Mutation analysis of BRAF and KIT in circulating melanoma cells at the single cell level

British Journal of Cancer

Volumn 106, Issue 5, 2012, Pages 939-946

  Sakaizawa, K ^a   Goto, Y ^a   Kiniwa, Y ^a   Uchiyama, A ^a   Harada, K ^b   Shimada, S ^a   Saida, T ^c   Ferrone, S ^a   Takata, M ^a   Uhara, H ^a   Okuyama, R ^a  

^a SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

BRAF; circulating tumour cells; HMW MAA; KIT; melanoma; oncogene mutations

Indexed keywords

CD45 ANTIGEN; GLYCOPROTEIN GP 100; MELAN A; MELANOMA ANTIGEN;

ADULT; AGED; ARTICLE; BRAF GENE; CIRCULATING TUMOR CELL; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE MUTATION; GENE SEQUENCE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOMAGNETIC SEPARATION; KIT GENE; MALE; MELANOMA CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE CELL ANALYSIS;

AGED; AGED, 80 AND OVER; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; BASE SEQUENCE; CELL LINE, TUMOR; CELL SEPARATION; DNA MUTATIONAL ANALYSIS; FEMALE; GENES, RAS; GENOTYPE; HUMANS; IMMUNOMAGNETIC SEPARATION; MALE; MART-1 ANTIGEN; MELANOMA; MIDDLE AGED; MOLECULAR TARGETED THERAPY; MUTATION; NEOPLASM PROTEINS; NEOPLASTIC CELLS, CIRCULATING; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-KIT; SEQUENCE ANALYSIS, DNA; SINGLE-CELL ANALYSIS; SKIN NEOPLASMS;

EID: 84857794472     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2012.12     Document Type: Article

References (46)

1. Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, Tibbe AG, Uhr JW, Terstappen LW (2004) Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res 10: 6897-6904 (Pubitemid 39383039)
2. Ausch C, Dandachi N, Buxhofer-Ausch V, Balic M, Huber K, Bauernhofer T, Ogris E, Hinterberger W, Braun S, Schiessel R (2007) Immunomagnetic CD45 depletion does not improve cytokeratin 20 RT-PCR in colorectal cancer. Clin Chem Lab Med 45: 351-356 (Pubitemid 46480895)
3. Becker JC, Brocker EB, Schadendorf D, Ugurel S (2007) Imatinib in melanoma: a selective treatment option based on KIT mutation status? J Clin Oncol 25: e9 (Pubitemid 350002910)
4. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622
5. Buttner C, Henz BM, Welker P, Sepp NT, Grabbe J (1998) Identification of activating c-kit mutations in adult-, but not in childhood-onset indolent mastocytosis: a possible explanation for divergent clinical behavior. J Invest Dermatol 111: 1227-1231 (Pubitemid 29115205)
6. Campoli MR, Chang CC, Kageshita T, Wang X, McCarthy JB, Ferrone S (2004) Human high molecular weight-melanoma-associated antigen (HMW-MAA): a melanoma cell surface chondroitin sulfate proteoglycan (MSCP) with biological and clinical significance. Crit Rev Immunol 24: 267-296 (Pubitemid 40052428)
7. Carvajal RD, Antonescu CR, Wolchok JD, Chapman PB, Roman RA, Teitcher J, Panageas KS, Busam KJ, Chmielowski B, Lutzky J, Pavlick AC, Fusco A, Cane L, Takebe N, Vemula S, Bouvier N, Bastian BC, Schwartz GK (2011) KIT as a therapeutic target in metastatic melanoma. JAMA 305: 2327-2334
8. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, O'Day SJ, Sosman JA, Kirkwood JM, Eggermont AM, Dreno B, Nolop K, Li J, Nelson B, Hou J, Lee RJ, Flaherty KT, McArthur AG (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516
9. Curtin JA, Busam K, Pinkel D, Bastian BC (2006) Somatic activation of KIT in distinct subtypes of melanoma. J Clin Oncol 24: 4340-4346 (Pubitemid 46630793)
10. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, 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 BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA (2002) Mutations of the BRAF gene in human cancer. Nature 417: 949-954 (Pubitemid 34716871)
11. De Giorgi V, Pinzani P, Salvianti F, Panelos J, Paglierani M, Janowska A, Grazzini M, Wechsler J, Orlando C, Santucci M, Lotti T, Pazzagli M, Massi D (2010) Application of a filtration-and isolation-by-size technique for the detection of circulating tumor cells in cutaneous melanoma. J Invest Dermatol 130: 2440-2447
12. Ellison G, Donald E, McWalter G, Knight L, Fletcher L, Sherwood J, Cantarini M, Orr M, Speake G (2010) A comparison of ARMS and DNA sequencing for mutation analysis in clinical biopsy samples. J Exp Clin Cancer Res 29: 132
13. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O'Dwyer PJ, Lee RJ, Grippo JF, Nolop K, Chapman PB (2010) Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 363: 809-819
14. Flores LM, Kindelberger DW, Ligon AH, Capelletti M, Fiorentino M, Loda M, Cibas ES, Janne PA, Krop IE (2010) Improving the yield of circulating tumour cells facilitates molecular characterisation and recognition of discordant HER2 amplification in breast cancer. Br J Cancer 102: 1495-1502
15. Galanzha EI, Shashkov EV, Spring PM, Suen JY, Zharov VP (2009) In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser. Cancer Res 69: 7926-7934
16. Guo J, Si L, Kong Y, FlahertyKT,XuX, Zhu Y,Corless CL, Li L, Li H, Sheng X, Cui C, Chi Z, Li S, Han M, Mao L, Lin X, Du N, Zhang X, Li J, Wang B, Qin S (2011) Phase II, open-label, single-arm trial of imatinib mesylate in patients with metastatic melanoma harboring c-Kit mutation or amplification. J Clin Oncol 29: 2904-2909
17. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, Alvarado R, Ludlam MJ, Stokoe D, Gloor SL, Vigers G, Morales T, Aliagas I, Liu B, Sideris S, Hoeflich KP, Jaiswal BS, Seshagiri S, Koeppen H, Belvin M, Friedman LS, Malek S (2010) RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464: 431-435
18. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, Hussain J, Reis-Filho JS, Springer CJ, Pritchard C, Marais R (2010) Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140: 209-221
19. Hofmann UB, Kauczok-Vetter CS, Houben R, Becker JC (2009) Overexpression of the KIT/SCF in uveal melanoma does not translate into clinical efficacy of imatinib mesylate. Clin Cancer Res 15: 324-329
20. Kitago M, Koyanagi K, Nakamura T, Goto Y, Faries M, O'Day SJ, Morton DL, Ferrone S, Hoon DS (2009) mRNA expression and BRAF mutation in circulating melanoma cells isolated from peripheral blood with high molecular weight melanoma-associated antigen-specific monoclonal antibody beads. Clin Chem 55: 757-764
21. Koyanagi K, Kuo C, Nakagawa T, Mori T, Ueno H, Lorico Jr AR, Wang HJ, Hseuh E, O'Day SJ, Hoon DS (2005) Multimarker quantitative real-time PCR detection of circulating melanoma cells in peripheral blood: relation to disease stage in melanoma patients. Clin Chem 51: 981-988 (Pubitemid 40740878)
22. Krebs MG, Hou JM, Ward TH, Blackhall FH, Dive C (2010) Circulating tumour cells: their utility in cancer management and predicting outcomes. Ther Adv Med Oncol 2: 351-365
23. Lanternier F, Cohen-Akenine A, Palmerini F, Feger F, Yang Y, Zermati Y, Barete S, Sans B, Baude C, Ghez D, Suarez F, Delarue R, Casassus P, Bodemer C, Catteau A, Soppelsa F, Hanssens K, Arock M, Sobol H, Fraitag S, Canioni D, Moussy A, Launay JM, Dubreuil P, Hermine O, Lortholary O (2008) Phenotypic and genotypic characteristics of mastocytosis according to the age of onset. PLoS One 3: e1906
24. Lin J, Goto Y, Murata H, Sakaizawa K, Uchiyama A, Saida T, Takata M (2011) Polyclonality of BRAF mutations in primary melanoma and the selection of mutant alleles during progression. Br J Cancer 104: 464-468
25. Lin J, Takata M, Murata H, Goto Y, Kido K, Ferrone S, Saida T (2009) Polyclonality of BRAF mutations in acquired melanocytic nevi. J Natl Cancer Inst 101: 1423-1427
26. Maheswaran S, Sequist LV, Nagrath S, Ulkus L, Brannigan B, Collura CV, Inserra E, Diederichs S, Iafrate AJ, Bell DW, Digumarthy S, Muzikansky A, Irimia D, Settleman J, Tompkins RG, Lynch TJ, Toner M, Haber DA (2008) Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 359: 366-377
27. Mellado B, Gutierrez L, Castel T, Colomer D, Fontanillas M, Castro J, Estape J (1999) Prognostic significance of the detection of circulating malignant cells by reverse transcriptase-polymerase chain reaction in long-term clinically disease-free melanoma patients. Clin Cancer Res 5: 1843-1848 (Pubitemid 29334467)
28. Meng S, Tripathy D, Shete S, Ashfaq R, Haley B, Perkins S, Beitsch P, Khan A, Euhus D, Osborne C, Frenkel E, Hoover S, Leitch M, Clifford E, Vitetta E, Morrison L, Herlyn D, Terstappen LW, Fleming T, Fehm T, Tucker T, Lane N, Wang J, Uhr J (2004) HER-2 gene amplification can be acquired as breast cancer progresses. Proc Natl Acad Sci USA 101: 9393-9398 (Pubitemid 38812885)
29. Mocellin S, Keilholz U, Rossi CR, Nitti D (2006) Circulating tumor cells: the 'leukemic phase' of solid cancers. Trends Mol Med 12: 130-139
30. Negin BP, Cohen SJ (2010) Circulating tumor cells in colorectal cancer: past, present, and future challenges. Curr Treat Options Oncol 11: 1-13
31. Ossowski L, Aguirre-Ghiso JA (2010) Dormancy of metastatic melanoma. Pigment Cell Melanoma Res 23: 41-56
32. Palmieri G, Strazzullo M, Ascierto PA, Satriano SM, Daponte A, Castello G (1999) Polymerase chain reaction-based detection of circulating melanoma cells as an effective marker of tumor progression. Melanoma Cooperative Group. J Clin Oncol 17: 304-311 (Pubitemid 29022407)
33. Pantel K, Cote RJ, Fodstad O (1999) Detection and clinical importance of micrometastatic disease. J Natl Cancer Inst 91: 1113-1124 (Pubitemid 29330549)
34. Paterlini-Brechot P, Benali NL (2007) Circulating tumor cells (CTC) detection: clinical impact and future directions. Cancer Lett 253: 180-204 (Pubitemid 47017533)
35. Pestrin M, Bessi S, Galardi F, Truglia M, Biggeri A, Biagioni C, Cappadona S, Biganzoli L, Giannini A, Di Leo A (2009) Correlation of HER2 status between primary tumors and corresponding circulating tumor cells in advanced breast cancer patients. Breast Cancer Res Treat 118: 523-530
36. Piyamongkol W, Bermudez MG, Harper JC, Wells D (2003) Detailed investigation of factors influencing amplification efficiency and allele drop-out in single cell PCR: implications for preimplantation genetic diagnosis. Mol Hum Reprod 9: 411-420 (Pubitemid 36874299)
37. Platz A, Egyhazi S, Ringborg U, Hansson J (2008) Human cutaneous melanoma; a review of NRAS and BRAF mutation frequencies in relation to histogenetic subclass and body site. Mol Oncol 1: 395-405
38. Riethdorf S, Pantel K (2010) Advancing personalized cancer therapy by detection and characterization of circulating carcinoma cells. Ann NY Acad Sci 1210: 66-77
39. Romano E, Schwartz GK, Chapman PB, Wolchock JD, Carvajal RD (2011) Treatment implications of the emerging molecular classification system for melanoma. Lancet Oncol 12: 913-922
40. StoeckleinNH, Hosch SB, Bezler M, Stern F,Hartmann CH,Vay C, SiegmundA, Scheunemann P, Schurr P, KnoefelWT, Verde PE, Reichelt U, Erbersdobler A, Grau R, Ullrich A, Izbicki JR, Klein CA (2008) Direct genetic analysis of single disseminated cancer cells for prediction of outcome and therapy selection in esophageal cancer. Cancer Cell 13: 441-453 (Pubitemid 351609446)
41. Suesskind D, Ulmer A, Schiebel U, Fierlbeck G, Spitzer B, Spitzer MS, Bartz-Schmidt KU, Grisanti S (2011) Circulating melanoma cells in peripheral blood of patients with uveal melanoma before and after different therapies and association with prognostic parameters: a pilot study. Acta Ophthalmol 89: 17-24
42. Tarn C, Merkel E, Canutescu AA, Shen W, Skorobogatko Y, Heslin MJ, Eisenberg B, Birbe R, Patchefsky A, Dunbrack R, Arnoletti JP, von Mehren M, Godwin AK (2005) Analysis of KIT mutations in sporadic and familial gastrointestinal stromal tumors: therapeutic implications through protein modeling. Clin Cancer Res 11: 3668-3677 (Pubitemid 40685583)
43. Terheyden P, Houben R, Pajouh P, Thorns C, Zillikens D, Becker JC (2010) Response to imatinib mesylate depends on the presence of the V559Amutated KIT oncogene. J Invest Dermatol 130: 314-316
44. Ulmer A, Schmidt-Kittler O, Fischer J, Ellwanger U, Rassner G, Riethmuller G, Fierlbeck G, Klein CA (2004) Immunomagnetic enrichment, genomic characterization, and prognostic impact of circulating melanoma cells. Clin Cancer Res 10: 531-537 (Pubitemid 38173991)
45. Woodman SE, Davies MA (2010) Targeting KIT in melanoma: a paradigm of molecular medicine and targeted therapeutics. Biochem Pharmacol 80: 568-574
46. Wulfing P, Borchard J, Buerger H, Heidl S, Zanker KS, Kiesel L, Brandt B (2006) HER2-positive circulating tumor cells indicate poor clinical outcome in stage I to III breast cancer patients. Clin Cancer Res 12: 1715-1720