Metastatic melanoma and immunotherapy

Clinical Immunology

Volumn 172, Issue , 2016, Pages 105-110

  Herzberg, Benjamin ^a   Fisher, David E ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

Checkpoint; Immunotherapy; Melanoma; T cell; Vitiligo

Indexed keywords

ANTINEOPLASTIC AGENT; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOMODULATING AGENT; PROGRAMMED DEATH 1 RECEPTOR;

ARTICLE; CANCER IMMUNOTHERAPY; CELLULAR IMMUNITY; DRUG RESPONSE; HUMAN; IMMUNE RESPONSE; METASTATIC MELANOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); TUMOR ESCAPE; TUMOR IMMUNITY; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; MELANOMA; T LYMPHOCYTE;

ANIMALS; HUMANS; IMMUNOTHERAPY; MELANOMA; T-LYMPHOCYTES;

EID: 84993953600     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.07.006     Document Type: Article

References (89)

1. [1] American Cancer Society, Cancer Facts & Figures 2016. 2016, American Cancer Society, Atlanta.
2. [2] Pardoll, D.M., The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12:4 (2012), 252–264.
3. [3] Drake, C.G., Lipson, E.J., Brahmer, J.R., Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer. Nat. Rev. Clin. Oncol. 11:1 (2014), 24–37.
4. [4] de Visser, K.E., Eichten, A., Coussens, L.M., Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 6:1 (2006), 24–37.
5. [5] Natali, P.G., et al. Selective changes in expression of HLA class I polymorphic determinants in human solid tumors. Proc. Natl. Acad. Sci. U. S. A. 86:17 (1989), 6719–6723.
6. [6] Blanchet, O., et al. Altered binding of regulatory factors to HLA class I enhancer sequence in human tumor cell lines lacking class I antigen expression. Proc. Natl. Acad. Sci. U. S. A. 89:8 (1992), 3488–3492.
7. [7] Urban, J.L., Kripke, M.L., Schreiber, H., Stepwise immunologic selection of antigenic variants during tumor growth. J. Immunol. 137:9 (1986), 3036–3041.
8. [8] Kusmartsev, S., Gabrilovich, D.I., Effect of tumor-derived cytokines and growth factors on differentiation and immune suppressive features of myeloid cells in cancer. Cancer Metastasis Rev. 25:3 (2006), 323–331.
9. [9] Munn, D.H., et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297:5588 (2002), 1867–1870.
10. [10] Beyer, M., Schultze, J.L., Regulatory T cells in cancer. Blood 108:3 (2006), 804–811.
11. [11] Coley, W., The treatment of malignant tumors by repeated inoculations of erysipelas with a report of ten original cases. Am. J. Med. Sci. 105 (1893), 487–511.
12. [12] Cole, W.H., Everson, T.C., Spontaneous regression of cancer: preliminary report. Ann. Surg. 144:3 (1956), 366–383.
13. [13] Greene, M.H., Young, T.I., Clark, W.H. Jr., Malignant melanoma in renal-transplant recipients. Lancet 1:8231 (1981), 1196–1199.
14. [14] Atkins, M.B., 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. 17:7 (1999), 2105–2116.
15. [15] Fyfe, G., et al. Results of treatment of 255 patients with metastatic renal cell carcinoma who received high-dose recombinant interleukin-2 therapy. J. Clin. Oncol. 13:3 (1995), 688–696.
16. [16] Fisher, R.I., Rosenberg, S.A., Fyfe, G., Long-term survival update for high-dose recombinant interleukin-2 in patients with renal cell carcinoma. Cancer J. Sci. Am. 6:Suppl 1 (2000), S55–S57.
17. [17] Atkins, M.B., et al. High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update. Cancer J. Sci. Am. 6:Suppl 1 (2000), S11–S14.
18. [18] Jansen, R.L., et al. Interleukin-2 and interferon-alpha in the treatment of patients with advanced non-small-cell lung cancer. J. Immunother. 12:1 (1992), 70–73 1991.
19. [19] Schiller, J.H., Morgan-Ihrig, C., Levitt, M.L., Concomitant administration of interleukin-2 plus tumor necrosis factor in advanced non-small cell lung cancer. Am. J. Clin. Oncol. 18:1 (1995), 47–51.
20. [20] van der Bruggen, P., et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254:5038 (1991), 1643–1647.
21. [21] Chianese-Bullock, K.A., et al. MAGE-A1-, MAGE-A10-, and gp100-derived peptides are immunogenic when combined with granulocyte-macrophage colony-stimulating factor and montanide ISA-51 adjuvant and administered as part of a multipeptide vaccine for melanoma. J. Immunol. 174:5 (2005), 3080–3086.
22. [22] Butterfield, L.H., Cancer vaccines. BMJ, 350, 2015, h988.
23. [23] Ribas, A., et al. Current developments in cancer vaccines and cellular immunotherapy. J. Clin. Oncol. 21:12 (2003), 2415–2432.
24. [24] Melero, I., et al. Therapeutic vaccines for cancer: an overview of clinical trials. Nat. Rev. Clin. Oncol. 11:9 (2014), 509–524.
25. [25] Vujanovic, L., Butterfield, L.H., Melanoma cancer vaccines and anti-tumor T cell responses. J. Cell. Biochem. 102:2 (2007), 301–310.
26. [26] Hoon, D.S., et al. Melanoma patients immunized with melanoma cell vaccine induce antibody responses to recombinant MAGE-1 antigen. J. Immunol. 154:2 (1995), 730–737.
27. [27] Kruit, W.H., et al. Phase 1/2 study of subcutaneous and intradermal immunization with a recombinant MAGE-3 protein in patients with detectable metastatic melanoma. Int. J. Cancer 117:4 (2005), 596–604.
28. [28] Restifo, N.P., Dudley, M.E., Rosenberg, S.A., Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12:4 (2012), 269–281.
29. [29] Rosenberg, S.A., et al. Gene transfer into humans–immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N. Engl. J. Med. 323:9 (1990), 570–578.
30. [30] Rosenberg, S.A., et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N. Engl. J. Med. 319:25 (1988), 1676–1680.
31. [31] Dudley, M.E., et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298:5594 (2002), 850–854.
32. [32] Rosenberg, S.A., et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17:13 (2011), 4550–4557.
33. [33] Kershaw, M.H., Westwood, J.A., Darcy, P.K., Gene-engineered T cells for cancer therapy. Nat. Rev. Cancer 13:8 (2013), 525–541.
34. [34] Fife, B.T., Bluestone, J.A., Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol. Rev. 224 (2008), 166–182.
35. [35] Surh, C.D., Sprent, J., T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:6501 (1994), 100–103.
36. [36] Brunet, J.F., et al. A new member of the immunoglobulin superfamily–CTLA-4. Nature 328:6127 (1987), 267–270.
37. [37] Linsley, P.S., et al. CTLA-4 is a second receptor for the B cell activation antigen B7. J. Exp. Med. 174:3 (1991), 561–569.
38. [38] Walunas, T.L., et al. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1:5 (1994), 405–413.
39. [39] Walunas, T.L., Bakker, C.Y., Bluestone, J.A., CTLA-4 ligation blocks CD28-dependent T cell activation. J. Exp. Med. 183:6 (1996), 2541–2550.
40. [40] Topalian, S.L., Drake, C.G., Pardoll, D.M., Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 27:4 (2015), 450–461.
41. [41] Tivol, E.A., et al. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3:5 (1995), 541–547.
42. [42] Waterhouse, P., et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 270:5238 (1995), 985–988.
43. [43] Blank, C., et al. PD-L1/B7H-1 inhibits the effector phase of tumor rejection by T cell receptor (TCR) transgenic CD8 + T cells. Cancer Res. 64:3 (2004), 1140–1145.
44. [44] Freeman, G.J., et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192:7 (2000), 1027–1034.
45. [45] Ishida, Y., et al. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11:11 (1992), 3887–3895.
46. [46] Keir, M.E., et al. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26 (2008), 677–704.
47. [47] Spranger, S., et al. Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8(+) T cells directly within the tumor microenvironment. J. Immunother. Cancer, 2, 2014, 3.
48. [48] Barber, D.L., et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:7077 (2006), 682–687.
49. [49] Dong, H., et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8:8 (2002), 793–800.
50. [50] Ahmadzadeh, M., et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 114:8 (2009), 1537–1544.
51. [51] Nishimura, H., et al. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11:2 (1999), 141–151.
52. [52] Nishimura, H., et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291:5502 (2001), 319–322.
53. [53] Huang, C.T., et al. Role of LAG-3 in regulatory T cells. Immunity 21:4 (2004), 503–513.
54. [54] Woo, S.R., et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res. 72:4 (2012), 917–927.
55. [55] Leach, D.R., Krummel, M.F., Allison, J.P., Enhancement of antitumor immunity by CTLA-4 blockade. Science 271:5256 (1996), 1734–1736.
56. [56] Robert, C., et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med. 364:26 (2011), 2517–2526.
57. [57] Hodi, F.S., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363:8 (2010), 711–723.
58. [58] Schadendorf, D., et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma. J. Clin. Oncol. 33:17 (2015), 1889–1894.
59. [59] Prieto, P.A., et al. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin. Cancer Res. 18:7 (2012), 2039–2047.
60. [60] Wolchok, J.D., et al. Four-year survival rates for patients with metastatic melanoma who received ipilimumab in phase II clinical trials. Ann. Oncol. 24:8 (2013), 2174–2180.
61. [61] Ribas, A., Flaherty, K.T., Gauging the long-term benefits of ipilimumab in melanoma. J. Clin. Oncol. 33:17 (2015), 1865–1866.
62. [62] Robert, C., et al. Pembrolizumab versus ipilimumab in advanced melanoma. N. Engl. J. Med. 372:26 (2015), 2521–2532.
63. [63] Robert, C., et al. Nivolumab in previously untreated melanoma without BRAF mutation. N. Engl. J. Med. 372:4 (2015), 320–330.
64. [64] Ackerman, A., et al. Outcomes of patients with metastatic melanoma treated with immunotherapy prior to or after BRAF inhibitors. Cancer 120:11 (2014), 1695–1701.
65. [65] Bhatia, S., Thompson, J.A., PD-1 blockade in melanoma: a promising start, but a long way to go. JAMA 315:15 (2016), 1573–1575.
66. [66] Wolchok, J.D., et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369:2 (2013), 122–133.
67. [67] Larkin, J., Hodi, F.S., Wolchok, J.D., Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 373:13 (2015), 1270–1271.
68. [68] Wolchok, J.D., et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin. Cancer Res. 15:23 (2009), 7412–7420.
69. [69] Gangadhar, T.C., Vonderheide, R.H., Mitigating the toxic effects of anticancer immunotherapy. Nat. Rev. Clin. Oncol. 11:2 (2014), 91–99.
70. [70] Weber, J.S., et al. Patterns of onset and resolution of immune-related adverse events of special interest with ipilimumab: detailed safety analysis from a phase 3 trial in patients with advanced melanoma. Cancer 119:9 (2013), 1675–1682.
71. [71] Dillard, T., et al. Anti-CTLA-4 antibody therapy associated autoimmune hypophysitis: serious immune related adverse events across a spectrum of cancer subtypes. Pituitary 13:1 (2010), 29–38.
72. [72] Ansell, S.M., et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N. Engl. J. Med. 372:4 (2015), 311–319.
73. [73] Herbst, R.S., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515:7528 (2014), 563–567.
74. [74] Taube, J.M., et al. Differential expression of immune-regulatory genes associated with PD-L1 display in melanoma: implications for PD-1 pathway blockade. Clin. Cancer Res. 21:17 (2015), 3969–3976.
75. [75] Johnson, D.B., et al. Melanoma-specific MHC-II expression represents a tumour-autonomous phenotype and predicts response to anti-PD-1/PD-L1 therapy. Nat. Commun., 7, 2016, 10582.
76. [76] Tumeh, P.C., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515:7528 (2014), 568–571.
77. [77] Lynch, T.J., et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J. Clin. Oncol. 30:17 (2012), 2046–2054.
78. [78] Reck, M., et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial. Ann. Oncol. 24:1 (2013), 75–83.
79. [79] Topalian, S.L., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366:26 (2012), 2443–2454.
80. [80] Brahmer, J.R., et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 28:19 (2010), 3167–3175.
81. [81] Snyder, A., et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371:23 (2014), 2189–2199.
82. [82] Rizvi, N.A., et al. Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer. Science, 2015.
83. [83] Van Allen, E.M., et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 350:6257 (2015), 207–211.
84. [84] Garon, E.B., et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N. Engl. J. Med. 372:21 (2015), 2018–2028.
85. [85] Yadav, M., et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 515:7528 (2014), 572–576.
86. [86] Jones, B., Clinical genetics. Sequencing for tailored melanoma immunotherapy. Nat. Rev. Genet., 16(5), 2015, 259.
87. [87] Hua, C., et al. Association of vitiligo with tumor response in patients with metastatic melanoma treated with pembrolizumab. JAMA Dermatol. 152:1 (2016), 45–51.
88. [88] Sanlorenzo, M., et al. Pembrolizumab cutaneous adverse events and their association with disease progression. JAMA Dermatol. 151:11 (2015), 1206–1212.
89. [89] Vanderlugt, C.L., Miller, S.D., Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat. Rev. Immunol. 2:2 (2002), 85–95.