Tumor Homogeneity between Primary and Metastatic Sites for BRAF Status in Metastatic Melanoma Determined by Immunohistochemical and Molecular Testing

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Boursault, Lucile ^a   Haddad, Véronique ^a   Vergier, Béatrice ^a   Cappellen, David ^a   Verdon, Severine ^a   Bellocq, Jean Pierre ^b   Jouary, Thomas ^a   Merlio, Jean Philippe ^a  

^a BORDEAUX UNIVERSITY HOSPITAL   (France)

^b UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; B RAF KINASE; B RAF KINASE ANTIBODY; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BRAF GENE; CANCER CELL; CANCER STAGING; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; METASTATIC MELANOMA; MUTATIONAL ANALYSIS; ONCOGENE; PREDICTIVE VALUE; PREVALENCE; SCORING SYSTEM; SENSITIVITY AND SPECIFICITY;

GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; MELANOMA; MUTATION; NEOPLASM STAGING; NUCLEIC ACID DENATURATION; PROTO-ONCOGENE PROTEINS B-RAF; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; SKIN NEOPLASMS;

EID: 84882715124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070826     Document Type: Article

References (50)

1. Forsea AM, Del Marmol V, De Vries E, Bailey EE, Geller AC, (2012) Melanoma incidence and mortality in Europe: new estimates, persistent disparities. Br J Dermatol 167: 1124-1130 doi:10.1111/j.1365-2133.2012.11125.x.
2. GLOBOCAN 2008 (n.d.). Available: http://globocan.iarc.fr/. Accessed 2013 Jan 20.
3. Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, et al. (2012) Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 62: 220-241 doi:10.3322/caac.21149.
4. Chapman PB, Einhorn LH, Meyers ML, Saxman S, Destro AN, et al. (1999) Phase III multicenter randomized trial of the Dartmouth regimen versus dacarbazine in patients with metastatic melanoma. J Clin Oncol 17: 2745-2751.
5. Atkins MB, Lotze MT, Dutcher JP, Fisher RI, Weiss G, et al. (1999) High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 17: 2105-2116.
6. Middleton MR, Grob JJ, Aaronson N, Fierlbeck G, Tilgen W, et al. (2000) Randomized phase III study of temozolomide versus dacarbazine in the treatment of patients with advanced metastatic malignant melanoma. J Clin Oncol 18: 158-166.
7. Curtin JA, Fridlyand J, Kageshita T, Patel HN, Busam KJ, et al. (2005) Distinct sets of genetic alterations in melanoma. N Engl J Med 353: 2135-2147 doi:10.1056/NEJMoa050092.
8. Hacker E, Nagore E, Cerroni L, Woods SL, Hayward NK, et al. (2012) NRAS and BRAF Mutations in Cutaneous Melanoma and the Association with MC1R Genotype: Findings from Spanish and Austrian Populations. J Invest Dermatol doi:10.1038/jid.2012.385.
9. Long GV, Menzies AM, Nagrial AM, Haydu LE, Hamilton AL, et al. (2011) Prognostic and Clinicopathologic Associations of Oncogenic BRAF in Metastatic Melanoma. JCO 29: 1239-1246 doi:10.1200/JCO.2010.32.4327.
10. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, et al. (2002) Mutations of the BRAF gene in human cancer. Nature 417: 949-954 doi:10.1038/nature00766.
11. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, et al. (2010) Inhibition of Mutated, Activated BRAF in Metastatic Melanoma. New England Journal of Medicine 363: 809-819 doi:10.1056/NEJMoa1002011.
12. Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, et al. (2012) Survival in BRAF V600-Mutant Advanced Melanoma Treated with Vemurafenib. New England Journal of Medicine 366: 707-714 doi:10.1056/NEJMoa1112302.
13. Fecher LA, Amaravadi RK, Flaherty KT, (2008) The MAPK pathway in melanoma. Curr Opin Oncol 20: 183-189 doi:10.1097/CCO.0b013e3282f5271c.
14. Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, et al. (2002) High frequency of BRAF mutations in nevi. Nature Genetics 33: 19-20 doi:10.1038/ng1054.
15. Yazdi AS, Palmedo G, Flaig MJ, Puchta U, Reckwerth A, et al. (2003) Mutations of the BRAF gene in benign and malignant melanocytic lesions. J Invest Dermatol 121: 1160-1162 doi:10.1046/j.1523-1747.2003.12559.x.
16. Lee J-H, Choi J-W, Kim Y-S, (2011) Frequencies of BRAF and NRAS mutations are different in histological types and sites of origin of cutaneous melanoma: a meta-analysis. Br J Dermatol 164: 776-784 doi:10.1111/j.1365-2133.2010.10185.x.
17. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, et al. (2012) Improved Survival with MEK Inhibition in BRAF-Mutated Melanoma. New England Journal of Medicine 367: 107-114 doi:10.1056/NEJMoa1203421.
18. Hauschild A, Grob J-J, Demidov LV, Jouary T, Gutzmer R, et al. (2012) Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet 380: 358-365 doi:10.1016/S0140-6736(12)60868-X.
19. Long GV, Trefzer U, Davies MA, Kefford RF, Ascierto PA, et al. (2012) Dabrafenib in patients with Val600Glu or Val600Lys BRAF-mutant melanoma metastatic to the brain (BREAK-MB): a multicentre, open-label, phase 2 trial. Lancet Oncol 13: 1087-1095 doi:10.1016/S1470-2045(12)70431-X.
20. Menzies AM, Long GV, Murali R, (2012) Dabrafenib and its potential for the treatment of metastatic melanoma. Drug Des Devel Ther 6: 391-405 doi:10.2147/DDDT.S38998.
21. Rubinstein J, Sznol M, Pavlick A, Ariyan S, Cheng E, et al. (2010) Incidence of the V600K mutation among melanoma patients with BRAF mutations, and potential therapeutic response to the specific BRAF inhibitor PLX4032. Journal of Translational Medicine 8: 67 doi:10.1186/1479-5876-8-67.
22. Dahlman KB, Xia J, Hutchinson K, Ng C, Hucks D, et al. (2012) BRAFL597 Mutations in Melanoma Are Associated with Sensitivity to MEK Inhibitors. Cancer Discovery 2: 791-797 doi:10.1158/2159-8290.CD-12-0097.
23. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, et al. (2012) Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 367: 1694-1703 doi:10.1056/NEJMoa1210093.
24. Colomba E, Hélias-Rodzewicz Z, Von Deimling A, Marin C, Terrones N, et al. (2012) Detection of BRAF p.V600E Mutations in Melanomas: Comparison of Four Methods Argues for Sequential Use of Immunohistochemistry and Pyrosequencing. J Mol Diagn doi:10.1016/j.jmoldx.2012.09.001.
25. Lade-Keller J, Rømer KM, Guldberg P, Riber-Hansen R, Hansen LL, et al. (n.d.) Evaluation of BRAF Mutation Testing Methodologies in Formalin-Fixed Paraffin-Embedded Cutaneous Melanomas. The Journal of Molecular Diagnostics Available: http://www.sciencedirect.com/science/article/pii/S1525157812002620. Accessed 29 November 2012.
26. Curry JL, Torres-Cabala CA, Tetzlaff MT, Bowman C, Prieto VG, (2012) Molecular Platforms Utilized to Detect BRAF V600E Mutation in Melanoma. Semin Cutan Med Surg 31: 267-273 doi:10.1016/j.sder.2012.07.007.
27. Long GV, Wilmott JS, Capper D, Preusser M, Zhang YE, et al. (2012) Immunohistochemistry Is Highly Sensitive and Specific for the Detection of V600E BRAF Mutation in Melanoma. Am J Surg Pathol doi:10.1097/PAS.0b013e31826485c0.
28. Capper D, Preusser M, Habel A, Sahm F, Ackermann U, et al. (2011) Assessment of BRAF V600E mutation status by immunohistochemistry with a mutation-specific monoclonal antibody. Acta Neuropathol 122: 11-19 doi:10.1007/s00401-011-0841-z.
29. Capper D, Berghoff AS, Magerle M, Ilhan A, Wöhrer A, et al. (2012) Immunohistochemical testing of BRAF V600E status in 1,120 tumor tissue samples of patients with brain metastases. Acta Neuropathol 123: 223-233 doi:10.1007/s00401-011-0887-y.
30. Feller JK, Yang S, Mahalingam M, (2012) Immunohistochemistry with a mutation-specific monoclonal antibody as a screening tool for the BRAFV600E mutational status in primary cutaneous malignant melanoma. Mod Pathol doi:10.1038/modpathol.2012.168.
31. Skorokhod A, Capper D, Von Deimling A, Enk A, Helmbold P, (2012) Detection of BRAF V600E mutations in skin metastases of malignant melanoma by monoclonal antibody VE1. J Am Acad Dermatol 67: 488-491 doi:10.1016/j.jaad.2012.03.022.
32. Busam KJ, Hedvat C, Pulitzer M, Von Deimling A, Jungbluth AA, (2013) Immunohistochemical analysis of BRAF(V600E) expression of primary and metastatic melanoma and comparison with mutation status and melanocyte differentiation antigens of metastatic lesions. Am J Surg Pathol 37: 413-420 doi:10.1097/PAS.0b013e318271249e.
33. Colombino M, Capone M, Lissia A, Cossu A, Rubino C, et al. (2012) BRAF/NRAS mutation frequencies among primary tumors and metastases in patients with melanoma. J Clin Oncol 30: 2522-2529 doi:10.1200/JCO.2011.41.2452.
34. Yancovitz M, Litterman A, Yoon J, Ng E, Shapiro RL, et al. (2012) Intra- and inter-tumor heterogeneity of BRAF(V600E))mutations in primary and metastatic melanoma. PLoS ONE 7: e29336 doi:10.1371/journal.pone.0029336.
35. Paternoster SF, Brockman SR, McClure RF, Remstein ED, Kurtin PJ, et al. (2002) A new method to extract nuclei from paraffin-embedded tissue to study lymphomas using interphase fluorescence in situ hybridization. Am J Pathol 160: 1967-1972 doi:10.1016/S0002-9440(10)61146-7.
36. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, et al. (2011) Improved Survival with Vemurafenib in Melanoma with BRAF V600E Mutation. New England Journal of Medicine 364: 2507-2516 doi:10.1056/NEJMoa1103782.
37. Ilie M, Long E, Hofman V, Dadone B, Marquette CH, et al. (2012) Diagnostic value of immunohistochemistry for the detection of the BRAFV600E mutation in primary lung adenocarcinoma Caucasian patients. Ann Oncol doi:10.1093/annonc/mds534.
38. Wilmott JS, Menzies AM, Haydu LE, Capper D, Preusser M, et al. (2013) BRAF(V600E) protein expression and outcome from BRAF inhibitor treatment in BRAF(V600E) metastatic melanoma. Br J Cancer 108: 924-931 doi:10.1038/bjc.2013.29.
39. Tan YH, Liu Y, Eu KW, Ang PW, Li WQ, et al. (2008) Detection of BRAF V600E mutation by pyrosequencing. Pathology 40: 295-298 doi:10.1080/00313020801911512.
40. Spittle C, Ward MR, Nathanson KL, Gimotty PA, Rappaport E, et al. (2007) Application of a BRAF pyrosequencing assay for mutation detection and copy number analysis in malignant melanoma. J Mol Diagn 9: 464-471 doi:10.2353/jmoldx.2007.060191.
41. Cousins MM, Donnell D, Eshleman SH, (2013) Impact of mutation type and amplicon characteristics on genetic diversity measures generated using a high-resolution melting diversity assay. J Mol Diagn 15: 130-137 doi:10.1016/j.jmoldx.2012.08.008.
42. Klein O, Clements A, Menzies AM, O'Toole S, Kefford RF, et al. (2012) BRAF inhibitor activity in V600R metastatic melanoma. Eur J Cancer doi:10.1016/j.ejca.2012.11.004.
43. Dahlman KB, Xia J, Hutchinson K, Ng C, Hucks D, et al. (2012) BRAFL597 Mutations in Melanoma Are Associated with Sensitivity to MEK Inhibitors. Cancer Discovery 2: 791-797 doi:10.1158/2159-8290.CD-12-0097.
44. Anderson S, Bloom KJ, Vallera DU, Rueschoff J, Meldrum C, et al. (2012) Multisite analytic performance studies of a real-time polymerase chain reaction assay for the detection of BRAF V600E mutations in formalin-fixed, paraffin-embedded tissue specimens of malignant melanoma. Arch Pathol Lab Med 136: 1385-1391 doi:10.5858/arpa.2011-0505-OA.
45. Lin J, Goto Y, Murata H, Sakaizawa K, Uchiyama A, et al. (2011) Polyclonality of BRAF mutations in primary melanoma and the selection of mutant alleles during progression. Br J Cancer 104: 464-468 doi:10.1038/sj.bjc.6606072.
46. Jaeger J, Koczan D, Thiesen H-J, Ibrahim SM, Gross G, et al. (2007) Gene expression signatures for tumor progression, tumor subtype, and tumor thickness in laser-microdissected melanoma tissues. Clin Cancer Res 13: 806-815 doi:10.1158/1078-0432.CCR-06-1820.
47. Richtig E, Schrama D, Ugurel S, Fried I, Niederkorn A, et al. (2012) BRAF mutation analysis of only one single metastatic lesion can restrict the treatment of melanoma- a case report. British Journal of Dermatology: no-no doi:10.1111/j.1365-2133.2012.11121.x.
48. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, et al. (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468: 973-977 doi:10.1038/nature09626.
49. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, et al. (2010) RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464: 431-435 doi:10.1038/nature08833.
50. Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, et al. (2011) RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 480: 387-390 doi:10.1038/nature10662.