Targeted Therapies for Cutaneous Melanoma

Hematology/Oncology Clinics of North America

Volumn 28, Issue 3, 2014, Pages 491-505

  Kee, Damien ^a,b   McArthur, Grant ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

BRAF; MAPK signaling; MEK; Melanoma; NRAS; Targeted therapy

Indexed keywords

ANTINEOPLASTIC AGENT; BINIMETINIB; COBIMETINIB; DABRAFENIB; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; RAF INHIBITOR; SORAFENIB; TRAMETINIB; UNCLASSIFIED DRUG; VEMURAFENIB; B RAF KINASE; BRAF PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; OXIME; PROTEIN KINASE INHIBITOR; SULFONAMIDE;

ADVANCED CANCER; ARTHRALGIA; BRAF GENE; BRAIN METASTASIS; CANCER COMBINATION CHEMOTHERAPY; CENTRAL SEROUS RETINOPATHY; CHILL; DISEASES; DRUG EFFICACY; DRUG TARGETING; EXON; EYE TOXICITY; FACIAL NERVE PARALYSIS; FATIGUE; FEVER; GENE MUTATION; HEADACHE; HUMAN; HYPERKERATOSIS; KERATOACANTHOMA; MELANOMA; MONOTHERAPY; NAUSEA; NAUSEA AND VOMITING; NEUROTOXICITY; ONCOGENE; ONCOGENE C KIT; ONCOGENE N RAS; OVERALL SURVIVAL; PAPILLOMA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHOTOSENSITIVITY; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; QT PROLONGATION; RASH; REVIEW; SQUAMOUS CELL CARCINOMA; TREATMENT RESPONSE; UVEITIS; ANTAGONISTS AND INHIBITORS; GENETICS; MOLECULARLY TARGETED THERAPY; MUTATION; PROCEDURES; SKIN NEOPLASMS; SURVIVAL;

HUMANS; IMIDAZOLES; INDOLES; MELANOMA; MOLECULAR TARGETED THERAPY; MUTATION; OXIMES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SKIN NEOPLASMS; SULFONAMIDES; SURVIVAL ANALYSIS;

EID: 84901607500     PISSN: 08898588     EISSN: 15581977     Source Type: Journal    
DOI: 10.1016/j.hoc.2014.02.003     Document Type: Review

References (88)

1. Narayanan D.L., Saladi R.N., Fox J.L. Ultraviolet radiation and skin cancer. Int J Dermatol 2010, 49(9):978-986.
2. Balch C.M., Gershenwald J.E., Soong S.J., et al. Final version of 2009 AJCC melanoma staging and classification. JClin Oncol 2009, 27(36):6199-6206.
3. La Porta C.A. Drug resistance in melanoma: new perspectives. Curr Med Chem 2007, 14(4):387-391.
4. Jilaveanu L.B., Aziz S.A., Kluger H.M. Chemotherapy and biologic therapies for melanoma: do they work?. Clin Dermatol 2009, 27(6):614-625.
5. Chapman P.B., Hauschild A., Robert C., et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. NEngl J Med 2011, 364(26):2507-2516.
6. Robert C., Thomas L., Bondarenko I., et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. NEngl J Med 2011, 364(26):2517-2526.
7. Schadendorf D, Hodi FS, Robert C, etal. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in metastatic or locally advanced, unresectable melanoma [Abstract 24]. Presented at: European Cancer Congress. Amsterdam, The Netherlands, September 27-October 1, 2013.
8. Brahmer J.R., Tykodi S.S., Chow L.Q., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. NEngl J Med 2012, 366(26):2455-2465.
9. Topalian S.L., Hodi F.S., Brahmer J.R., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. NEngl J Med 2012, 366(26):2443-2454.
10. Yoon S., Seger R. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 2006, 24(1):21-44.
11. Greaves W.O., Verma S., Patel K.P., et al. Frequency and spectrum of BRAF mutations in a retrospective, single-institution study of 1112 cases of melanoma. JMol Diagn 2013, 15(2):220-226.
12. Long G.V., Menzies A.M., Nagrial A.M., et al. Prognostic and clinicopathologic associations of oncogenic BRAF in metastatic melanoma. JClin Oncol 2011, 29(10):1239-1246.
13. Platz A., Egyhazi S., Ringborg U., et al. Human cutaneous melanoma; a review of NRAS and BRAF mutation frequencies in relation to histogenetic subclass and body site. Mol Oncol 2008, 1(4):395-405.
14. Davies H., Bignell G.R., Cox C., et al. Mutations of the BRAF gene in human cancer. Nature 2002, 417(6892):949-954.
15. Curtin J.A., Busam K., Pinkel D., et al. Somatic activation of KIT in distinct subtypes of melanoma. JClin Oncol 2006, 24(26):4340-4346.
16. Beadling C., Jacobson-Dunlop E., Hodi F.S., et al. KIT gene mutations and copy number in melanoma subtypes. Clin Cancer Res 2008, 14(21):6821-6828.
17. Guo J., Si L., Kong Y., et al. Phase II, open-label, single-arm trial of imatinib mesylate in patients with metastatic melanoma harboring c-Kit mutation or amplification. JClin Oncol 2011, 29(21):2904-2909.
18. Romano E., Schwartz G.K., Chapman P.B., et al. Treatment implications of the emerging molecular classification system for melanoma. Lancet Oncol 2011, 12(9):913-922.
19. Pollock P.M., Harper U.L., Hansen K.S., et al. High frequency of BRAF mutations in nevi. Nat Genet 2003, 33(1):19-20.
20. Gast A., Scherer D., Chen B., et al. Somatic alterations in the melanoma genome: a high-resolution array-based comparative genomic hybridization study. Genes Chromosomes Cancer 2010, 49(8):733-745.
21. Tsao H., Goel V., Wu H., et al. Genetic interaction between NRAS and BRAF mutations and PTEN/MMAC1 inactivation in melanoma. JInvest Dermatol 2004, 122(2):337-341.
22. Wilhelm S.M., Adnane L., Newell P., et al. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol Cancer Ther 2008, 7(10):3129-3140.
23. Eisen T., Ahmad T., Flaherty K.T., et al. Sorafenib in advanced melanoma: a phase II randomised discontinuation trial analysis. Br J Cancer 2006, 95(5):581-586.
24. Ott P.A., Hamilton A., Min C., et al. Aphase II trial of sorafenib in metastatic melanoma with tissue correlates. PLoS One 2010, 5(12):e15588.
25. Flaherty K.T., Lee S.J., Zhao F., et al. Phase III trial of carboplatin and paclitaxel with or without sorafenib in metastatic melanoma. JClin Oncol 2013, 31(3):373-379.
26. Flaherty K.T., Schiller J., Schuchter L.M., et al. Aphase I trial of the oral, multikinase inhibitor sorafenib in combination with carboplatin and paclitaxel. Clin Cancer Res 2008, 14(15):4836-4842.
27. Liu L., Cao Y., Chen C., et al. Sorafenib blocks the RAF/MEK/ERK pathway, inhibits tumor angiogenesis, and induces tumor cell apoptosis in hepatocellular carcinoma model PLC/PRF/5. Cancer Res 2006, 66(24):11851-11858.
28. Tsai J., Lee J.T., Wang W., et al. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci USA 2008, 105(8):3041-3046.
29. Joseph E.W., Pratilas C.A., Poulikakos P.I., et al. The RAF inhibitor PLX4032 inhibits ERK signaling and tumor cell proliferation in a V600E BRAF-selective manner. Proc Natl Acad Sci USA 2010, 107(33):14903-14908.
30. Yang H., Higgins B., Kolinsky K., et al. RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models. Cancer Res 2010, 70(13):5518-5527.
31. Hatzivassiliou G., Song K., Yen I., et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010, 464(7287):431-435.
32. Poulikakos P.I., Zhang C., Bollag G., et al. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010, 464(7287):427-430.
33. Flaherty K.T., Puzanov I., Kim K.B., et al. Inhibition of mutated, activated BRAF in metastatic melanoma. NEngl J Med 2010, 363(9):809-819.
34. Bollag G., Hirth P., Tsai J., et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 2010, 467(7315):596-599.
35. 18F]fluorodeoxyglucose-positron emission tomography responses to vemurafenib in BRAF-mutant advanced melanoma. JClin Oncol 2012, 30(14):1628-1634.
36. Sosman J.A., Kim K.B., Schuchter L., et al. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. NEngl J Med 2012, 366(8):707-714.
37. Korn E.L., Liu P.Y., Lee S.J., et al. Meta-analysis of phase II cooperative group trials in metastatic stage IV melanoma to determine progression-free and overall survival benchmarks for future phase II trials. JClin Oncol 2008, 26(4):527-534.
38. McArthur G.A., Chapman P.B., Robert C., et al. Safety and efficacy of vemurafenib in BRAFV600E and BRAFV600K mutation-positive melanoma (BRIM-3): extended follow-up of a phase 3, randomised, open-label study. Lancet Oncol 2014, 15(3):323-332.
39. Falchook G.S., Long G.V., Kurzrock R., et al. Dabrafenib in patients with melanoma, untreated brain metastases, and other solid tumours: a phase 1 dose-escalation trial. Lancet 2012, 379(9829):1893-1901.
40. Ascierto P.A., Minor D., Ribas A., et al. Phase II trial (BREAK-2) of the BRAF inhibitor dabrafenib (GSK2118436) in patients with metastatic melanoma. JClin Oncol 2013, 31(26):3205-3211.
41. Hauschild A., Grob J.J., Demidov L.V., et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet 2012, 380(9839):358-365.
42. Anderson S., Bloom K.J., Vallera D.U., et al. 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 2012, 136(11):1385-1391.
43. Davies M.A., Liu P., McIntyre S., et al. Prognostic factors for survival in melanoma patients with brain metastases. Cancer 2011, 117(8):1687-1696.
44. Fife K.M., Colman M.H., Stevens G.N., et al. Determinants of outcome in melanoma patients with cerebral metastases. JClin Oncol 2004, 22(7):1293-1300.
45. Agarwala S.S., Kirkwood J.M., Gore M., et al. Temozolomide for the treatment of brain metastases associated with metastatic melanoma: a phase II study. JClin Oncol 2004, 22(11):2101-2107.
46. Margolin K., Ernstoff M.S., Hamid O., et al. Ipilimumab in patients with melanoma and brain metastases: an open-label, phase 2 trial. Lancet Oncol 2012, 13(5):459-465.
47. Mornex F., Thomas L., Mohr P., et al. Aprospective randomized multicentre phase III trial of fotemustine plus whole brain irradiation versus fotemustine alone in cerebral metastases of malignant melanoma. Melanoma Res 2003, 13(1):97-103.
48. Long G.V., Trefzer U., Davies M.A., et al. 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 2012, 13(11):1087-1095.
49. Buckmelter A.J., Ren L., Laird E.R., et al. The discovery of furo[2,3-c]pyridine-based indanone oximes as potent and selective B-Raf inhibitors. Bioorg Med Chem Lett 2011, 21(4):1248-1252.
50. Dummer R., Goldinger S.M., Turtschi C.P., et al. Vemurafenib in patients with BRAF mutation-positive melanoma with symptomatic brain metastases: final results of an open-label pilot study. Eur J Cancer 2014, 50(3):611-621.
51. Gerstner E.R., Fine R.L. Increased permeability of the blood-brain barrier to chemotherapy in metastatic brain tumors: establishing a treatment paradigm. JClin Oncol 2007, 25(16):2306-2312.
52. Su F., Viros A., Milagre C., et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. NEngl J Med 2012, 366(3):207-215.
53. Oberholzer P.A., Kee D., Dziunycz P., et al. RAS mutations are associated with the development of cutaneous squamous cell tumors in patients treated with RAF inhibitors. JClin Oncol 2012, 30(3):316-321.
54. Flaherty K.T., Infante J.R., Daud A., et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. NEngl J Med 2012, 367(18):1694-1703.
55. Zimmer L., Hillen U., Livingstone E., et al. Atypical melanocytic proliferations and new primary melanomas in patients with advanced melanoma undergoing selective BRAF inhibition. JClin Oncol 2012, 30(19):2375-2383.
56. Callahan M.K., Rampal R., Harding J.J., et al. Progression of RAS-mutant leukemia during RAF inhibitor treatment. NEngl J Med 2012, 367(24):2316-2321.
57. Andrews M., Behren A., Chiohn F., et al. BRAF inhibitor-driven tumor proliferation in a KRAS-mutated colon carcinoma is not overcome by MEK1/2 inhibition. JClin Oncol 2013, 31(35):e448-e451.
58. Trunzer K., Pavlick A.C., Schuchter L., et al. Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. JClin Oncol 2013, 31(14):1767-1774.
59. Nazarian R., Shi H., Wang Q., et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010, 468(7326):973-977.
60. Shi H., Moriceau G., Kong X., et al. Melanoma whole-exome sequencing identifies (V600E)B-RAF amplification-mediated acquired B-RAF inhibitor resistance. Nat Commun 2012, 3:724.
61. Poulikakos P.I., Persaud Y., Janakiraman M., et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 2011, 480(7377):387-390.
62. Johannessen C.M., Boehm J.S., Kim S.Y., et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010, 468(7326):968-972.
63. Straussman R., Morikawa T., Shee K., et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012, 487(7408):500-504.
64. Villanueva J., Vultur A., Lee J.T., et al. Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell 2010, 18(6):683-695.
65. Wilson T.R., Fridlyand J., Yan Y., et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012, 487(7408):505-509.
66. Yadav V., Zhang X., Liu J., et al. Reactivation of mitogen-activated protein kinase (MAPK) pathway by FGF receptor 3 (FGFR3)/Ras mediates resistance to vemurafenib in human B-RAF V600E mutant melanoma. JBiol Chem 2012, 287(33):28087-28098.
67. Solit D.B., Garraway L.A., Pratilas C.A., et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 2006, 439(7074):358-362.
68. Rinehart J., Adjei A.A., Lorusso P.M., et al. Multicenter phase II study of the oral MEK inhibitor, CI-1040, in patients with advanced non-small-cell lung, breast, colon, and pancreatic cancer. JClin Oncol 2004, 22(22):4456-4462.
69. LoRusso P.M., Krishnamurthi S.S., Rinehart J.J., et al. Phase I pharmacokinetic and pharmacodynamic study of the oral MAPK/ERK kinase inhibitor PD-0325901 in patients with advanced cancers. Clin Cancer Res 2010, 16(6):1924-1937.
70. Kirkwood J.M., Bastholt L., Robert C., et al. Phase II, open-label, randomized trial of the MEK1/2 inhibitor selumetinib as monotherapy versus temozolomide in patients with advanced melanoma. Clin Cancer Res 2012, 18(2):555-567.
71. Gilmartin A.G., Bleam M.R., Groy A., et al. GSK1120212 (JTP-74057) is an inhibitor of MEK activity and activation with favorable pharmacokinetic properties for sustained invivo pathway inhibition. Clin Cancer Res 2011, 17(5):989-1000.
72. McArthur G, Gonzalez R, Pavlick A, etal. Vemurafenib (VEM) and MEK inhibitor, cobimetinib (GDC-0973), in advanced BRAFV600-mutated melanoma (BRIM7): dose-escalation and expansion results of a phase IB study [Abstract 3703]. Paper presented at: European Cancer Congress. Amsterdam, The Netherlands. September 27-October 1, 2013. Available at:. http://eccamsterdam2013.ecco-org.eu/Scientific-Programme/Abstract-search.aspx?abstractid=7015.
73. Devitt B., Liu W., Salemi R., et al. Clinical outcome and pathological features associated with NRAS mutation in cutaneous melanoma. Pigment Cell Melanoma Res 2011, 24(4):666-672.
74. Jakob J.A., Bassett R.L., Ng C.S., et al. NRAS mutation status is an independent prognostic factor in metastatic melanoma. Cancer 2012, 118(16):4014-4023.
75. Eskandarpour M., Kiaii S., Zhu C., et al. Suppression of oncogenic NRAS by RNA interference induces apoptosis of human melanoma cells. Int J Cancer 2005, 115(1):65-73.
76. Gysin S., Salt M., Young A., et al. Therapeutic strategies for targeting ras proteins. Genes Cancer 2011, 2(3):359-372.
77. Kelleher F.C., McArthur G.A. Targeting NRAS in melanoma. Cancer J 2012, 18(2):132-136.
78. Kwong L.N., Costello J.C., Liu H., et al. Oncogenic NRAS signaling differentially regulates survival and proliferation in melanoma. Nat Med 2012, 18(10):1503-1510.
79. Ascierto P.A., Schadendorf D., Berking C., et al. MEK162 for patients with advanced melanoma harbouring NRAS or Val600 BRAF mutations: a non-randomised, open-label phase 2 study. Lancet Oncol 2013, 14(3):249-256.
80. Delord J.P., Houédé N., Awada A., et al. Pimasertib (MSC1936369B/AS703026), aselective oral MEK1/2 inhibitor, shows clinical activity in melanoma. Eur J Cancer 2012, 48(Suppl):190.
81. Curtin J.A., Fridlyand J., Kageshita T., et al. Distinct sets of genetic alterations in melanoma. NEngl J Med 2005, 353(20):2135-2147.
82. Carvajal R.D., Antonescu C.R., Wolchok J.D., et al. KIT as a therapeutic target in metastatic melanoma. JAMA 2011, 305(22):2327-2334.
83. Hodi F.S., Corless C.L., Giobbie-Hurder A., et al. Imatinib for melanomas harboring mutationally activated or amplified KIT arising on mucosal, acral, and chronically sun-damaged skin. JClin Oncol 2013, 31(26):3182-3190.
84. Quintas-Cardama A., Lazar A.J., Woodman S.E., et al. Complete response of stage IV anal mucosal melanoma expressing KIT Val560Asp to the multikinase inhibitor sorafenib. Nat Clin Pract Oncol 2008, 5(12):737-740.
85. Woodman S.E., Trent J.C., Stemke-Hale K., et al. Activity of dasatinib against L576P KIT mutant melanoma: molecular, cellular, and clinical correlates. Mol Cancer Ther 2009, 8(8):2079-2085.
86. Minor D.R., Kashani-Sabet M., Garrido M., et al. Sunitinib therapy for melanoma patients with KIT mutations. Clin Cancer Res 2012, 18(5):1457-1463.
87. Cho J.H., Kim K.M., Kwon M., et al. Nilotinib in patients with metastatic melanoma harboring KIT gene aberration. Invest New Drugs 2012, 30(5):2008-2014.
88. Kee D., Zalcberg J.R. Current and emerging strategies for the management ofimatinib-refractory advanced gastrointestinal stromal tumors. Ther Adv Med Oncol 2012, 4(5):255-270.