Wan P.T., Garnett M.J., Roe S.M., et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116 (2004) 855-867
87. Willmore C., Holden J.A., Zhou L., et al. Detection of c-kit-activating mutations in gastrointestinal stromal tumors by high-resolution amplicon melting analysis. Am. J. Clin. Pathol. 122 (2004) 206-216
88. Willmore-Payne C., Holden J.A., Tripp S., and Layfield L.J. Human malignant melanoma: detection of BRAF- and c-kit-activating mutations by high-resolution amplicon melting analysis. Human Pathol. 36 (2005) 486-493
89. Willmore-Payne C., Holden J.A., Hirschowitz S., et al. BRAF and c-kit gene copy number in mutation-positive malignant melanoma. Human Pathol. 37 (2006) 520-527
90. Willmore-Payne C., Holden J.A., and Layfield L.J. Detection of epidermal growth factor receptor and human epidermal growth factor receptor 2 activating mutations in lung adenocarcinoma by high-resolution melting amplicon analysis: correlation with gene copy number, protein expression, and hormone receptor expression. Human Pathol. 37 (2006) 755-763
91. Wyman K., Atkins M.B., Prieto V., et al. Multicenter Phase II trial of high-dose imatinib mesylate in metastatic melanoma: significant toxicity with no clinical efficacy. Cancer 106 (2006) 2005-2011
92. Yun C.H., Boggon T.J., Li Y., et al. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cells 11 (2007) 217-227
93. Zhang X., and Chang A. Somatic mutations of the epidermal growth factor receptor and non-small-cell lung cancer. J. Med. Genet. 44 (2007) 166-172
94. Zhong H., and Bowen J.P. Molecular design and clinical development of VEGFR kinase inhibitors. Curr. Top. Med. Chem. 7 (2007) 1379-1393