Programmed death-1 checkpoint blockade in acute myeloid leukemia

Expert Opinion on Biological Therapy

Volumn 15, Issue 8, 2015, Pages 1191-1203

  Sehgal, Alison ^a   Whiteside, Theresa L ^a   Boyiadzis, Michael ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Acute myeloid leukemia; Checkpoint inhibition; Immunotherapy; Programmed death 1

Indexed keywords

ANTINEOPLASTIC AGENT; BLOCKING ANTIBODY; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 1 BLOCKING ANTIBODY; UNCLASSIFIED DRUG; ANTIBODY; PROGRAMMED DEATH 1 RECEPTOR;

ACUTE MYELOBLASTIC LEUKEMIA; FOLLOW UP; HEMATOPOIETIC CELL; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE; IMMUNOLOGY; LEUKEMIA, MYELOID, ACUTE; T LYMPHOCYTE; TUMOR ESCAPE;

ANIMALS; ANTIBODIES; ANTIGENS, CD274; ANTINEOPLASTIC AGENTS; GENES, CDC; HUMANS; LEUKEMIA, MYELOID, ACUTE; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTES; TUMOR ESCAPE; UP-REGULATION;

EID: 84936952943     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2015.1051028     Document Type: Review

References (91)

1. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331(6024):1565-70
2. Topalian SL, Drake CG, Pardoll DM. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol 2012;24(2):207-12
3. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12(4):252-64
4. Tivol EA, Borriello F, Schweitzer AN, 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 1995;3(5):541-7
5. Waterhouse P, Penninger JM, Timms E, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 1995;270(5238):985-8
6. Parry RV, Chemnitz JM, Frauwirth KA, et al. CTLA-4 and PD-1 Receptors Inhibit T-Cell Activation by Distinct Mechanisms. Mol Cell Biol 2005;25(21):9543-53
7. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002;8(8):793-800
8. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996;271(5256):1734-6
9. Iwai Y, Ishida M, Tanaka Y, et al. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA 2002;99(19):12293-7
10. Hodi FS, Mihm MC, Soiffer RJ, 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 USA 2003;100(8):4712-17
11. Yang Y-F, Zou J-P, Mu J, et al. Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyteassociated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages. Cancer Res 1997;57(18):4036-41
12. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363(8):711-23
13. Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369(2):134-44
14. Freeman GJ, Long AJ, Iwai Y, 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 2000;192(7):1027-34
15. Tseng SY, Otsuji M, Gorski K, et al. B7- DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J Exp Med 2001;193(7):839-46
16. Latchman Y, Wood CR, Chernova T, et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001;2(3):261-8
17. Keir ME, Francisco LM, Sharpe AH. PD-1 and its ligands in T-cell immunity. Curr Opin Immunol 2007;19(3):309-14
18. Wilke CM, Wei S, Wang L, et al. Dual biological effects of the cytokines interleukin-10 and interferon-gamma. Cancer Immunol Immunother 2011;60(11):1529-41
19. Francisco LM, Salinas VH, Brown KE, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med 2009;206(13):3015-29
20. Pantaleo G, Koup RA. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat Med 2004;10(8):806-10
21. Letvin NL, Walker BD. Immunopathogenesis and immunotherapy in AIDS virus infections. Nat Med 2003;9(7):861-6
22. Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol 2005;5(3):215-29
23. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006;439(7077):682-7
24. Day CL, Kaufmann DE, Kiepiela P, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006;443(7109):350-4
25. Radziewicz H, Ibegbu CC, Fernandez ML, et al. Liver-infiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J Virol 2007;81(6):2545-53
26. Wang J, Yoshida T, Nakaki F, et al. Establishment of NOD-Pdcd1-/- mice as an efficient animal model of type I diabetes. Proc Natl Acad Sci USA 2005;102(33):11823-8
27. Nishimura H, Nose M, Hiai H, et al. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999;11(2):141-51
28. Okazaki T, Tanaka Y, Nishio R, et al. Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat Med 2003;9(12):1477-83
29. Old LJ, Boyse EA. Immunology of Experimental Tumors. Annu Rev Med 1964;15:167-86
30. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011;29:235-71
31. Whiteside TL. Induced regulatory T cells in inhibitory microenvironments created by cancer. Expert Opin Biol Ther 2014;14(10):1411-25
32. Chen DS, Irving BA, Hodi FS. Molecular pathways: next-generation immunotherapy-inhibiting programmed death-ligand 1 and programmed death-1. Clin Cancer Res 2012;18(24):6580-7
33. Thompson RH, Gillett MD, Cheville JC, et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc Natl Acad Sci USA 2004;101(49):17174-9
34. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366(26):2443-54
35. Gao Q, Wang XY, Qiu SJ, et al. Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma. Clin Cancer Res 2009;15(3):971-9
36. Hino R, Kabashima K, Kato Y, et al. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer 2010;116(7):1757-66
37. Mu CY, Huang JA, Chen Y, et al. High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol 2011;28(3):682-8
38. Taube JM, Klein A, Brahmer JR, et al. 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(19):5064-74
39. Nomi T, Sho M, Akahori T, et al. Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res 2007;13(7):2151-7
40. Okudaira K, Hokari R, Tsuzuki Y, et al. Blockade of B7-H1 or B7-DC induces an anti-tumor effect in a mouse pancreatic cancer model. Int J Oncol 2009;35(4):741-9
41. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci USA 2010;107(9):4275-80
42. Zhou Q, Xiao H, Liu Y, et al. Blockade of programmed death-1 pathway rescues the effector function of tumor-infiltrating T cells and enhances the antitumor efficacy of lentivector immunization. J Immunol 2010;185(9):5082-92
43. 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 2012;366(26):2455-65
44. Pasquini MC ZX. Current use and outcome of hematopoietic stem cell transplantation: CIBMTR Summary Slides. 2014. Available from: http://www.cibmtr.org [Accessed 1 March 2015]
45. Collins RH Jr, Shpilberg O, Drobyski WR, et al. Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. J Clin Oncol 1997;15(2):433-44
46. Kolb HJ, Schattenberg A, Goldman JM, et al. Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. Blood 1995;86(5):2041-50
47. Schmid C, Labopin M, Nagler A, et al. Donor lymphocyte infusion in the treatment of first hematological relapse after allogeneic stem-cell transplantation in adults with acute myeloid leukemia: a retrospective risk factors analysis and comparison with other strategies by the EBMT Acute Leukemia Working Party. J Clin Oncol 2007;25(31):4938-45
48. Goulmy E. Minor histocompatibility antigens: allo target molecules for tumorspecific immunotherapy. Cancer J 2004;10(1):1-7
49. Bodey B. Cancer-testis antigens: promising targets for antigen directed antineoplastic immunotherapy. Expert Opin Biol Ther 2002;2(6):577-84
50. Anguille S, Van Tendeloo VF, Berneman ZN. Leukemia-associated antigens and their relevance to the immunotherapy of acute myeloid leukemia. Leukemia 2012;26(10):2186-96
51. Makita M, Azuma T, Hamaguchi H, et al. Leukemia-associated fusion proteins, dek-can and bcr-abl, represent immunogenic HLA-DR-restricted epitopes recognized by fusion peptidespecific CD4+ T lymphocytes. Leukemia 2002;16(12):2400-7
52. Osman Y, Takahashi M, Zheng Z, et al. Dendritic cells stimulate the expansion of PML-RAR alpha specific cytotoxic T-lymphocytes: its applicability for antileukemia immunotherapy. J Exp Clin Cancer Res 1999;18(4):485-92
53. Graf C, Heidel F, Tenzer S, et al. A neoepitope generated by an FLT3 internal tandem duplication (FLT3-ITD) is recognized by leukemiareactive autologous CD8+ T cells. Blood 2007;109(7):2985-8
54. Greiner J, Ono Y, Hofmann S, et al. Mutated regions of nucleophosmin 1 elicit both CD4(+) and CD8(+) T-cell responses in patients with acute myeloid leukemia. Blood 2012;120(6):1282-9
55. Buggins AG, Milojkovic D, Arno MJ, et al. Microenvironment produced by acute myeloid leukemia cells prevents T cell activation and proliferation by inhibition of NF-kappaB, c-Myc, and pRb pathways. J Immunol 2001;167(10):6021-30
56. Mussai F, De Santo C, Abu-Dayyeh I, et al. Acute myeloid leukemia creates an arginase-dependent immunosuppressive microenvironment. Blood 2013;122(5):749-58
57. Iachininoto MG, Nuzzolo ER, Bonanno G, et al. Cyclooxygenase-2 (COX-2) inhibition constrains indoleamine 2,3-dioxygenase 1 (IDO1) activity in acute myeloid leukaemia cells. Molecules 2013;18(9):10132-45
58. Locafaro G, Amodio G, Tomasoni D, et al. HLA-G expression on blasts and tolerogenic cells in patients affected by acute myeloid leukemia. J Immunol Res 2014;2014:636292
59. Chen X, Kline DE, Kline J. Peripheral T-cell tolerance in hosts with acute myeloid leukemia. Oncoimmunology 2013;2(8):e25445
60. Szczepanski MJ, Szajnik M, Czystowska M, et al. Increased frequency and suppression by regulatory T cells in patients with acute myelogenous leukemia. Clin Cancer Res 2009;15(10):3325-32
61. Ustun C, Miller JS, Munn DH, et al. Regulatory T cells in acute myelogenous leukemia: is it time for immunomodulation? Blood 2011;118(19):5084-95
62. Zhou Q, Bucher C, Munger ME, et al. Depletion of endogenous tumorassociated regulatory T cells improves the efficacy of adoptive cytotoxic T-cell immunotherapy in murine acute myeloid leukemia. Blood 2009;114(18):3793-802
63. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 2004;4(10):762-74
64. Fallarino F, Grohmann U, You S, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J Immunol 2006;176(11):6752-61
65. Curti A, Pandolfi S, Valzasina B, et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood 2007;109(7):2871-7
66. Corm S, Berthon C, Imbenotte M, et al. Indoleamine 2,3-dioxygenase activity of acute myeloid leukemia cells can be measured from patients' sera by HPLC and is inducible by IFN-gamma. Leuk Res 2009;33(3):490-4
67. Shenghui Z, Yixiang H, Jianbo W, et al. Elevated frequencies of CD4(+) CD25(+) CD127lo regulatory T cells is associated to poor prognosis in patients with acute myeloid leukemia. Int J Cancer 2011;129(6):1373-81
68. Wang X, Zheng J, Liu J, et al. Increased population of CD4(+)CD25(high), regulatory T cells with their higher apoptotic and proliferating status in peripheral blood of acute myeloid leukemia patients. Eur J Haematol 2005;75(6):468-76
69. Lichtenegger FS, Lorenz R, Gellhaus K, et al. Impaired NK cells and increased T regulatory cell numbers during cytotoxic maintenance therapy in AML. Leuk Res 2014;38(8):964-9
70. Kanakry CG, Hess AD, Gocke CD, et al. Early lymphocyte recovery after intensive timed sequential chemotherapy for acute myelogenous leukemia: peripheral oligoclonal expansion of regulatory T cells. Blood 2011;117(2):608-17
71. Jie HB, Gildener-Leapman N, Li J, et al. Intratumoral regulatory T cells upregulate immunosuppressive molecules in head and neck cancer patients. Br J Cancer 2013;109(10):2629-35
72. Amarnath S, Mangus CW, Wang JC, et al. The PDL1-PD1 axis converts human TH1 cells into regulatory T cells. Sci Transl Med 2011;3(111):111ra20
73. Zhou Q, Munger ME, Highfill SL, et al. Program death-1 signaling and regulatory T cells collaborate to resist the function of adoptively transferred cytotoxic T lymphocytes in advanced acute myeloid leukemia. Blood 2010;116(14):2484-93
74. Zhang L, Gajewski TF, Kline J. PD-1/ PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 2009;114(8):1545-52
75. Yang H, Bueso-Ramos C, DiNardo C, et al. Expression of PD-L1, PD-L2, PD- 1 and CTLA4 in myelodysplastic syndromes is enhanced by treatment with hypomethylating agents. Leukemia 2014;28(6):1280-8
76. Kronig H, Kremmler L, Haller B, et al. Interferon-induced programmed deathligand 1 (PD-L1/B7-H1) expression increases on human acute myeloid leukemia blast cells during treatment. Eur J Haematol 2014;92(3):195-203
77. Norde WJ, Maas F, Hobo W, et al. PD- 1/PD-L1 interactions contribute to functional T-cell impairment in patients who relapse with cancer after allogeneic stem cell transplantation. Cancer Res 2011;71(15):5111-22
78. Laszlo GS, Gudgeon CJ, Harrington KH, et al. Cellular determinants for preclinical activity of a novel CD33/CD3 bispecific T-cell engager (BiTE) antibody, AMG 330, against human AML. Blood 2014;123(4):554-61
79. Krupka C, Kufer P, Kischel R, et al. CD33 target validation and sustained depletion of AML blasts in long-term cultures by the bispecific T-cell-engaging antibody AMG 330. Blood 2014;123(3):356-65
80. Pyzer AR, Avigan DE, Rosenblatt J. Clinical trials of dendritic cell-based cancer vaccines in hematologic malignancies. Hum Vaccin Immunother 2014;10(11):3125-31
81. Woo SR, Turnis ME, Goldberg MV, et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res 2012;72(4):917-27
82. Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013;369(2):122-33
83. Triebel F, Jitsukawa S, Baixeras E, et al. LAG-3, a novel lymphocyte activation gene closely related to CD4. J Exp Med 1990;171(5):1393-405
84. Kisielow M, Kisielow J, Capoferri-Sollami G, Karjalainen K. Expression of lymphocyte activation gene 3 (LAG-3) on B cells is induced by T cells. Eur J Immunol 2005;35(7):2081-8
85. Matsuzaki J, Gnjatic S, Mhawech-Fauceglia P, et al. Tumor-infiltrating NY-ESO-1-specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer. Proc Natl Acad Sci USA 2010;107(17):7875-80
86. Berrien-Elliott MM, Jackson SR, Meyer JM, et al. Durable adoptive immunotherapy for leukemia produced by manipulation of multiple regulatory pathways of CD8+ T-cell tolerance. Cancer Res 2013;73(2):605-16
87. Jin HT, Anderson AC, Tan WG, et al. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci USA 2010;107(33):14733-8
88. Takamura S, Tsuji-Kawahara S, Yagita H, et al. Premature terminal exhaustion of Friend virus-specific effector CD8+ T cells by rapid induction of multiple inhibitory receptors. J Immunol 2010;184(9):4696-707
89. Sakuishi K, Apetoh L, Sullivan JM, et al. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore antitumor immunity. J Exp Med 2010;207(10):2187-94
90. Zhou Q, Munger ME, Veenstra RG, et al. Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood 2011;117(17):4501-10
91. Whiteside TL. Inhibiting the inhibitors: evaluating agents targeting cancer immunosuppression. Expert Opin Biol Ther 2010;10(7):1019-35