The immune-related role of BRAF in melanoma

Molecular Oncology

Volumn 9, Issue 1, 2015, Pages 93-104

  Tomei, Sara ^a,b,c   Bedognetti, Davide ^a,c   De Giorgi, Valeria ^a   Sommariva, Michele ^a,d   Civini, Sara ^a   Reinboth, Jennifer ^a,e,f   Al Hashmi, Muna ^c   Ascierto, Maria Libera ^a,g   Liu, Qiuzhen ^a   Ayotte, Ben D ^h   Worschech, Andrea ^b   Uccellini, Lorenzo ^a,i   Ascierto, Paolo A ^j   Stroncek, David ^a   Palmieri, Giuseppe ^k   Chouchane, Lotfi ^b   Wang, Ena ^a,c   Marincola, Francesco M ^a,c  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (Qatar)

^c SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

^d UNIVERSITY OF MILAN   (Italy)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f GENELUX CORPORATION   (United States)

^g UNIVERSITY OF GENOA   (Italy)

^h NORTHERN MICHIGAN UNIVERSITY   (United States)

ⁱ UNIVERSITY OF MILAN   (Italy)

^j NATIONAL CANCER INSTITUTE   (Italy)

^k CNR   (Italy)

more..

Author keywords

BRAF; Immune phenotype; Melanoma; NRAS

Indexed keywords

B RAF KINASE; MITOGEN ACTIVATED PROTEIN KINASE; RAS PROTEIN; BRAF PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; NRAS PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; MAJOR CLINICAL STUDY; MELANOMA; MELANOMA CELL; METASTASIS; POLYMERASE CHAIN REACTION; TUMOR GENE; TUMOR IMMUNITY; WILD TYPE; DNA MICROARRAY; FEMALE; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MUTATION; PATHOLOGY; TH1 CELL; TUMOR CELL LINE;

CELL LINE, TUMOR; FEMALE; GTP PHOSPHOHYDROLASES; HUMANS; MALE; MELANOMA; MEMBRANE PROTEINS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS B-RAF; TH1 CELLS;

EID: 84920379679     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.07.014     Document Type: Article

References (56)

1. Ascierto P.A., Kirkwood J.M., Grob J.J., Simeone E., Grimaldi A.M., Maio M., Palmieri G., Testori A., Marincola F.M., Mozzillo N. The role of BRAF V600 mutation in melanoma. J.Transl. Med. 2012, 10:85.
2. Bedognetti D., Balwit J.M., Wang E., Disis M.L., Britten C.M., Delogu L.G., Tomei S., Fox B.A., Gajewski T.F., Marincola F.M., Butterfield L.H. SITC/iSBTc cancer immunotherapy biomarkers resource document: online resources and useful tools - a compass in the land of biomarker discovery. J.Transl. Med. 2011, 9:155.
3. Bedognetti D., Spivey T.L., Zhao Y., Uccellini L., Tomei S., Dudley M.E., Ascierto M.L., De Giorgi V., Liu Q., Delogu L.G., et al. CXCR3/CCR5 pathways in metastatic melanoma patients treated with adoptive therapy and interleukin-2. Br. J. Cancer 2013, 109:2412-2423.
4. Bittner M., Meltzer P., Chen Y., Jiang Y., Seftor E., Hendrix M., Radmacher M., Simon R., Yakhini Z., Ben-Dor A., et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000, 406:536-540.
5. Bloethner S., Chen B., Hemminki K., Muller-Berghaus J., Ugurel S., Schadendorf D., Kumar R. Effect of common B-RAF and N-RAS mutations on global gene expression in melanoma cell lines. Carcinogenesis 2005, 26:1224-1232.
6. Brose M.S., Volpe P., Feldman M., Kumar M., Rishi I., Gerrero R., Einhorn E., Herlyn M., Minna J., Nicholson A., et al. BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res. 2002, 62:6997-7000.
7. Castelli C., Sensi M., Lupetti R., Mortarini R., Panceri P., Anichini A., Parmiani G. Expression of interleukin 1 alpha, interleukin 6, and tumor necrosis factor alpha genes in human melanoma clones is associated with that of mutated N-RAS oncogene. Cancer Res. 1994, 54:4785-4790.
8. Cohen C., Zavala-Pompa A., Sequeira J.H., Shoji M., Sexton D.G., Cotsonis G., Cerimele F., Govindarajan B., Macaron N., Arbiser J.L. Mitogen-actived protein kinase activation is an early event in melanoma progression. Clin. Cancer Res. 2002, 8:3728-3733.
9. Colombino M., Capone M., Lissia A., Cossu A., Rubino C., De Giorgi V., Massi D., Fonsatti E., Staibano S., Nappi O., et al. BRAF/NRAS mutation frequencies among primary tumors and metastases in patients with melanoma. J.Clin. Oncol.: Official J. Am. Soc. Clin. Oncol. 2012, 30:2522-2529.
10. 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., et al. Distinct sets of genetic alterations in melanoma. N.Engl. J. Med. 2005, 353:2135-2147.
11. Davies H., Bignell G.R., Cox C., Stephens P., Edkins S., Clegg S., Teague J., Woffendin H., Garnett M.J., Bottomley W., et al. Mutations of the BRAF gene in human cancer. Nature 2002, 417:949-954.
12. Devitt B., Liu W., Salemi R., Wolfe R., Kelly J., Tzen C.Y., Dobrovic A., McArthur G. Clinical outcome and pathological features associated with NRAS mutation in cutaneous melanoma. Pigment Cell Melanoma Res. 2011, 24:666-672.
13. Dhomen N., Marais R. BRAF signaling and targeted therapies in melanoma. Hematol. Oncol. Clin. N. Am. 2009, 23:529-545.
14. Edlundh-Rose E., Egyhazi S., Omholt K., Mansson-Brahme E., Platz A., Hansson J., Lundeberg J. NRAS and BRAF mutations in melanoma tumours in relation to clinical characteristics: a study based on mutation screening by pyrosequencing. Melanoma Res. 2006, 16:471-478.
15. Fedorenko I.V., Gibney G.T., Smalley K.S. NRAS mutant melanoma: biological behavior and future strategies for therapeutic management. Oncogene 2012, 32:3009-3018.
16. Frankel A.E., Koo H.M., Leppla S.H., Duesbery N.S., Vande Woude G.F. Novel protein targeted therapy of metastatic melanoma. Curr. Pharm. Des. 2003, 9:2060-2066.
17. Frederick D.T., Piris A., Cogdill A.P., Cooper Z.A., Lezcano C., Ferrone C.R., Mitra D., Boni A., Newton L.P., Liu C., et al. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res. 2013, 19:1225-1231.
18. Galon J., Angell H.K., Bedognetti D., Marincola F.M. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013, 39:11-26.
19. Gray-Schopfer V., Wellbrock C., Marais R. Melanoma biology and new targeted therapy. Nature 2007, 445:851-857.
20. Gray-Schopfer V.C., da Rocha Dias S., Marais R. The role of B-RAF in melanoma. Cancer Metastasis Rev. 2005, 24:165-183.
21. Hocker T.L., Singh M.K., Tsao H. Melanoma genetics and therapeutic approaches in the 21st century: moving from the benchside to the bedside. J.Invest Dermatol. 2008, 128:2575-2595.
22. Ibrahim N., Haluska F.G. Molecular pathogenesis of cutaneous melanocytic neoplasms. Annu. Rev. Pathol. 2009, 4:551-579.
23. Jakob J.A., Bassett R.L., Ng C.S., Curry J.L., Joseph R.W., Alvarado G.C., Rohlfs M.L., Richard J., Gershenwald J.E., Kim K.B., et al. NRAS mutation status is an independent prognostic factor in metastatic melanoma. Cancer 2012, 118:4014-4023.
24. Jin P., Civini S., Zhao Y., De Giorgi V., Ren J., Sabatino M., Jin J., Wang H., Bedognetti D., Marincola F., Stroncek D. Direct T cell-tumour interaction triggers TH1 phenotype activation through the modification of the mesenchymal stromal cells transcriptional programme. Br. J. Cancer 2014, 110:2955-2964.
25. Johansson P., Pavey S., Hayward N. Confirmation of a BRAF mutation-associated gene expression signature in melanoma. Pigment Cell Res. 2007, 20:216-221.
26. Jonsson G., Busch C., Knappskog S., Geisler J., Miletic H., Ringner M., Lillehaug J.R., Borg A., Lonning P.E. Gene expression profiling-based identification of molecular subtypes in stage IV melanomas with different clinical outcome. Clin. Cancer Res. 2010, 16:3356-3367.
27. Joseph R.W., Sullivan R.J., Harrell R., Stemke-Hale K., Panka D., Manoukian G., Percy A., Bassett R.L., Ng C.S., Radvanyi L., et al. Correlation of NRAS mutations with clinical response to high-dose IL-2 in patients with advanced melanoma. J.Immunother. 2012, 35:66-72.
28. Kannengiesser C., Spatz A., Michiels S., Eychene A., Dessen P., Lazar V., Winnepenninckx V., Lesueur F., Druillennec S., Robert C., et al. Gene expression signature associated with BRAF mutations in human primary cutaneous melanomas. Mol. Oncol. 2008, 1:425-430.
29. Karasarides M., Chiloeches A., Hayward R., Niculescu-Duvaz D., Scanlon I., Friedlos F., Ogilvie L., Hedley D., Martin J., Marshall C.J., et al. B-RAF is a therapeutic target in melanoma. Oncogene 2004, 23:6292-6298.
30. Khalili J.S., Liu S., Rodriguez-Cruz T.G., Whittington M., Wardell S., Liu C., Zhang M., Cooper Z.A., Frederick D.T., Li Y., et al. Oncogenic BRAF(V600E) promotes stromal cell-mediated immunosuppression via induction of interleukin-1 in melanoma. Clin. Cancer Res. 2012, 18:5329-5340.
31. Kimura E.T., Nikiforova M.N., Zhu Z., Knauf J.A., Nikiforov Y.E., Fagin J.A. High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res. 2003, 63:1454-1457.
32. Kumar R., Angelini S., Snellman E., Hemminki K. BRAF mutations are common somatic events in melanocytic nevi. J.Invest. Dermatol. 2004, 122:342-348.
33. Linard B., Bezieau S., Benlalam H., Labarriere N., Guilloux Y., Diez E., Jotereau F. A ras-mutated peptide targeted by CTL infiltrating a human melanoma lesion. J.Immunol. 2002, 168:4802-4808.
34. Maurer G., Tarkowski B., Baccarini M. Raf kinases in cancer-roles and therapeutic opportunities. Oncogene 2011, 30:3477-3488.
35. Murtas D., Maric D., De Giorgi V., Reinboth J., Worschech A., Fetsch P., Filie A., Ascierto M.L., Bedognetti D., Liu Q., et al. IRF-1 responsiveness to IFN-gamma predicts different cancer immune phenotypes. Br. J. Cancer 2013, 109:76-82.
36. Nikolaou V.A., Stratigos A.J., Flaherty K.T., Tsao H. Melanoma: new insights and new therapies. J.Invest Dermatol. 2012, 132:854-863.
37. Packer L.M., East P., Reis-Filho J.S., Marais R. Identification of direct transcriptional targets of (V600E)BRAF/MEK signalling in melanoma. Pigment Cell Melanoma Res. 2009, 22:785-798.
38. Palmieri G., Capone M., Ascierto M.L., Gentilcore G., Stroncek D.F., Casula M., Sini M.C., Palla M., Mozzillo N., Ascierto P.A. Main roads to melanoma. J.Transl Med. 2009, 7:86.
39. Pavey S., Johansson P., Packer L., Taylor J., Stark M., Pollock P.M., Walker G.J., Boyle G.M., Harper U., Cozzi S.J., et al. Microarray expression profiling in melanoma reveals a BRAF mutation signature. Oncogene 2004, 23:4060-4067.
40. Pollock P.M., Harper U.L., Hansen K.S., Yudt L.M., Stark M., Robbins C.M., Moses T.Y., Hostetter G., Wagner U., Kakareka J., et al. High frequency of BRAF mutations in nevi. Nat. Genet. 2003, 33:19-20.
41. Satyamoorthy K., Li G., Gerrero M.R., Brose M.S., Volpe P., Weber B.L., Van Belle P., Elder D.E., Herlyn M. Constitutive mitogen-activated protein kinase activation in melanoma is mediated by both BRAF mutations and autocrine growth factor stimulation. Cancer Res. 2003, 63:756-759.
42. Schramm S.J., Campain A.E., Scolyer R.A., Yang Y.H., Mann G.J. Review and cross-validation of gene expression signatures and melanoma prognosis. J.Invest Dermatol. 2012, 132:274-283.
43. Sensi M., Nicolini G., Petti C., Bersani I., Lozupone F., Molla A., Vegetti C., Nonaka D., Mortarini R., Parmiani G., et al. Mutually exclusive NRASQ61R and BRAFV600E mutations at the single-cell level in the same human melanoma. Oncogene 2006, 25:3357-3364.
44. Smalley K.S. A pivotal role for ERK in the oncogenic behaviour of malignant melanoma?. Int. J. Cancer 2003, 104:527-532.
45. Spivey T.L., De Giorgi V., Zhao Y., Bedognetti D., Pos Z., Lui Q., Tomei S., Ascierto M.L., Uccellini L., Reinboth J., et al. The stable traits of melanoma genetics: an alternate approach to target discovery. BMC Genomics 2012, 13:156.
46. Sumimoto H., Imabayashi F., Iwata T., Kawakami Y. The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J.Exp. Med. 2006, 203:1651-1656.
47. Tomei S., Wang E., Delogu L.G., Marincola F.M., Bedognetti D. Non-BRAF-targeted therapy, immunotherapy, and combination therapy for melanoma. Expert Opin. Biol. Ther. 2014, 14:663-686.
48. Tompers Frederick D., Piris A., Cogdill A.P., Cooper Z.A., Lezcano C., Ferrone C.R., Mitra D., Boni A., Newton L.P., Liu C., et al. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res. 2013, 19:1225-1231.
49. Ulloa-Montoya F., Louahed J., Dizier B., Gruselle O., Spiessens B., Lehmann F.F., Suciu S., Kruit W.H., Eggermont A.M., Vansteenkiste J., Brichard V.G. Predictive gene signature in MAGE-A3 antigen-specific Cancer immunotherapy. J.Clin. Oncol.: Official J. Am. Soc. Clin. Oncol. 2013, 31:2388-2395.
50. van Elsas A., Zerp S.F., van der Flier S., Kruse K.M., Aarnoudse C., Hayward N.K., Ruiter D.J., Schrier P.I. Relevance of ultraviolet-induced N-ras oncogene point mutations in development of primary human cutaneous melanoma. Am. J. Pathol. 1996, 149:883-893.
51. Viros A., Fridlyand J., Bauer J., Lasithiotakis K., Garbe C., Pinkel D., Bastian B.C. Improving melanoma classification by integrating genetic and morphologic features. PLoS Med. 2008, 5:e120.
52. Wang E., Bedognetti D., Marincola F.M. Prediction of response to anticancer immunotherapy using gene signatures. J.Clin. Oncol.: Official J. Am. Soc. Clin. Oncol. 2013, 31:2369-2371.
53. Wang E., Bedognetti D., Tomei S., Marincola F.M. Common pathways to tumor rejection. Ann. N. Y. Acad. Sci. 2013, 1284:75-79.
54. Wang E., Uccellini L., Marincola F.M. A genetic inference on cancer immune responsiveness. Oncoimmunology 2012, 1:520-525.
55. Wilmott J.S., Long G.V., Howle J.R., Haydu L.E., Sharma R.N., Thompson J.F., Kefford R.F., Hersey P., Scolyer R.A. Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma. Clin. Cancer Res. 2012, 18:1386-1394.
56. Zambon A., Niculescu-Duvaz I., Niculescu-Duvaz D., Marais R., Springer C.J. Small molecule inhibitors of BRAF in clinical trials. Bioorg. Med. Chem. Lett. 2012, 22:789-792.