Role of B-RafV600E in differentiated thyroid cancer and preclinical validation of compounds against B-RafV600E

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1795, Issue 2, 2009, Pages 152-161

  Nucera, Carmelo ^a   Goldfarb, Melanie ^b   Hodin, Richard ^a   Parangi, Sareh ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

B RafV600E; Compounds; Differentiated thyroid cancer; Extrathyroidal extension; MAP kinases; Papillary thyroid cancer; Papillary thyroid microcarcinoma; Preclinical validations; Wild type B Raf

Indexed keywords

5 (4 BROMO 2 CHLOROANILINO) 4 FLUORO 1 METHYL 1H BENZIMIDAZOLE 6 CARBOHYDROXAMIC ACID 2 HYDROXYETHYL ESTER; AAL 881; ANTINEOPLASTIC AGENT; B RAF KINASE; B RAF V 600 E KINASE; C 1 1040; IODINE 131; LBT 613; MITOGEN ACTIVATED PROTEIN KINASE; MOTESANIB; PLX 4032; PLX 4720; RADIOACTIVE IODINE; SB 590885; SORAFENIB; THYROXINE; TUMOR MARKER; UNCLASSIFIED DRUG;

CANCER CHEMOTHERAPY; CANCER INCIDENCE; CANCER RECURRENCE; CANCER SIZE; CARCINOGENESIS; CELL PROLIFERATION; DIARRHEA; DRUG MEGADOSE; DRUG RESEARCH; GENE MUTATION; HUMAN; HYPERTENSION; HYPOTHYROIDISM; LOW DRUG DOSE; LYMPH NODE METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; THYROID CANCER; THYROID CARCINOMA; THYROID PAPILLARY CARCINOMA; VALIDATION STUDY;

BENZENESULFONATES; BIOPSY, NEEDLE; HUMANS; ISOQUINOLINES; MUTATION; PROTO-ONCOGENE PROTEINS B-RAF; PYRIDINES; THYROID NEOPLASMS;

EID: 62949115193     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbcan.2009.01.003     Document Type: Review

References (73)

1. S.E.a.E.R.S. Program, www.seer.cancer.gov (2007).
2. NCCN, Practice guidelines in Oncology www.nccn.org (2007).
3. Kondo T., Ezzat S., and Asa S.L. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat. Rev. Cancer 6 (2006) 292-306
4. Ciampi R., and Nikiforov Y.E. RET/PTC rearrangements and BRAF mutations in thyroid tumorigenesis. Endocrinology 148 (2007) 936-941
5. Santoro M., Melillo R.M., Carlomagno F., Fusco A., and Vecchio G. Molecular mechanisms of RET activation in human cancer. Ann. N. Y. Acad. Sci. 963 (2002) 116-121
6. Giordano T., Kuick R., Thomas D.G., Misek D.E., Vinco M., Sanders D., Zhu Z., Ciampi R., Roh M., Shedden K., Gauger P., Doherty G., Thompson N.W., Hanash S., Koenig R.J., and Nikiforov Y.E. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene 24 (2005) 6646-6656
7. Xing M. BRAF mutation in thyroid cancer. Endocr. Relat. Cancer 12 (2005) 245-262
8. Riesco-Eizaguirre G., and Santisteban P. New insights in thyroid follicular cell biology and its impact in thyroid cancer therapy. Endocr. Relat. Cancer 14 (2007) 957-977
9. Rapp U., Goldsborough M.D., Mark G.E., Bonner T.I., Groffen J., Reynolds F.H., and Stephenson J.R. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 4218-4222
10. Leicht D., Balan V., Kaplun A., Singh-Gupta V., Kaplun L., Dobson M., and Tzivion G. Raf kinases: function, regulation and role in human cancer. Biochim. Biophys. Acta 1773 (2007) 1196-1212
11. Kondo T., Nakazawa T., Murata S., Kurebayashi J., Ezzat S., Asa S.L., and Katoh R. Enhanced B-Raf protein expression is independent of V600E mutant status in thyroid carcinomas. Hum. Pathol. 38 (2007) 1810-1818
12. Emuss V., Garnett M., Mason C., and Marais R. Mutations of C-RAF are rare in human cancer because C-RAF has a low basal kinase activity compared with B-RAF. Cancer Res. 65 (2005) 9719-9726
13. Davies H., Bignell G.R., Cox C., Stephens P., Edkins S., Clegg S., Teague J., Woffendin H., Garnett M.J., Bottomley W., Davis N., Dicks E., Ewing R., Floyd Y., Gray K., Hall S., Hawes R., Hughes J., Kosmidou V., Menzies A., Mould C., Parker A., Stevens C., Watt S., Hooper S., Wilson R., Jayatilake H., Gusterson B.A., Cooper C., Shipley J., Hargrave D., Pritchard-Jones K., Maitland N., Chenevix-Trench G., Riggins G.J., Bigner D.D., Palmieri G., Cossu A., Flanagan A., Nicholson A., Ho J.W., Leung S.Y., Yuen S.T., Weber B.L., Seigler H.F., Darrow T.L., Paterson H., Marais R., Marshall C.J., Wooster R., Stratton M.R., and Futreal P.A. Mutations of the BRAF gene in human cancer. Nature 417 (2002) 949-954
14. Soares P., Trovisco V., Rocha A.S., Feijão T., Rebocho A.P., Fonseca E., Vieira de Castro I., Cameselle-Teijeiro J., Cardoso-Oliveira M., and Sobrinho-Simões M. 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 (2004) 572-576
15. Oliveira C., Pinto M., Duval A., Brennetot C., Domingo E., Espín E., Armengol M., Yamamoto H., Hamelin R., Seruca R., and Schwartz Jr. S. BRAF mutations characterize colon but not gastric cancer with mismatch repair deficiency. Oncogene 22 (2003) 9192-9196
16. Brummer T., Martin P., Herzog S., Misawa Y., Daly R.J., and Reth M. Functional analysis of the regulatory requirements of B-Raf and the B-Raf(V600E) oncoprotein. Oncogene 25 (2006) 6262-6276
17. McKay M., and Morrison D.K. Integrating signals from RTKs to ERK/MAPK. Oncogene 26 (2007) 3113-3121
18. Raman M., Chen W., and Cobb M.H. Differential regulation and properties of MAPKs. Oncogene 26 (2007) 3100-3112
19. Turjanski A., Vaqué J.P., and Gutkind J.S. MAP kinases and the control of nuclear events. Oncogene 26 (2007) 3240-3253
20. Dhillon A., and Kolch W. Oncogenic B-Raf mutations: crystal clear at last. Cancer Cell 5 (2004) 303-304
21. Ikenoue T., Hikiba Y., Kanai F., Tanaka Y., Imamura J., Imamura T., Ohta M., Ijichi H., Tateishi K., Kawakami T., Aragaki J., Matsumura M., Kawabe T., and Omata M. Functional analysis of mutations within the kinase activation segment of B-Raf in human colorectal tumors. Cancer Res. 63 (2003) 8132-8137
22. Zhang B., and Guan K.L. Activation of B-Raf kinase requires phosphorylation of the conserved residues Thr598 and Ser601. EMBO J. 19 (2000) 5429-5439
23. Wan P.T., Garnett M.J., Roe S.M., Lee S., Niculescu-Duvaz D., Good V.M., Jones C.M., Marshall C.J., Springer C.J., Barford D., and Marais R. Cancer Genome Project, Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116 (2004) 855-867
24. Tuveson D., Weber B.L., and Herlyn M. BRAF as a potential therapeutic target in melanoma and other malignancies. Cancer Cell 4 (2003) 95-98
25. Xing M. BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocr. Rev. 28 (2007) 742-762
26. Nagataki S., and Nyström E. Epidemiology and primary prevention of thyroid cancer. Thyroid 12 (2002) 889-896
27. Tronko M., Howe G.R., Bogdanova T.I., Bouville A.C., Epstein O.V., Brill A.B., Likhtarev I.A., Fink D.J., Markov V.V., Greenebaum E., Olijnyk V.A., Masnyk I.J., Shpak V.M., McConnell R.J., Tereshchenko V.P., Robbins J., Zvinchuk O.V., Zablotska L.B., Hatch M., Luckyanov N.K., Ron E., Thomas T.L., Voillequé P.G., and Beebe G.W. A cohort study of thyroid cancer and other thyroid diseases after the Chernobyl accident: thyroid cancer in Ukraine detected during first screening. J. Natl. Cancer Inst. 98 (2006) 897-903
28. Mack W., Preston-Martin S., Bernstein L., Qian D., and Xiang M. Reproductive and hormonal risk factors for thyroid cancer in Los Angeles County females. Cancer Epidemiol. Biomarkers Prev. 8 (1999) 991-997
29. Hemminki K., Eng C., and Chen B. Familial risks for nonmedullary thyroid cancer. J. Clin. Endocrinol. Metab. 90 (2005) 5747-5753
30. Oh S., Yoon Y.S., and Shin S.A. Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea National Health Insurance Corporation Study. J. Clin. Oncol. 23 (2005) 4742-4754
31. Mack W., Preston-Martin S., Dal Maso L., Galanti R., Xiang M., Franceschi S., Hallquist A., Jin F., Kolonel L., La Vecchia C., Levi F., Linos A., Lund E., McTiernan A., Mabuchi K., Negri E., Wingren G., and Ron E. A pooled analysis of case-control studies of thyroid cancer: cigarette smoking and consumption of alcohol, coffee, and tea. Cancer Causes Control 14 (2003) 773-785
32. Curtin J.A., Fridlyand J., Kageshita T., Patel H.N., Busam K.J., Kutzner H., Cho K.H., Aiba S., Brocker E.B., LeBoit P.E., Pinkel D., and Bastian B.C. Distinct sets of genetic alterations in melanoma. N. Engl. J. Med. 353 (2005) 2135-2147
33. Frasca F., Nucera C., Pellegriti G., Gangemi P., Attard M., Stella M., Loda M., Vella V., Giordano C., Trimarchi F., Mazzon E., Belfiore A., and Vigneri R. BRAF(V600E) mutation and the biology of papillary thyroid cancer. Endocr. Relat. Cancer 15 (2008) 191-205
34. Leenhardt L., Grosclaude P., Chérié-Challine L., and Thyroid Cancer Committee. Increased incidence of thyroid carcinoma in France: a true epidemic or thyroid nodule management effects? Report from the French Thyroid Cancer Committee. Thyroid 14 (2004) 1056-1060
35. Lee J., 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
36. Elisei R., Ugolini C., Viola D., Lupi C., Biagini A., Giannini R., Romei C., Miccoli P., Pinchera A., and Basolo F. BRAFV600E mutation and outcome of patients with papillary thyroid carcinoma: a 15-year median follow-up study. J. Clin. Endocrinol. Metab. 93 (2008) 3943-3949
37. Rodolico V., Cabibi D., Pizzolanti G., Richiusa P., Gebbia N., Martorana A., Russo A., Amato M.C., Galluzzo A., and Giordano C. BRAF V600E mutation and p27 kip1 expression in papillary carcinomas of the thyroid < or = 1 cm and their paired lymph node metastases. Cancer 110 (2007) 1218-1226
38. Kebebew E., Weng J., Bauer J., Ranvier G., Clark O.H., Duh Q.Y., Shibru D., Bastian B., and Griffin A. The prevalence and prognostic value of BRAF mutation in thyroid cancer. Ann. Surg. 246 (2007) 466-470
39. Namba H., Nakashima M., Hayashi T., Hayashida N., Maeda S., Rogounovitch T.I., Ohtsuru A., Saenko V.A., Kanematsu T., and Yamashita S. Clinical implication of hot spot BRAF mutation, V599E, in papillary thyroid cancers. J. Clin. Endocrinol. Metab. 88 (2003) 4393-4397
40. Musholt P., Musholt T.J., Morgenstern S.C., Worm K., Sheu S.Y., and Schmid K.W. Follicular histotypes of oncocytic thyroid carcinomas do not carry mutations of the BRAF hot-spot. World J. Surg. 32 (2008) 722-728
41. Espinosa A., Porchia L., and Ringel M.D. Targeting BRAF in thyroid cancer. Br. J. Cancer 96 (2007) 16-20
42. Nikiforova M., Ciampi R., Salvatore G., Santoro M., Gandhi M., Knauf J.A., Thomas G.A., Jeremiah S., Bogdanova T.I., Tronko M.D., Fagin J.A., and Nikiforov Y.E. Low prevalence of BRAF mutations in radiation-induced thyroid tumors in contrast to sporadic papillary carcinomas. Cancer Lett. 209 (2004) 1-6
43. Begum S., Rosenbaum E., Henrique R., Cohen Y., Sidransky D., and Westra W.H. BRAF mutations in anaplastic thyroid carcinoma: implications for tumor origin, diagnosis and treatment. Mod. Pathol. 17 (2004) 1359-1363
44. Nikiforova M., Kimura E.T., Gandhi M., Biddinger P.W., Knauf J.A., Basolo F., Zhu Z., Giannini R., Salvatore G., Fusco A., Santoro M., Fagin J.A., and Nikiforov Y.E. BRAF mutations in thyroid tumors are restricted to papillary carcinomas and anaplastic or poorly differentiated carcinomas arising from papillary carcinomas. J. Clin. Endocrinol. Metab. 88 (2003) 5399-5404
45. Santoro M., Carlomagno F., Hay I.D., Herrmann M.A., Grieco M., Melillo R., Pierotti M.A., Bongarzone I., Della Porta G., Berger N., et al. Ret oncogene activation in human thyroid neoplasms is restricted to the papillary cancer subtype. J. Clin. Invest. 89 (1992) 1517-1522
46. Kim T., Kim W.B., Song J.Y., Rhee Y.S., Gong G., Cho Y.M., Kim S.Y., Kim S.C., Hong S.J., and Shong Y.K. The BRAF mutation is not associated with poor prognostic factors in Korean patients with conventional papillary thyroid microcarcinoma. Clin. Endocrinol. (Oxf.) 63 (2005) 588-593
47. Lupi C., Giannini R., Ugolini C., Proietti A., Berti P., Minuto M., Materazzi G., Elisei R., Santoro M., Miccoli P., and Basolo F. Association of BRAF V600E mutation with poor clinicopathological outcomes in 500 consecutive cases of papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 92 (2007) 4085-4090
48. Sedliarou I., Saenko V., Lantsov D., Rogounovitch T., Namba H., Abrosimov A., Lushnikov E., Kumagai A., Nakashima M., Meirmanov S., Mine M., Hayashi T., and Yamashita S. The BRAFT1796A transversion is a prevalent mutational event in human thyroidmicrocarcinoma. Int. J. Oncol. 25 (2004) 1729-1735
49. Trovisco V., Soares P., Preto A., de Castro I.V., Lima J., Castro P., Máximo V., Botelho T., Moreira S., Meireles A.M., Magalhães J., Abrosimov A., Cameselle-Teijeiro J., and Sobrinho-Simões M. Type and prevalence of BRAF mutations are closely associated with papillary thyroid carcinoma histotype and patients' age but not with tumour aggressiveness. Virchows Arch. 446 (2005) 589-595
50. Ugolini C., Giannini R., Lupi C., Salvatore G., Miccoli P., Proietti A., Elisei R., Santoro M., and Basolo F. Presence of BRAF V600E in very early stages of papillary thyroid carcinoma. Thyroid 17 (2007) 381-388
51. Puxeddu E., Durante C., Avenia N., Filetti S., and Russo D. Clinical implications of BRAF mutation in thyroid carcinoma. Trends Endocrinol. Metab. 19 (2008) 138-145
52. Jin L., Sebo T.J., Nakamura N., Qian X., Oliveira A., Majerus J.A., Johnson M.R., and Lloyd R.V. BRAF mutation analysis in fine needle aspiration (FNA) cytology of the thyroid. Diagn. Mol. Pathol. 15 (2006) 136-143
53. Cohen Y., Rosenbaum E., Clark D.P., Zeiger M.A., Umbricht C.B., Tufano R.P., Sidransky D., and Westra W.H. 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 (2004) 2761-2765
54. Salvatore G., Giannini R., Faviana P., Caleo A., Migliaccio I., Fagin J.A., Nikiforov Y.E., Troncone G., Palombini L., Basolo F., and Santoro M. Analysis of BRAF point mutation and RET/PTC rearrangement refines the fine-needle aspiration diagnosis of papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 89 (2004) 5175-5180
55. Baudin E., and Schlumberger M. New therapeutic approaches for metastatic thyroid carcinoma. Lancet Oncol. 8 (2007) 148-156
56. Cooper D., Doherty G.M., Haugen B.R., Kloos R.T., Lee S.L., Mandel S.J., Mazzaferri E.L., McIver B., Sherman S.I., and Tuttle R.M. The American Thyroid Association Guidelines Taskforce. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 16 (2006) 109-142
57. Pacini F., Schlumberger M., Dralle H., Elisei R., Smit J.W., and Wiersinga W. European Thyroid Cancer Taskforce., European Thyroid Cancer Taskforce. European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur. J. Endocrinol. 154 (2006) 787-803
58. Garraway L., Widlund H.R., Rubin M.A., Getz G., Berger A.J., Ramaswamy S., Beroukhim R., Milner D.A., Granter S.R., Du J., Lee C., Wagner S.N., Li C., Golub T.R., Rimm D.L., Meyerson M.L., Fisher D.E., and Sellers W.R. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436 (2005) 117-122
59. Fagin J. How thyroid tumors start and why it matters: kinase mutants as targets for solid cancer pharmacotherapy. J. Endocrinol. 183 (2004) 249-256
60. Tsai J., Lee J.T., Wang W., Cho H., Mamo S., Bremer R., Gillette S., Kong J., Haass N.K., Sproesser K., Li L., Smalley K.S., Fong D., Zhu Y.L., Marimuthu A., Nguyen H., Lam B., Liu J., Cheung I., Rice J., Suzuki Y., Luu C., Settachatgul C., Shellooe R., Cantwell J., Kim S.H., Schlessinger J., Zhang K.Y., West B.L., Powell B., Habets G., Zhang C., Ibrahim P.N., Hirth P., Artis D.R., Herlyn M., and Bollag G. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 3041-3046
61. King A., Patrick D.R., Batorsky R.S., Ho M.L., Do H.T., Zhang S.Y., Kumar R., Rusnak D.W., Takle A.K., Wilson D.M., Hugger E., Wang L., Karreth F., Lougheed J.C., Lee J., Chau D., Stout T.J., May E.W., Rominger C.M., Schaber M.D., Luo L., Lakdawala A.S., Adams J.L., Contractor R.G., Smalley K.S., Herlyn M., Morrissey M.M., Tuveson D.A., and Huang P.S. Demonstration of a genetic therapeutic index for tumors expressing oncogenic BRAF by the kinase inhibitor SB-590885. Cancer Res. 66 (2006) 11100-11105
62. Friday B., Yu C., Dy G.K., Smith P.D., Wang L., Thibodeau S.N., and Adjei A.A. BRAF V600E disrupts AZD6244-induced abrogation of negative feedback pathways between extracellular signal-regulated kinase and Raf proteins. Cancer Res. 68 (2008) 6145-6153
63. Sherman S., Wirth L.J., Droz J.P., Hofmann M., Bastholt L., Martins R.G., Licitra L., Eschenberg M.J., Sun Y.N., Juan T., Stepan D.E., Schlumberger M.J., and Motesanib Thyroid Cancer Study Group. Motesanib diphosphate in progressive differentiated thyroid cancer. N. Engl. J. Med. 359 (2008) 31-42
64. Schweppe R., Klopper J.P., Korch C., Pugazhenthi U., Benezra M., Knauf J.A., Fagin J.A., Marlow L., Copland J.A., Smallridge R.C., and Haugen B.R. DNA profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J. Clin. Endocrinol. Metab. 93 (2008) 4331-4341
65. Beeram M., Patnaik A., and Rowinsky E.K. Raf: a strategic target for therapeutic development against cancer. J. Clin. Oncol. 23 (2005) 6771-6790
66. Salvatore G., De Falco V., Salerno P., Nappi T.C., Pepe S., Troncone G., Carlomagno F., Melillo R.M., Wilhelm S.M., and Santoro M. BRAF is a therapeutic target in aggressive thyroid carcinoma. Clin. Cancer Res. 5 (2006) 1623-1629
67. Kim S., Yazici Y.D., Calzada G., Wang Z.Y., Younes M.N., Jasser S.A., El-Naggar A.K., and Myers J.N. Sorafenib inhibits the angiogenesis and growth of orthotopic anaplastic thyroid carcinoma xenografts in nude mice. Mol. Cancer Ther. 6 (2007) 1785-1792
68. Carlomagno F., Anaganti S., Guida T., Salvatore G., Troncone G., Wilhelm S.M., and Santoro M. BAY 43-9006 inhibition of oncogenic RET mutants. J. Natl. Cancer Inst. 98 (2006) 326-334
69. http://www.pslgroup.com/news/content.nsf/medicalnews/852571020057CCF6852 57384005A45B1?OpenDocument&id=&count=10.
70. Ouyang B., Knauf J.A., Smith E.P., Zhang L., Ramsey T., Yusuff N., Batt D., and Fagin J.A. 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. 12 (2006) 1785-1793
71. Mitsiades C., Negri J., McMullan C., McMillin D.W., Sozopoulos E., Fanourakis G., Voutsinas G., Tseleni-Balafouta S., Poulaki V., Batt D., and Mitsiades N. Targeting BRAFV600E in thyroid carcinoma: therapeutic implications. Mol. Cancer Ther. 6 (2007) 1070-1078
72. Sathornsumetee S., Hjelmeland A.B., Keir S.T., McLendon R.E., Batt D., Ramsey T., Yusuff N., Rasheed B.K., Kieran M.W., Laforme A., Bigner D.D., Friedman H.S., and Rich J.N. AAL881, a novel small molecule inhibitor of RAF and vascular endothelial growth factor receptor activities, blocks the growth of malignant glioma. Cancer Res. 66 (2006) 8722-8730
73. Sala E., Mologni L., Truffa S., Gaetano C., Bollag G.E., and Gambacorti-Passerini C. BRAF silencing by short hairpin RNA or chemical blockade by PLX4032 leads to different responses in melanoma and thyroid carcinoma cells. Mol. Cancer Res. 6 (2008) 751-759