Routine multiplex mutational profiling of melanomas enables enrollment in genotype-driven therapeutic trials

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Lovly, Christine M ^a   Dahlman, Kimberly Brown ^a   Fohn, Laurel E ^a   Su, Zengliu ^a   Dias Santagata, Dora ^b   Hicks, Donna J ^a   Hucks, Donald ^a   Berry, Elizabeth ^a   Terry, Charles ^a   Duke, MarKeesa ^a   Su, Yingjun ^a   Sobolik Delmaire, Tammy ^a   Richmond, Ann ^a   Kelley, Mark C ^a   Vnencak Jones, Cindy L ^c   Iafrate, A John ^b   Sosman, Jeffrey ^a   Pao, William ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE INHIBITOR; DASATINIB; DNA; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NILOTINIB; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; SUNITINIB; VEMURAFENIB; B RAF KINASE; BRAF PROTEIN, HUMAN; GNA11 PROTEIN, HUMAN; GNAQ PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; NERVE PROTEIN; PROTEIN P21; SHANK2 PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR;

ARTICLE; CANCER CELL CULTURE; CANCER GENETICS; CANCER RESISTANCE; CAPILLARY ELECTROPHORESIS; CLINICAL FEATURE; CLINICAL STUDY; CONTROLLED STUDY; DNA FINGERPRINTING; DRUG SENSITIVITY; GENE FREQUENCY; GENE IDENTIFICATION; GENE MUTATION; GENETIC SCREENING; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; MELANOMA; METASTASIS; MOLECULARLY TARGETED THERAPY; MULTIPLEX POLYMERASE CHAIN REACTION; MULTIPLEX PRIMER EXTENSION; NUCLEIC ACID ANALYSIS; ONCOGENE; ONCOGENE CTNNB1; ONCOGENE GNA11; ONCOGENE GNAQ; ONCOGENE KIT; ONCOGENE N RAS; PATIENT SELECTION; POINT MUTATION; PROCESS DEVELOPMENT; SENSITIVITY ANALYSIS; TISSUE PREPARATION; VALIDATION PROCESS; CLINICAL TRIAL (TOPIC); GENETICS; MALE; MOLECULAR DIAGNOSIS; NUCLEOTIDE SEQUENCE; ORGANIZATION AND MANAGEMENT; SKIN TUMOR; TUMOR CELL LINE;

CELL LINE, TUMOR; CLINICAL TRIALS AS TOPIC; DNA MUTATIONAL ANALYSIS; ELIGIBILITY DETERMINATION; GENETIC TESTING; GTP-BINDING PROTEIN ALPHA SUBUNITS; HUMANS; MALE; MELANOMA; MOLECULAR DIAGNOSTIC TECHNIQUES; NERVE TISSUE PROTEINS; POINT MUTATION; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-KIT; PROTO-ONCOGENE PROTEINS P21(RAS); SKIN NEOPLASMS;

EID: 84859972424     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035309     Document Type: Article

References (56)

1. Siegel R, Ward E, Brawley O, Jemal A, (2011) Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61: 212-236.
2. 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.
3. Curtin JA, Busam K, Pinkel D, Bastian BC, (2006) Somatic activation of KIT in distinct subtypes of melanoma. J Clin Oncol 24: 4340-4346.
4. 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.
5. Fisher DE, Barnhill R, Hodi FS, Herlyn M, Merlino G, et al. (2010) Melanoma from bench to bedside: meeting report from the 6th international melanoma congress. Pigment Cell Melanoma Res 23: 14-26.
6. Van Raamsdonk CD, Bezrookove V, Green G, Bauer J, Gaugler L, et al. (2009) Frequent somatic mutations of GNAQ in uveal melanoma and blue naevi. Nature 457: 599-602.
7. Van Raamsdonk CD, Griewank KG, Crosby MB, Garrido MC, Vemula S, et al. (2010) Mutations in GNA11 in uveal melanoma. N Engl J Med 363: 2191-2199.
8. Delmas V, Beermann F, Martinozzi S, Carreira S, Ackermann J, et al. (2007) Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev 21: 2923-2935.
9. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, et al. (2010) Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 363: 809-819.
10. Sosman J, Kim K, Schuchter L, Gonzalez R, Pavlick A, et al. (2010) An open-label, multicenter Phase II study of continuous oral dosing of RG7204 (PLX4032) in previously treated patients with BRAF V600E mutation-positive metastatic melanoma. Pigment Cell Melanoma Res 23: Abs. 30.
11. Kefford R, Arkenau H, Brown MP, Millward M, Infante JR, et al. (2010) Phase I/II study of GSK2118436, a selective inhibitor of oncogenic mutant BRAF kinase, in patients with metastatic melanoma and other solid tumors. J Clin Oncol 28: abstr 8503.
12. Terheyden P, Houben R, Pajouh P, Thorns C, Zillikens D, et al. (2010) Response to imatinib mesylate depends on the presence of the V559A-mutated KIT oncogene. J Invest Dermatol 130: 314-316.
13. Handolias D, Hamilton AL, Salemi R, Tan A, Moodie K, et al. (2010) Clinical responses observed with imatinib or sorafenib in melanoma patients expressing mutations in KIT. Br J Cancer 102: 1219-1223.
14. Antonescu CR, Busam KJ, Francone TD, Wong GC, Guo T, et al. (2007) L576P KIT mutation in anal melanomas correlates with KIT protein expression and is sensitive to specific kinase inhibition. Int J Cancer 121: 257-264.
15. Lutzky J, Bauer J, Bastian BC, (2008) Dose-dependent, complete response to imatinib of a metastatic mucosal melanoma with a K642E KIT mutation. Pigment Cell Melanoma Res 21: 492-493.
16. Hodi FS, Friedlander P, Corless CL, Heinrich MC, Mac Rae S, et al. (2008) Major response to imatinib mesylate in KIT-mutated melanoma. J Clin Oncol 26: 2046-2051.
17. Jiang X, Zhou J, Yuen NK, Corless CL, Heinrich MC, et al. (2008) Imatinib targeting of KIT-mutant oncoprotein in melanoma. Clin Cancer Res 14: 7726-7732.
18. Carvajal RD, Chapman PB, Wolchok JD, Cane L, Teitcher JB, et al. (2009) A phase II study of imatinib mesylate (IM) for patients with advanced melanma harboring somatic alterations of KIT. J Clin Oncol 27: abstr 9001.
19. Guo J, Si L, Kong Y, Flaherty KT, Xu X, et al. (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.
20. Carvajal RD, Antonescu CR, Wolchok JD, Chapman PB, Roman RA, et al. (2011) KIT as a therapeutic target in metastatic melanoma. JAMA 305: 2327-2334.
21. Jaiswal BS, Janakiraman V, Kljavin NM, Eastham-Anderson J, Cupp JE, et al. (2009) Combined targeting of BRAF and CRAF or BRAF and PI3K effector pathways is required for efficacy in NRAS mutant tumors. PLoS One 4: e5717.
22. Chattopadhyay C, Ellerhorst JA, Ekmekcioglu S, Greene VR, Davies MA, et al. (2011) Association of activated c-Met with NRAS-mutated human melanomas: A possible avenue for targeting. Int J Cancer.
23. Dias-Santagata D, Akhavanfard S, David SS, Vernovsky K, Kuhlmann G, et al. (2010) Rapid targeted mutational analysis of human tumours: a clinical platform to guide personalized cancer medicine. EMBO Mol Med 2: 146-158.
24. Su Z, Dias-Santagata D, Duke M, Hutchinson K, Lin YL, et al. (2011) A platform for rapid detection of multiple oncogenic mutations with relevance to targeted therapy in non-small-cell lung cancer. J Mol Diagn 13: 74-84.
25. Sequist LV, Heist RS, Shaw AT, Fidias P, Rosovsky R, et al. (2011) Implementing multiplexed genotyping of non-small-cell lung cancers into routine clinical practice. Ann Oncol 22: 2616-2624.
26. 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.
27. Xing F, Persaud Y, Pratilas CA, Taylor BS, Janakiraman M, et al. (2011) Concurrent loss of the PTEN and RB1 tumor suppressors attenuates RAF dependence in melanomas harboring (V600E)BRAF. Oncogene.
28. McGuinness C, Wesley UV, (2008) Dipeptidyl peptidase IV (DPPIV), a candidate tumor suppressor gene in melanomas is silenced by promoter methylation. Front Biosci 13: 2435-2443.
29. Zuidervaart W, van der Velden PA, Hurks MH, van Nieuwpoort FA, Out-Luiting CJ, et al. (2003) Gene expression profiling identifies tumour markers potentially playing a role in uveal melanoma development. Br J Cancer 89: 1914-1919.
30. Levy C, Khaled M, Iliopoulos D, Janas MM, Schubert S, et al. (2010) Intronic miR-211 assumes the tumor suppressive function of its host gene in melanoma. Mol Cell 40: 841-849.
31. Tsao H, Goel V, Wu H, Yang G, Haluska FG, (2004) Genetic interaction between NRAS and BRAF mutations and PTEN/MMAC1 inactivation in melanoma. J Invest Dermatol 122: 337-341.
32. Woodman SE, Trent JC, Stemke-Hale K, Lazar AJ, Pricl S, et al. (2009) Activity of dasatinib against L576P KIT mutant melanoma: molecular, cellular, and clinical correlates. Mol Cancer Ther 8: 2079-2085.
33. Yang H, Higgins B, Kolinsky K, Packman K, Go Z, et al. (2010) RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models. Cancer Res 70: 5518-5527.
34. Maldonado JL, Fridlyand J, Patel H, Jain AN, Busam K, et al. (2003) Determinants of BRAF mutations in primary melanomas. J Natl Cancer Inst 95: 1878-1890.
35. 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.
36. Atkins MB, Hsu J, Lee S, Cohen GI, Flaherty LE, et al. (2008) Phase III trial comparing concurrent biochemotherapy with cisplatin, vinblastine, dacarbazine, interleukin-2, and interferon alfa-2b with cisplatin, vinblastine, and dacarbazine alone in patients with metastatic malignant melanoma (E3695): a trial coordinated by the Eastern Cooperative Oncology Group. J Clin Oncol 26: 5748-5754.
37. 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.
38. Falkson CI, Ibrahim J, Kirkwood JM, Coates AS, Atkins MB, et al. (1998) Phase III trial of dacarbazine versus dacarbazine with interferon alpha-2b versus dacarbazine with tamoxifen versus dacarbazine with interferon alpha-2b and tamoxifen in patients with metastatic malignant melanoma: an Eastern Cooperative Oncology Group study. J Clin Oncol 16: 1743-1751.
39. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, et al. (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516.
40. Sosman J, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, et al. (2012) Long-term Survival in Vemurafenib-Treated BRAFV600-mutant Advanced Melanoma. New England Journal of Medicine. In press.
41. Long GV, Menzies AM, Nagrial AM, Haydu LE, Hamilton AL, et al. (2011) Prognostic and Clinicopathologic Associations of Oncogenic BRAF in Metastatic Melanoma. J Clin Oncol 29: 1239-1246.
42. 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.
43. Andre F, Delaloge S, Soria JC, (2011) Biology-Driven Phase II Trials: What Is the Optimal Model for Molecular Selection? J Clin Oncol pp. 1236-1238.
44. King AJ, Patrick DR, Batorsky RS, Ho ML, Do HT, et al. (2006) Demonstration of a genetic therapeutic index for tumors expressing oncogenic BRAF by the kinase inhibitor SB-590885. Cancer Res 66: 11100-11105.
45. Tsai J, Lee JT, Wang W, Zhang J, Cho H, et al. (2008) Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci U S A 105: 3041-3046.
46. Rubinstein JC, Sznol M, Pavlick AC, 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. J Transl Med 8: 67.
47. Infante JR, Fecher LA, Nallapareddy S, Gordon MS, Flaherty K, et al. (2010) Safety and efficacy results from the first-in-human study of the oral MEK 1/2 inhibitor GSK1120212. J Clin Oncol 28: abstr 2503.
48. Beadling C, Jacobson-Dunlop E, Hodi FS, Le C, Warrick A, et al. (2008) KIT gene mutations and copy number in melanoma subtypes. Clin Cancer Res 14: 6821-6828.
49. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N, (2010) RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 464: 427-430.
50. 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.
51. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, et al. (2010) Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140: 209-221.
52. Omholt K, Platz A, Ringborg U, Hansson J, (2001) Cytoplasmic and nuclear accumulation of beta-catenin is rarely caused by CTNNB1 exon 3 mutations in cutaneous malignant melanoma. Int J Cancer 92: 839-842.
53. Reifenberger J, Knobbe CB, Wolter M, Blaschke B, Schulte KW, et al. (2002) Molecular genetic analysis of malignant melanomas for aberrations of the WNT signaling pathway genes CTNNB1, APC, ICAT and BTRC. Int J Cancer 100: 549-556.
54. Demunter A, Libbrecht L, Degreef H, De Wolf-Peeters C, van den Oord JJ, (2002) Loss of membranous expression of beta-catenin is associated with tumor progression in cutaneous melanoma and rarely caused by exon 3 mutations. Mod Pathol 15: 454-461.
55. Bauer J, Kilic E, Vaarwater J, Bastian BC, Garbe C, et al. (2009) Oncogenic GNAQ mutations are not correlated with disease-free survival in uveal melanoma. Br J Cancer 101: 813-815.
56. Dunn EF, Iida M, Myers RA, Campbell DA, Hintz KA, et al. (2010) Dasatinib sensitizes KRAS mutant colorectal tumors to cetuximab. Oncogene 30: 561-574.