Cytotoxic T lymphocyte antigen-4 and immune checkpoint blockade

Journal of Clinical Investigation

Volumn 125, Issue 9, 2015, Pages 3377-3383

  Buchbinder, Elizabeth ^a   Stephen Hodi, F ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DABRAFENIB; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 2; IPILIMUMAB; NIVOLUMAB; TRAMETINIB; VEMURAFENIB; CTLA4 PROTEIN, HUMAN; MONOCLONAL ANTIBODY;

CANCER IMMUNOTHERAPY; HUMAN; IMMUNE CHECKPOINT BLOCKADE; IMMUNE RESPONSE; IMMUNE SYSTEM; MELANOMA; NONHUMAN; PATIENT SELECTION; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECTS; IMMUNOLOGY; METASTASIS; PATHOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL CYCLE CHECKPOINTS; CTLA-4 ANTIGEN; HUMANS; MELANOMA; NEOPLASM METASTASIS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84941615057     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80012     Document Type: Review

References (87)

1. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol. 2011;29:235-271
2. Atkins MB, 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. 1999;17(7):2105-2116
3. Rosenberg SA, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res. 2011;17(13):4550-4557
4. Fong L, Small EJ. Anti-cytotoxic T-lymphocyte antigen-4 antibody: the first in an emerging class of immunomodulatory antibodies for cancer treatment. J Clin Oncol. 2008;26(32):5275-5283
5. Mocellin S, Nitti D. CTLA-4 blockade and the renaissance of cancer immunotherapy. Biochim Biophys Acta. 2013;1836(2):187-196
6. Poschke I, Mougiakakos D, Kiessling R. Camouflage and sabotage: tumor escape from the immune system. Cancer Immunol Immunother. 2011;60(8):1161-1171
7. Bronte V, Mocellin S. Suppressive influences in the immune response to cancer. J Immunother. 2009;32(1):1-11
8. Allison JP, Hurwitz AA, Leach DR. Manipulation of costimulatory signals to enhance antitumor T-cell responses. Curr Opin Immunol. 1995;7(5):682-686
9. Bretscher P, Cohn M. A theory of self-nonself discrimination. Science. 1970;169(3950):1042-1049
10. Sharpe AH, Abbas AK. T-cell costimulation-biology, therapeutic potential, and challenges. N Engl J Med. 2006;355(10):973-975
11. Kroczek RA, Mages HW, Hutloff A. Emerging paradigms of T-cell co-stimulation. Curr Opin Immunol. 2004;16(3):321-327
12. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol. 2002;2(2):116-126
13. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev. 2008;224:166-182
14. Scalapino KJ1, Daikh DI. CTLA-4: a key regulatory point in the control of autoimmune disease. Immunol Rev. 2008;223:143-155
15. Walunas TL, et al. CTLA-4 can function as a negative regulator of T cell activation. Immunity. 1994;1(5):405-413
16. Linsley PS, Bradshaw J, Greene J, Peach R, Bennett KL, Mittler RS. Intracellular trafficking of CTLA-4 and focal localization towards sites of TCR engagement. Immunity. 1996;4(6):535-543
17. Egen JG, Allison JP. Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. Immunity. 2002;16(1):23-35
18. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med. 1995;182(2):459-465
19. Qureshi OS, et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science. 2011;332(6029):600-603
20. Brunner MC, Chambers CA, Chan FK, Hanke J, Winoto A, Allison JP. CTLA-4-mediated inhibition of early events of T cell proliferation. J Immunol. 1999;162(10):5813-5820
21. Marengere LE, Waterhouse P, Duncan GS, Mittrucker HW, Feng GS, Mak TW. Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4. Science. 1996;272(5265):1170-1173
22. Parry RV, et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol. 2005;25(21):9543-9553
23. Takahashi T, et al. Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-Associated antigen 4. J Exp Med. 2000;192(2):303-310
24. Waterhouse P, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270(5238):985-988
25. Wing K, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 2008;322(5899):271-275
26. Selby MJ, et al. Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells. Cancer Immunol Res. 2013;1(1):32-42
27. Simpson TR, et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J Exp Med. 2013;210(9):1695-1710
28. Peggs KS, Quezada SA, Chambers CA, Korman AJ, Allison JP. Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med. 2009;206(8):1717-1725
29. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science. 1996;271(5256):1734-1736
30. Kwon ED, et al. Manipulation of T cell costimulatory and inhibitory signals for immunotherapy of prostate cancer. Proc Natl Acad Sci U S A. 1997;94(15):8099-8103
31. van Elsas A, Hurwitz AA, Allison JP. Combination immunotherapy of B16 melanoma using anticytotoxic T lymphocyte-Associated antigen 4 (CTLA-4) and granulocyte/macrophage colonystimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J Exp Med. 1999;190(3):355-366
32. Keler T, et al. Activity and safety of CTLA-4 blockade combined with vaccines in cynomolgus macaques. J Immunol. 2003;171(11):6251-6259
33. Small EJ, Tchekmedyian NS, Rini BI, Fong L, Lowy I, Allison JP. A pilot trial of CTLA-4 blockade with human anti-CTLA-4 in patients with hormone-refractory prostate cancer. Clin Cancer Res. 2007;13(6):1810-1815
34. Hodi FS, et al. Biologic activity of cytotoxic T lymphocyte-Associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A. 2003;100(8):4712-4717
35. Kirkwood JM, Strawderman MH, Ernstoff MS, Smith TJ, Borden EC, Blum RH. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol. 1996;14(1):7-17
36. Tchekmedyian S, Glaspy J, Korman A, Keler T, Deo Y, Davis T. MDX-010 (human anti-CTLA4): a phase I trial in malignant melanoma. Proc Am Soc Clin Oncol. 2002;(Abstract 56).
37. Weber JS, et al. Phase I/II study of ipilimumab for patients with metastatic melanoma. J Clin Oncol. 2008;26(36):5950-5956
38. Maker AV, et al. Intrapatient dose escalation of anti-CTLA-4 antibody in patients with metastatic melanoma. J Immunother. 2006;29(4):455-463
39. Wolchok JD, et al. Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol. 2010;11(2):155-164
40. ODay SJ, et al. Efficacy and safety of ipilimumab monotherapy in patients with pretreated advanced melanoma: a multicenter single-Arm phase II study. Ann Oncol. 2010;21(8):1712-1717
41. Camacho LH, et al. Phase I/II trial of tremelimumab in patients with metastatic melanoma. J Clin Oncol. 2009;27(7):1075-1081
42. Hodi FS, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711-723
43. Patel PM, et al. Extended schedule, escalated dose temozolomide versus dacarbazine in stage IV melanoma: final results of a randomised phase III study (EORTC 18032). Eur J Cancer. 2011;47(10):1476-1483
44. Robert C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med. 2011;364(26):2517-2526
45. Ribas A, et al. Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol. 2013;31(5):616-622
46. Margolin K, et al. Ipilimumab in patients with melanoma and brain metastases: an open-label, phase 2 trial. Lancet Oncol. 2012;13(5):459-465
47. Calabro L, Danielli R, Sigalotti L, Maio M. Clinical studies with anti-CTLA-4 antibodies in non-melanoma indications. Semin Oncol. 2010;37(5):460-467
48. Lynch TJ, 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. 2012;30(17):2046-2054
49. Kwon ED, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol. 2014;15(7):700-712
50. Yang JC, et al. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunother. 2007;30(8):825-830
51. Wolchok JD, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15(23):7412-7420
52. Wolchok JD, et al. Development of ipilimumab: a novel immunotherapeutic approach for the treatment of advanced melanoma. Ann N Y Acad Sci. 2013;1291:1-13
53. Coit DG, et al. Melanoma, version 4. 2014. J Natl Compr Canc Netw. 2014;12(5):621-629
54. Robert C, Schadendorf D, Messina M, Hodi FS, ODay S, MDX010-20 investigators. Efficacy and safety of retreatment with ipilimumab in patients with pretreated advanced melanoma who progressed after initially achieving disease control. Clin Cancer Res. 2013;19(8):2232-2239
55. Prieto PA, et al. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin Cancer Res. 2012;18(7):2039-2047
56. McDermott D, Haanen J, Chen TT, Lorigan P, ODay S, MDX010-20 Investigators. Efficacy and safety of ipilimumab in metastatic melanoma patients surviving more than 2 years following treatment in a phase III trial (MDX010-20). Ann Oncol. 2013;24(10):2694-2698
57. Hamid O, et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Transl Med. 2011;9:204
58. Callahan MK, Postow MA, Wolchok JD. Immunomodulatory therapy for melanoma: ipilimumab and beyond. Clin Dermatol. 2013;31(2):191-199
59. Ji RR, et al. An immune-Active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother. 2012;61(7):1019-1031
60. Charen AS, et al. The neoantigen landscape underlying clinical response to ipilimumab. J Clin Oncol. 2014;32:5s(suppl; abstr 3003).
61. Adaniel C, et al. Germline genetic determinants of immunotherapy response in metastatic melanoma. J Clin Oncol. 2014;32:5s(suppl; abstr 3004)
62. Snyder A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014;371(23):2189-2199
63. Weber JS, Kahler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol. 2012;30(21):2691-2697
64. Weber JS, Dummer R, de Pril V, Lebbe C, Hodi FS, MDX010-20 Investigators. 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. 2013;119(9):1675-1682
65. Weber J, et al. A randomized, double-blind, placebo-controlled, phase II study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma. Clin Cancer Res. 2009;15(17):5591-5598
66. Blansfield JA, et al. Cytotoxic T-lymphocyteassociated antigen-4 blockage can induce autoimmune hypophysitis in patients with metastatic melanoma and renal cancer. J Immunother. 2005;28(6):593-598
67. Kyi C, Hellmann MD, Wolchok JD, Chapman PB, Postow MA. Opportunistic infections in patients treated with immunotherapy for cancer. J Immunother Cancer. 2014;2:19
68. Postow MA, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med. 2012;366(10):925-931
69. Stamell EF, Wolchok JD, Gnjatic S, Lee NY, Brownell I. The abscopal effect associated with a systemic anti-melanoma immune response. Int J Radiat Oncol Biol Phys. 2013;85(2):293-295
70. Chapman PB, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011;364(26):2507-2516
71. Robert C, et al. Improved overall survival in melanoma with combined dabrafenib and trametinib. N Engl J Med. 2015;372(1):30-39
72. Larkin J, et al. Combined vemurafenib and cobimetinib in BRAF-mutated melanoma. N Engl J Med. 2014;371(20):1867-1876
73. Boni A, et al. Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function. Cancer Res. 2010;70(13):5213-5219
74. Frederick DT, 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(5):1225-1231
75. Gargett T, Fraser CK, Dotti G, Yvon ES, Brown MP. BRAF and MEK inhibition variably affect GD2-specific chimeric antigen receptor (CAR) T-cell function in vitro. J Immunother. 2015;38(1):12-23
76. Ribas A, Hodi FS, Callahan M, Konto C, Wolchok J. Hepatotoxicity with combination of vemurafenib and ipilimumab. N Engl J Med. 2013;368(14):1365-1366
77. Motz GT, et al. Tumor endothelium FasL establishes a selective immune barrier promoting tolerance in tumors. Nat Med. 2014;20(6):607-615
78. Hodi FS, et al. Bevacizumab plus ipilimumab in patients with metastatic melanoma. Cancer Immunol Res. 2014;2(7):632-642
79. Maker AV, et al. Tumor regression and autoimmunity in patients treated with cytotoxic T lymphocyte-Associated antigen 4 blockade and interleukin 2: a phase I/II study. Ann Surg Oncol. 2005;12(12):1005-1016
80. Hodi FS, et al. Ipilimumab plus sargramostim vs ipilimumab alone for treatment of metastatic melanoma: a randomized clinical trial. JAMA. 2014;312(17):1744-1753
81. Topalian SL, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol. 2014;32(10):1020-1030
82. Robert C, et al. Anti-programmed-deathreceptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet. 2014;384(9948):1109-1117
83. Wolchok JD, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122-133
84. Sznol M, et al. Survival, response duration, and activity by BRAF mutation (MT) status of nivolumab (NIVO, anti-PD-1, BMS-936558, ONO-4538) and ipilimumab (IPI) concurrent therapy in advanced melanoma (MEL). J Clin Oncol. 2014;32:5s(suppl; abstr LBA9003).
85. Eggermont AM, et al. Ipilimumab versus placebo after complete resection of stage II melanoma: Initial efficacy and safety results from EORTC 18071 phase III trial. J Clin Oncol. 2014;32:5s(suppl; abstr LBA9008).
86. Jonasch E, et al. Adjuvant high-dose interferon alfa-2b in patients with high-risk melanoma. Cancer J. 2000;6(3):139-145
87. Buchbinder EI, McDermott DF. Cytotoxic T-lymphocyte antigen-4 blockade in melanoma. Clin Ther. 2015;37(4):755-763.