Combined treatment with dabrafenib and trametinib with immune-stimulating antibodies for BRAF mutant melanoma

OncoImmunology

Volumn 5, Issue 7, 2016, Pages

  Homet Moreno, Blanca ^a   Mok, Stephen ^b   Comin Anduix, Begonya ^a,b   Hu Lieskovan, Siwen ^a   Ribas, Antoni ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

checkpoint blockade; immunotherapy; melanoma; PD 1; targeted therapy

Indexed keywords

ANTIBODY; B RAF KINASE; CD134 ANTIBODY; CD137 ANTIBODY; DABRAFENIB; MUTANT PROTEIN; PD 1 ANTIBODY; PD L1 ANTIBODY; TRAMETINIB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOSTIMULATION; METASTATIC MELANOMA; MOUSE; NONHUMAN; TUMOR ASSOCIATED LEUKOCYTE; UPREGULATION;

EID: 84976439348     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1052212     Document Type: Article

References (54)

1. J.R.Brahmer, S.S.Tykodi, L.Q.Chow, W.J.Hwu, S.L.Topalian, P.Hwu, C.G.Drake, L.H.Camacho, J.Kauh, K.Odunsi et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; http://dx.doi.org/10.1056/NEJMoa1200694
2. O.Hamid, C.Robert, A.Daud, F.S.Hodi, W.J.Hwu, R.Kefford, J.D.Wolchok, P.Hersey, R.W.Joseph, J.S.Weber et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013; 369:134-44; PMID:23724846; http://dx.doi.org/10.1056/NEJMoa1305133
3. F.S.Hodi, S.J.O'Day, D.F.McDermott, R.W.Weber, J.A.Sosman, J.B.Haanen, R.Gonzalez, C.Robert, D.Schadendorf, J.C.Hassel et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
4. C.Robert, L.Thomas, I.Bondarenko, S.O'Day, J.Weber, C.Garbe, C.Lebbe, J.F.Baurain, A.Testori, J.J.Grob et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011; 364:2517-26; PMID:21639810; http://dx.doi.org/10.1056/NEJMoa1104621
5. S.L.Topalian, F.S.Hodi, J.R.Brahmer, S.N.Gettinger, D.C.Smith, D.F.McDermott, J.D.Powderly, R.D.Carvajal, J.A.Sosman, M.B.Atkins et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
6. B.B.Aggarwal, S.C.Gupta, J.H.Kim. Historical perspectives on tumor necrosis factor and its superfamily:25 years later, a golden journey. Blood 2012; 119:651-65; PMID:22053109; http://dx.doi.org/10.1182/blood-2011-04-325225
7. K.T.Flaherty, J.R.Infante, A.Daud, R.Gonzalez, R.F.Kefford, J.Sosman, O.Hamid, L.Schuchter, J.Cebon, N.Ibrahim et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012; 367:1694-703; PMID:23020132; http://dx.doi.org/10.1056/NEJMoa1210093
8. A.Boni, A.P.Cogdill, P.Dang, D.Udayakumar, C.N.Njauw, C.M.Sloss, C.R.Ferrone, K.T.Flaherty, D.P.Lawrence, D.E.Fisher et al. Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function. Cancer Res 2010; 70:5213-9; PMID:20551059; http://dx.doi.org/10.1158/0008-5472.CAN-10-0118
9. D.T.Frederick, A.Piris, A.P.Cogdill, Z.A.Cooper, C.Lezcano, C.R.Ferrone, D.Mitra, A.Boni, L.P.Newton, C.Liu 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; 19:1225-31; PMID:23307859; http://dx.doi.org/10.1158/1078-0432.CCR-12-1630
10. B.Sapkota, C.E.Hill, B.P.Pollack. Vemurafenib enhances MHC induction in BRAF homozygous melanoma cells. Oncoimmunology 2013; 2:e22890; PMID:23483066; http://dx.doi.org/10.4161/onci.22890
11. M.Donia, P.Fagone, F.Nicoletti, R.S.Andersen, E.Hogdall, P.T.Straten, M.H.Andersen, I.M.Svane. BRAF inhibition improves tumor recognition by the immune system:Potential implications for combinatorial therapies against melanoma involving adoptive T-cell transfer. Oncoimmunology 2012; 1:1476-83; PMID:23264894; http://dx.doi.org/10.4161/onci.21940
12. C.Liu, W.Peng, C.Xu, Y.Lou, M.Zhang, J.A.Wargo, J.Q.Chen, H.S.Li, S.S.Watowich, Y.Yang et al. BRAF inhibition increases tumor infiltration by T cells and enhances the antitumor activity of adoptive immunotherapy in mice. Clin Cancer Res 2013; 19:393-403; PMID:23204132; http://dx.doi.org/10.1158/1078-0432.CCR-12-1626
13. G.V.Long, J.S.Wilmott, L.E.Haydu, V.Tembe, R.Sharma, H.Rizos, J.F.Thompson, J.Howle, R.A.Scolyer, R.F.Kefford. Effects of BRAF inhibitors on human melanoma tissue before treatment, early during treatment, and on progression. Pigment Cell Melanoma Res 2013; 26:499-508; PMID:23557327; http://dx.doi.org/10.1111/pcmr.12098
14. J.S.Wilmott, G.V.Long, J.R.Howle, L.E.Haydu, R.N.Sharma, J.F.Thompson, R.F.Kefford, P.Hersey, R.A.Scolyer. Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma. Clin Cancer Res 2012; 18:1386-94; PMID:22156613; http://dx.doi.org/10.1158/1078-0432.CCR-11-2479
15. R.C.Koya, S.Mok, N.Otte, K.J.Blacketor, B.Comin-Anduix, P.C.Tumeh, A.Minasyan, N.A.Graham, T.G.Graeber, T.Chodon et al. BRAF inhibitor vemurafenib improves the antitumor activity of adoptive cell immunotherapy. Cancer Res 2012; 72:3928-37; PMID:22693252; http://dx.doi.org/10.1158/0008-5472.CAN-11-2837
16. J.Kim, A.C.Myers, L.Chen, D.M.Pardoll, Q.A.Truong-Tran, A.P.Lane, J.F.McDyer, L.Fortuno, R.P.Schleimer. Constitutive and inducible expression of b7 family of ligands by human airway epithelial cells. Am J Res Cell Mol Biol 2005; 33:280-9; PMID:15961727; http://dx.doi.org/10.1165/rcmb.2004-0129OC
17. S.K.Lee, S.H.Seo, B.S.Kim, C.D.Kim, J.H.Lee, J.S.Kang, P.J.Maeng, J.S.Lim. IFN-gamma regulates the expression of B7-H1 in dermal fibroblast cells. J Dermatol Sci 2005; 40:95-103; PMID:16085391; http://dx.doi.org/10.1016/j.jdermsci.2005.06.008
18. X.Jiang, J.Zhou, A.Giobbie-Hurder, J.Wargo, F.S.Hodi. 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 2013; 19:598-609; PMID:23095323; http://dx.doi.org/10.1158/1078-0432.CCR-12-2731
19. S.S.M.Hu-Lieskovan, B.Homet Moreno, J.Tsoi, L.Robert, L.Goedert, R.C.Koya, T.Graeber, B.Comin-Anduix, A.Ribas. Improved antitumor activity of immunotherapy combined with BRAF and MEK inhibitors in BRAFV600E mutant melanoma. Sci Transl Med 2015; 18:18;7(279):279ra41; PMID:25787767; http://dx.doi.org/10.1126/scitranslmed.aaa4691
20. I.Melero, A.M.Grimaldi, J.L.Perez-Gracia, P.A.Ascierto. Clinical development of immunostimulatory monoclonal antibodies and opportunities for combination. Clin Cancer Res 2013; 19:997-1008; PMID:23460531; http://dx.doi.org/10.1158/1078-0432.CCR-12-2214
21. I.Melero, S.Hervas-Stubbs, M.Glennie, D.M.Pardoll, L.Chen. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 2007; 7:95-106; PMID:17251916; http://dx.doi.org/10.1038/nrc2051
22. S.A.Ju, S.H.Cheon, S.M.Park, N.Q.Tam, Y.M.Kim, W.G.An, B.S.Kim. Eradication of established renal cell carcinoma by a combination of 5-fluorouracil and anti-4-1BB monoclonal antibody in mice. Int J Cancer 2008; 122:2784-90; PMID:18360825; http://dx.doi.org/10.1002/ijc.23457
23. Y.H.Kim, B.K.Choi, K.H.Kim, S.W.Kang, B.S.Kwon. Combination therapy with cisplatin and anti-4-1BB:synergistic anticancer effects and amelioration of cisplatin-induced nephrotoxicity. Cancer Res 2008; 68:7264-9; PMID:18794112; http://dx.doi.org/10.1158/0008-5472.CAN-08-1365
24. J.Kjaergaard, J.Tanaka, J.A.Kim, K.Rothchild, A.Weinberg, S.Shu. Therapeutic efficacy of OX-40 receptor antibody depends on tumor immunogenicity and anatomic site of tumor growth. Cancer Res 2000; 60:5514-21; PMID:11034096
25. I.Verbrugge, J.Hagekyriakou, L.L.Sharp, M.Galli, A.West, N.M.McLaughlin, H.Duret, H.Yagita, R.W.Johnstone, M.J.Smyth et al. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res 2012; 72:3163-74; PMID:22570253; http://dx.doi.org/10.1158/0008-5472.CAN-12-0210
26. A.D.Weinberg, M.M.Rivera, R.Prell, A.Morris, T.Ramstad, J.T.Vetto, W.J.Urba, G.Alvord, C.Bunce, J.Shields. Engagement of the OX-40 receptor in vivo enhances antitumor immunity. J Immunol 2000; 164:2160-9; http://dx.doi.org/10.4049/jimmunol.164.4.2160
27. M.Croft. Co-stimulatory members of the TNFR family:keys to effective T-cell immunity? Nat Rev Immunol 2003; 3:609-20; PMID:12974476; http://dx.doi.org/10.1038/nri1148
28. T.H.Watts. TNF/TNFR family members in costimulation of T cell responses. Annu Rev Immunol 2005; 23:23-68; PMID:15771565; http://dx.doi.org/10.1146/annurev.immunol.23.021704.115839
29. J.Foell, S.Strahotin, S.P.O'Neil, M.M.McCausland, C.Suwyn, M.Haber, P.N.Chander, A.S.Bapat, X.J.Yan, N.Chiorazzi et al. CD137 costimulatory T cell receptor engagement reverses acute disease in lupus-prone NZB x NZW F1 mice. J Clin Investig 2003; 111:1505-18; PMID:12750400; http://dx.doi.org/10.1172/JCI200317662
30. S.K.Seo, J.H.Choi, Y.H.Kim, W.J.Kang, H.Y.Park, J.H.Suh, B.K.Choi, D.S.Vinay, B.S.Kwon. 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nat Med 2004; 10:1088-94; PMID:15448685; http://dx.doi.org/10.1038/nm1107
31. Y.Sun, H.M.Chen, S.K.Subudhi, J.Chen, R.Koka, L.Chen, Y.X.Fu. Costimulatory molecule-targeted antibody therapy of a spontaneous autoimmune disease. Nat Med 2002; 8:1405-13; PMID:12426559; http://dx.doi.org/10.1038/nm1202-796
32. S.Mallett, S.Fossum, A.N.Barclay. Characterization of the MRC OX40 antigen of activated CD4 positive T lymphocytes–a molecule related to nerve growth factor receptor. EMBO J 1990; 9:1063-8; PMID:2157591
33. I.Gramaglia, A.Jember, S.D.Pippig, A.D.Weinberg, N.Killeen, M.Croft. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J Immunol 2000; 165:3043-50; http://dx.doi.org/10.4049/jimmunol.165.6.3043
34. I.Gramaglia, A.D.Weinberg, M.Lemon, M.Croft. Ox-40 ligand:a potent costimulatory molecule for sustaining primary CD4 T cell responses. J Immunol 1998; 161:6510-7
35. I.Melero, W.W.Shuford, S.A.Newby, A.Aruffo, J.A.Ledbetter, K.E.Hellstrom, R.S.Mittler, L.Chen. Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med 1997; 3:682-5; PMID:9176498; http://dx.doi.org/10.1038/nm0697-682
36. K.Takeda, Y.Kojima, T.Uno, Y.Hayakawa, M.W.Teng, H.Yoshizawa, H.Yagita, F.Gejyo, K.Okumura, M.J.Smyth. Combination therapy of established tumors by antibodies targeting immune activating and suppressing molecules. J Immunol 2010; 184:5493-501; http://dx.doi.org/10.4049/jimmunol.0903033
37. T.Uno, K.Takeda, Y.Kojima, H.Yoshizawa, H.Akiba, R.S.Mittler, F.Gejyo, K.Okumura, H.Yagita, M.J.Smyth. Eradication of established tumors in mice by a combination antibody-based therapy. Nat Med 2006; 12:693-8; PMID:16680149; http://dx.doi.org/10.1038/nm1405
38. D.A.Knight, S.F.Ngiow, M.Li, T.Parmenter, S.Mok, A.Cass, N.M.Haynes, K.Kinross, H.Yagita, R.C.Koya et al. Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J Clin Investig 2013; 123:1371-81; PMID:23454771; http://dx.doi.org/10.1172/JCI66236
39. S.Hu-Lieskovan, L.Robert, B.Homet Moreno, A.Ribas. Combining targeted therapy with immunotherapy in BRAF-mutant melanoma:promise and challenges. J Clin Oncol 2014; 32:2248-54; PMID:24958825; http://dx.doi.org/10.1200/JCO.2013.52.1377
40. A.Palazon, I.Martinez-Forero, A.Teijeira, A.Morales-Kastresana, C.Alfaro, M.F.Sanmamed, J.L.Perez-Gracia, I.Penuelas, S.Hervas-Stubbs, A.Rouzaut et al. The HIF-1alpha hypoxia response in tumor-infiltrating T lymphocytes induces functional CD137 (4-1BB) for immunotherapy. Cancer Discov 2012; 2:608-23; PMID:22719018; http://dx.doi.org/10.1158/2159-8290.CD-11-0314
41. F.Hirano, K.Kaneko, H.Tamura, H.Dong, S.Wang, M.Ichikawa, C.Rietz, D.B.Flies, J.S.Lau, G.Zhu et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res 2005; 65:1089-96; PMID:15705911
42. A.Hooijkaas, J.Gadiot, M.Morrow, R.Stewart, T.Schumacher, C.U.Blank. Selective BRAF inhibition decreases tumor-resident lymphocyte frequencies in a mouse model of human melanoma. Oncoimmunology 2012; 1:609-17; PMID:22934253; http://dx.doi.org/10.4161/onci.20226
43. M.Croft. Control of immunity by the TNFR-related molecule OX40 (CD134). Annu Rev Immunol 2010; 28:57-78; PMID:20307208; http://dx.doi.org/10.1146/annurev-immunol-030409-101243
44. W.L.Redmond, T.Triplett, K.Floyd, A.D.Weinberg. Dual anti-OX40/IL-2 therapy augments tumor immunotherapy via IL-2R-mediated regulation of OX40 expression. PLoS One 2012; 7:e34467; PMID:22496812; http://dx.doi.org/10.1371/journal.pone.0034467
45. P.C.Tumeh, C.L.Harview, J.H.Yearley, I.P.Shintaku, E.J.Taylor, L.Robert, B.Chmielowski, M.Spasic, G.Henry, V.Ciobanu et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515:568-71; PMID:25428505; http://dx.doi.org/10.1038/nature13954
46. Z.A.Cooper, D.T.Frederick, Z.Ahmed, J.A.Wargo. Combining checkpoint inhibitors and BRAF-targeted agents against metastatic melanoma. Oncoimmunology 2013; 2:e24320; PMID:23762807; http://dx.doi.org/10.4161/onci.24320
47. T.Bald, J.Landsberg, D.Lopez-Ramos, M.Renn, N.Glodde, P.Jansen, E.Gaffal, J.Steitz, R.Tolba, U.Kalinke et al. Immune cell-poor melanomas benefit from PD-1 blockade after targeted type I IFN activation. Cancer Discov 2014; 4:674-87; PMID:24589924; http://dx.doi.org/10.1158/2159-8290.CD-13-0458
48. J.M.Taube, A.Klein, J.R.Brahmer, H.Xu, X.Pan, J.H.Kim, L.Chen, D.M.Pardoll, S.L.Topalian, R.A.Anders. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014; 20:5064-74; PMID:24714771; http://dx.doi.org/10.1158/1078-0432.CCR-13-3271
49. Z.A.Cooper, V.R.Juneja, P.T.Sage, D.T.Frederick, A.Piris, D.Mitra, J.A.Lo, F.S.Hodi, G.J.Freeman, M.W.Bosenberg et al. Response to BRAF inhibition in melanoma is enhanced when combined with immune checkpoint blockade. Cancer Immunol Res 2014; 2:643-54; PMID:24903021; http://dx.doi.org/10.1158/2326-6066.CIR-13-0215
50. P.C.Ho, S.M.Kaech. BRAF-targeted therapy alters the functions of intratumoral CD4 T cells to inhibit melanoma progression. Oncoimmunology 2014; 3:e29126; PMID:25083331; http://dx.doi.org/10.4161/onci.29126
51. I.Marigo, L.Dolcetti, P.Serafini, P.Zanovello, V.Bronte. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 2008; 222:162-79; PMID:18364001; http://dx.doi.org/10.1111/j.1600-065X.2008.00602.x
52. D.I.Gabrilovich, S.Nagaraj. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9:162-74; PMID:19197294; http://dx.doi.org/10.1038/nri2506
53. K.Movahedi, M.Guilliams, J.Van den Bossche, R.Van den Bergh, C.Gysemans, A.Beschin, P.De Baetselier, J.A.Van Ginderachter. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111:4233-44; PMID:18272812; http://dx.doi.org/10.1182/blood-2007-07-099226
54. E.Peranzoni, S.Zilio, I.Marigo, L.Dolcetti, P.Zanovello, S.Mandruzzato, V.Bronte. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 2010; 22:238-44; PMID:20171075; http://dx.doi.org/10.1016/j.coi.2010.01.021