Combining targeted therapy with immunotherapy in BRAF-mutant melanoma: Promise and challenges

Journal of Clinical Oncology

Volumn 32, Issue 21, 2014, Pages 2248-2254

  Hu Lieskovan, Siwen ^a   Robert, Lidia ^a   Moreno, Blanca Homet ^a,b   Ribas, Antoni ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; B RAF KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR;

ANTIGEN EXPRESSION; ARTICLE; CANCER IMMUNOTHERAPY; CANCER TARGETED THERAPY; CANCER THERAPY; ENZYME INHIBITION; HUMAN; LYMPHOCYTE FUNCTION; LYMPHOCYTE HOMING; MELANOMA; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; HUMANS; IMMUNOTHERAPY; MELANOMA; MOLECULAR TARGETED THERAPY; MUTATION; PROGNOSIS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF;

EID: 84905825810     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2013.52.1377     Document Type: Article

References (51)

1. Hodi FS, O'Day SJ, McDermott DF, et al: Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363:711-723, 2010
2. Robert C, Thomas L, Bondarenko I, et al: Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364: 2517-2526, 2011
3. Topalian SL, Hodi FS, Brahmer JR, et al: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366:2443-2454, 2012
4. Brahmer JR, Tykodi SS, Chow LQ, et al: Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366:2455-2465, 2012
5. Gajewski TF: Failure at the effector phase: Immune barriers at the level of the melanoma tumor microenvironment. Clin Cancer Res 13:5256-5261, 2007
6. Kerkar SP, Restifo NP: Cellular constituents of immune escape within the tumor microenvironment. Cancer Res 72:3125-3130, 2012
7. Gray-Schopfer V, Wellbrock C, Marais R: Melanoma biology and new targeted therapy. Nature 445:851-857, 2007
8. Chapman PB, Hauschild A, Robert C, et al: Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516, 2011
9. Hauschild A, Grob JJ, Demidov LV, et al: Dabrafenib in BRAF-mutated metastatic melanoma: A multicentre, open-label, phase 3 randomised controlled trial. Lancet 380:358-365, 2012
10. Flaherty KT, Robert C, Hersey P, et al: Improved survival with MEK inhibition in BRAFmutated melanoma. N Engl J Med 367:107-114, 2012
11. Su F, Viros A, Milagre C, et al: RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med 366:207-215, 2012
12. Oberholzer PA, Kee D, Dziunycz P, et al: RAS mutations are associated with the development of cutaneous squamous cell tumors in patients treated with RAF inhibitors. J Clin Oncol 30:316-321, 2012
13. Trunzer K, Pavlick AC, Schuchter L, et al: Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. J Clin Oncol 31:1767-1774, 2013
14. Shi H, Hugo W, Kong X, et al: Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov 4:80-93, 2014
15. Van Allen EM, Wagle N, Sucker A, et al: The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov 4:94- 109, 2014
16. Flaherty KT, Infante JR, Daud A, et al: Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 367:1694- 1703, 2012
17. Cipponi A, Wieers G, van Baren N, et al: Tumor-infiltrating lymphocytes: Apparently good for melanoma patients-But why? Cancer Immunol Immunother 60:1153-1160, 2011
18. Rosenberg SA, Yang JC, Topalian SL, et al: Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using highdose bolus interleukin 2. JAMA 271:907-913, 1994
19. Atkins MB, Lotze MT, Dutcher JP, et al: 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, 1999 (Pubitemid 29318842)
20. Rosenberg SA, Yang JC, Sherry RM, et al: Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17:4550-4557, 2011
21. Hunder NN, Wallen H, Cao J, et al: Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 358:2698-2703, 2008 (Pubitemid 351860862)
22. Hamid O, Robert C, Daud A, et al: Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 369:134-144, 2013
23. Wolchok JD, Kluger H, Callahan MK, et al: Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369:122-133, 2013
24. Ku GY, Yuan J, Page DB, et al: Singleinstitution experience with ipilimumab in advanced melanoma patients in the compassionate use setting: Lymphocyte count after 2 doses correlates with survival. Cancer 116:1767-1775, 2010
25. Boni A, Cogdill AP, Dang P, et al: Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function. Cancer Res 70:5213-5219, 2010
26. Sapkota B, Hill CE, Pollack BP: Vemurafenib enhances MHC induction in BRAFV600E homozygous melanoma cells. Oncoimmunology 2:e22890, 2013
27. Frederick DT, Piris A, Cogdill AP, 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 19:1225-1231, 2013
28. Kono M, Dunn IS, Durda PJ, et al: Role of the mitogen-activated protein kinase signaling pathway in the regulation of human melanocytic antigen expression. Mol Cancer Res 4:779-792, 2006 (Pubitemid 44683317)
29. Sumimoto H, Imabayashi F, Iwata T, et al: The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J Exp Med 203:1651-1656, 2006 (Pubitemid 44036269)
30. Donia M, Fagone P, Nicoletti F, et al: BRAF inhibition improves tumor recognition by the immune system: Potential implications for combinatorial therapies against melanoma involving adoptive T-cell transfer. Oncoimmunology 1:1476-1483, 2012
31. Long GV, Wilmott JS, Haydu LE, et al: Effects of BRAF inhibitors on human melanoma tissue before treatment, early during treatment, and on progression. Pigment Cell Melanoma Res 26:499-508, 2013
32. Wilmott JS, Long GV, Howle JR, et al: Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma. Clin Cancer Res 18:1386-1394, 2012
33. Cooper ZA, Frederick DT, Ahmed Z, et al: Combining checkpoint inhibitors and BRAF-targeted agents against metastatic melanoma. Oncoimmunology 2:e24320, 2013
34. Khalili JS, Liu S, Rodríguez-Cruz TG, et al: Oncogenic BRAF(V600E) promotes stromal cellmediated immunosuppression via induction of interleukin-1 in melanoma. Clin Cancer Res 18:5329-5340, 2012
35. Koya RC, Mok S, Otte N, et al: BRAF inhibitor vemurafenib improves the antitumor activity of adoptive cell immunotherapy. Cancer Res 72:3928-3937, 2012
36. Comin-Anduix B, Chodon T, Sazegar H, et al: The oncogenic BRAF kinase inhibitor PLX4032/ RG7204 does not affect the viability or function of human lymphocytes across a wide range of concentrations. Clin Cancer Res 16:6040-6048, 2010
37. Knight DA, Ngiow SF, Li M, et al: Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J Clin Invest 123:1371-1381, 2013
38. Liu C, Peng W, Xu C, et al: BRAF inhibition increases tumor infiltration by T cells and enhances the antitumor activity of adoptive immunotherapy in mice. Clin Cancer Res 19:393-403, 2013
39. Landsberg J, Kohlmeyer J, Renn M, et al: Melanomas resist T-cell therapy through inflammationinduced reversible dedifferentiation. Nature 490:412-416, 2012
40. Gray-Schopfer VC, Karasarides M, Hayward R, et al: Tumor necrosis factor-alpha blocks apoptosis in melanoma cells when BRAF signaling is inhibited. Cancer Res 67:122-129, 2007 (Pubitemid 46142767)
41. Jiang X, Zhou J, Giobbie-Hurder A, et al: The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin Cancer Res 19:598-609, 2013
42. Haq R, Shoag J, Andreu-Perez P, et al: Oncogenic BRAF regulates oxidative metabolism via PGC1α and MITF. Cancer Cell 23:302-315, 2013
43. Hooijkaas A, Gadiot J, Morrow M, et al: Selective BRAF inhibition decreases tumor-resident lymphocyte frequencies in a mouse model of human melanoma. Oncoimmunology 1:609-617, 2012
44. Hong D, Vence L, Falchook G, et al: BRAF (V600) inhibitor GSK218436 targeted inhibition of mutant BRAF in cancer patients does not impair overall immune competency. Clin Cancer Res 18:2326-2335, 2012
45. Fife BT, Pauken KE: The role of the PD-1 pathway in autoimmunity and peripheral tolerance. Ann N Y Acad Sci 1217:45-59, 2011
46. Pardoll DM: The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12:252-264, 2012
47. Yamamoto R, Nishikori M, Tashima M, et al: B7-H1 expression is regulated by MEK/ERK signaling pathway in anaplastic large cell lymphoma and Hodgkin lymphoma. Cancer Sci 100:2093-2100, 2009
48. Berthon C, Driss V, Liu J, et al: In acute myeloid leukemia, B7-H1 (PD-L1) protection of blasts from cytotoxic T cells is induced by TLR ligands and interferon-gamma and can be reversed using MEK inhibitors. Cancer Immunol Immunother 59:1839-1849, 2010
49. Harding JJ, Pulitzer M, Chapman PB: Vemurafenib sensitivity skin reaction after ipilimumab. N Engl J Med 366:866-868, 2012
50. Ribas A, Hodi FS, Callahan M, et al: Hepatotoxicity with combination of vemurafenib and ipilimumab. N Engl J Med 368:1365-1366, 2013
51. Das Thakur M, Salangsang F, Landman AS, et al: Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature 494:251-255, 2013