Programmed death-1 immune checkpoint blockade in the treatment of hematological malignancies

Annals of Medicine

Volumn 48, Issue 6, 2016, Pages 428-439

  Tsirigotis, Panagiotis ^a   Savani, Bipin N ^b   Nagler, Arnon ^c  

^a UNIVERSITY OF ATHENS   (Greece)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c SHEBA MEDICAL CENTER   (Israel)

Author keywords

Hematological malignancies; immune checkpoint; leukemia; lymphoma; monoclonal antibodies; programmed death 1; targeted therapy; toxicity

Indexed keywords

ANTINEOPLASTIC AGENT; IPILIMUMAB; NIVOLUMAB; PEMBROLIZUMAB; PIDILIZUMAB; PROGRAMMED DEATH 1 RECEPTOR; TUMOR VACCINE; MONOCLONAL ANTIBODY; PDCD1 PROTEIN, HUMAN;

ALLOGENEIC STEM CELL TRANSPLANTATION; DRUG SAFETY; FOLLICULAR LYMPHOMA; HEMATOLOGIC MALIGNANCY; HODGKIN DISEASE; HUMAN; IMMUNOMODULATION; LARGE CELL LYMPHOMA; MULTIPLE MYELOMA; NONHODGKIN LYMPHOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; ANTAGONISTS AND INHIBITORS; CLINICAL TRIAL (TOPIC); DRUG EFFECTS; HEMATOLOGIC NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; SIGNAL TRANSDUCTION;

ANTIBODIES, MONOCLONAL; CLINICAL TRIALS AS TOPIC; HEMATOLOGIC NEOPLASMS; HUMANS; MOLECULAR TARGETED THERAPY; PROGRAMMED CELL DEATH 1 RECEPTOR; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

EID: 84969848944     PISSN: 07853890     EISSN: 13652060     Source Type: Journal    
DOI: 10.1080/07853890.2016.1186827     Document Type: Review

References (78)

1. P.Linsley, J.Ledbetter The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol. 1993;11:191–12.
2. W.K.Suh, A.Tafuri, N.N.Berg-Brown, A.Shahinian, S.Plyte, G.S.Duncan,. The inducible costimulator plays the major costimulatory role in humoral immune responses in the absence of CD28. J Immunol. 2004;172:5917–23.
3. D.M.Sansom, C.N.Manzotti, Y.Zheng What’s the difference between CD80 and CD86? Trends Immunol. 2003;24:313–18.
4. O.Joffre, M.A.Nolte, R.Sporri, C.Reis e Sousa Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev. 2009;227:234–47.
5. M.E.Keir, M.J.Butte, G.J.Freeman, A.H.Sharpe PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677–704.
6. L.S.Walker Treg and CTLA-4:Two intertwining pathways to immune tolerance. J Autoimmun. 2013;45:49–57.
7. D.Gardner, L.E.Jeffery, D.M.Sansom Understanding the CD28/CTLA-4 (CD152) pathway and its implications for costimulatory blockade. Am J Transplant. 2014;14:1985–91.
8. P.S.Linsley, J.L.Greene, W.Brady, J.Bajorath, J.A.Ledbetter, R.Peach Human B7-1 (CD80) and B7-2 (CD86) bind with similar avidities but distinct kinetics to CD28 and CTLA-4 receptors. Immunity. 1994;1:793–801.
9. E.A.Tivol, F.Borriello, A.N.Schweitzer, W.P.Lynch, J.A.Bluestone, A.H.Sharpe Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity. 1995;3:541–7.
10. Y.Latchman, C.R.Wood, T.Chernova, D.Chaudhary, M.Borde, I.Chernova,. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol. 2001;2:261–8.
11. H.Nishimura, M.Nose, H.Hiai, N.Minato, T.Honjo Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity. 1999;11:141–51.
12. L.M.1.Francisco, V.H.Salinas, K.E.Brown, V.K.Vanguri, G.J.Freeman, V.K.Kuchroo,. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 2009;206:3015–29.
13. C.L.Day, D.E.Kaufmann, P.Kiepiela, J.A.Brown, E.S.Moodley, S.Reddy,. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature. 2006;443:350–4.
14. L.M.Francisco, P.T.Sage, A.H.Sharpe The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010;236:219–42.
15. B.Lepenies, T.Jacobs The role of negative costimulators during parasitic infections. Endocr Metab Immune Disord Drug Targets. 2008;8:279–88.
16. S.Urbani, B.Amadei, D.Tola, G.Pedrazzi, L.Sacchelli, M.C.Cavallo,. Restoration of HCV-specific T cell functions by PD-1/PD-L1 blockade in HCV infection:effect of viremia levels and antiviral treatment. J Hepatol. 2008;48:548–58.
17. H.Dong, S.E.Strome, D.R.Salomao, H.Tamura, F.Hirano, D.B.Flies,. Tumor-associated B7-H1 promotes T-cell apoptosis:a potential mechanism of immune evasion. Nat Med. 2002;8:793–800.
18. M.Ahmadzadeh, L.A.Johnson, B.Heemskerk, J.R.Wunderlich, M.E.Dudley, D.E.White,. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood. 2009;114:1537–44.
19. Y.Iwai, M.Ishida, Y.Tanaka, T.Okazaki, T.Honjo, N.Minato 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;99:12293–7.
20. S.E.1.Strome, H.Dong, H.Tamura, S.G.Voss, D.B.Flies, K.Tamada,. B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res. 2003;63:6501–5.
21. R.Berger, R.Rotem-Yehudar, G.Slama, S.Landes, A.Kneller, M.Leiba,. Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res. 2008;14:3044–51.
22. P.Armand, A.Nagler, E.A.Weller, S.M.Devine, D.E.Avigan, Y.B.Chen,. Disabling immune tolerance by programmed death-1 blockade with pidilizumab after autologous hematopoietic stem-cell transplantation for diffuse large B-cell lymphoma:results of an international phase II trial. J Clin Oncol. 2013;31:4199–206.
23. S.L.Topalian, F.S.Hodi, J.R.Brahmer, S.N.Gettinger, D.C.Smith, D.F.McDermott,. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;28:2443–54.
24. F.S.Hodi, S.J.O'Day, D.F.McDermott, R.W.Weber, J.A.Sosman, J.B.Haanen,. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711–23.
25. O.Hamid, C.Robert, A.Daud, F.S.Hodi, W.J.Hwu, R.Kefford,. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013;369:134–44.
26. C.Robert, G.V.Long, B.Brady, C.Dutriaux, M.Maio, L.Mortier,. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320–30.
27. F.Balkwill, M.Capasso, T.Hagemann The tumor microenvironment at a glance. J Cell Sci. 2012;125:5591–6.
28. M.Teng, S.Ngiow, A.Ribas, M.Smyth Classifying cancers based on T-cell infiltration and PD-L1. Cancer Res. 2015;75:1–7.
29. L.Fehrenbacher, A.Spira, M.Ballinger, M.Kowanetz, J.Vansteenkiste, J.Mazieres,. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR):a multicentre, open-label, phase 2 randomised controlled trial. Lancet. 2016;387:1837–46.
30. H.Ueda, J.M.Howson, L.Esposito, L.Esposito, J.Heward, H.Snook,. Association of the T-cell regulatory gene CTLA-4 with susceptibility to autoimmune disease. Nature. 2003;423:506–11.
31. Y.Metaxas, H.Bertz, A.Spyridonidis, M.Spyroupoulou-Vlachou, C.Porzelius, J.Finke CT60 single-nucleotide polymorphism as a surrogate marker for donor lymphocyte infusion outcome after allogeneic cell transplantation for acute leukemia. Bone Marrow Transplant. 2012;47:411–15.
32. J.Brahmer, K.L.Reckamp, P.Baas, L.Crinò, W.E.Eberhardt, E.Poddubskaya,. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123–35.
33. J.M.Taube, A.Klein, J.R.Brahmer, H.Xu, X.Pan, J.H.Kim,. 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.
34. R.S.Herbst, J.C.Soria, M.Kowanetz, G.D.Fine, O.Hamid, M.S.Gordon,. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515:563–7.
35. D.M.Dorfman, J.A.Brown, A.Shahsafaei, G.J.Freeman Programmed death-1 (PD-1) is a marker of germinal center-associated T cells and angioimmunoblastic T-cell lymphoma. Am J Surg Pathol. 2006;30:802–10.
36. L.Xerri, B.Chetaille, N.Serriari, C.Attias, Y.Guillaume, C.Arnoulet,. Programmed death 1 is a marker of angioimmunoblastic T-cell lymphoma and B-cell small lymphocytic lymphoma/chronic lymphocytic leukemia. Hum Pathol. 2008;39:1050–8.
37. T.Shimauchi, K.Kabashima, D.Nakashima, K.Sugita, Y.Yamada, R.Hino,. Augmented expression of programmed death-1 in both neoplastic and nonneoplastic CD4+ T-cells in adult T-cell leukemia/lymphoma. Int J Cancer. 2007;121:2585–90.
38. M.R.Green, S.Rodig, P.Juszczynski, J.Ouyang, P.Sinha, E.O'Donnell,. Constitutive AP-1 activity and EBV infection induce PD-L1 in Hodgkin lymphomas and posttransplant lymphoproliferative disorders:implications for targeted therapy. Clin Cancer Res. 2012;18:1611–88.
39. J.A.Brown, D.M.Dorfman, F.R.Ma, E.L.Sullivan, O.Munoz, C.R.Wood,. Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production. J Immunol. 2003;170:1257–66.
40. J.Kiyasu, H.Miyoshi, A.Hirata, F.Arakawa, A.Ichikawa, D.Niino,. Expression of programmed cell death ligand 1 is associated with poor overall survival in patients with diffuse large B-cell lymphoma. Blood. 2015;126:2193–201.
41. D.Twa, F.Chan, S.Ben-Neriah, B.Woolcock, A.Mottok, K.Tan,. Genomic rearrangements involving programmed death ligands are recurrent in primary mediastinal large B-cell lymphoma. Blood. 2014;123:2062–5.
42. J.H.Myklebust, J.M.Irish, J.Brody, D.K.Czerwinski, R.Houot, H.E.Kohrt,. High PD-1 expression and suppressed cytokine signaling distinguish T cells infiltrating follicular lymphoma tumors from peripheral T cells. Blood. 2013;121:1367–76.
43. J.Carreras, A.Lopez-Guillermo, G.Roncador, N.Villamor, L.Colomo, A.Martinez,. High numbers of tumor-infi ltrating programmed cell death 1-positive regulatory lymphocytes are associated with improved overall survival in follicular lymphoma. J Clin Oncol. 2009;27:1470–6.
44. A.M.Lesokhin, S.M.Ansell, P.Armand, E.C.Scott, A.Halwani, M.Gutierrez,. Preliminary results of a phase I study of nivolumab (BMS-936558) in patients with relapsed or refractory lymphoid malignancies. Blood. 2014;124:291.
45. R.A.Wilcox, A.L.Feldman, D.A.Wada, Z.Z.Yang, N.I.Comfere, H.Dong,. B7-H1 (PD-L1, CD274) suppresses host immunity in T-cell lymphoproliferative disorders. Blood. 2009;114:2149–58.
46. L.Han, F.Liu, R.Li, Z.Li, X.Chen, Z.Zhou,. Role of programmed death ligands in effective T-cell interactions in extranodal natural killer/T-cell lymphoma. Oncol Lett. 2014;8:1461–9.
47. M.R.Green, S.Monti, S.J.Rodig, P.Juszczynski, T.Currie, E.O'Donnell,. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood. 2010;116:3268–77.
48. B.J.Chen, B.Chapuy, J.Ouyang, H.H.Sun, M.G.Roemer, M.L.Xu,. PD-L1 expression is characteristic of a subset of aggressive B-cell lymphomas and virus-associated malignancies. Clin Cancer Res. 2013;19:3462–73.
49. B.Chetaille, F.Bertucci, P.Finetti, B.Esterni, A.Stamatoullas, J.M.Picquenot,. Molecular profiling of classical Hodgkin lymphoma tissues uncovers variations in the tumor microenvironment and correlations with EBV infection and outcome. Blood. 2009;113:2765–75.
50. R.Yamamoto, M.Nishikori, T.Kitawaki, T.Sakai, M.Hishizawa, M.Tashima,. PD-1-PD-1 ligand interaction contributes to immunosuppressive microenvironment of Hodgkin lymphoma. Blood. 2008;111:3220–4.
51. J.M.Chemnitz, D.Eggle, J.Driesen, S.Classen, J.L.Riley, S.Debey-Pascher,. RNA fingerprints provide direct evidence for the inhibitory role of TGFbeta and PD-1 on CD4+ T cells in Hodgkin lymphoma. Blood. 2007;110:3226–33.
52. S.M.Ansell, A.M.Lesokhin, I.Borrello, A.Halwani, E.C.Scott, M.Gutierrez,. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med. 2015;372:311–19.
53. C.H.Moskowitz, V.Ribrag, J.-M.Michot, G.Martinelli, P.-L.Zinzani, M.Gutierrez,. PD-1 blockade with the monoclonal antibody pembrolizumab (MK-3475) in patients with classical Hodgkin lymphoma after brentuximab vedotin failure:preliminary results from a phase 1b study (KEYNOTE-013). Blood. 2014;124:290.
54. J.Liu, A.Hamrouni, D.Wolowiec, V.Coiteux, K.Kuliczkowski, D.Hetuin,. Plasma cells from multiple myeloma patients express B7-H1 (PD-L1) and increase expression after stimulation with IFN-gamma and TLR ligands via a MyD88-, TRAF6-, and MEK-dependent pathway. Blood. 2007;110:296–304.
55. S.Yousef, J.Marvin, M.Steinbach, A.Langemo, T.Kovacsovics, M.Binder,. Immunomodulatory molecule PD-L1 is expressed on malignant plasma cells and myeloma-propagating pre-plasma cells in the bone marrow of multiple myeloma patients. Blood Cancer J. 2015;5:e285.
56. M.Dhodapkar, R.Sexton, R.Das, K.Dhodapkar, L.Zhang, R.Sundaram,. Prospective analysis of antigen-specific immunity, stem-cell antigens, and immune checkpoints in monoclonal gammopathy. Blood. 2015;126:2475–8.
57. H.Yang, C.Bueso-Ramos, C.DiNardo, M.R.Estecio, M.Davanlou, Q.R.Geng,. Expression of PD-L1, PD-L2, PD-1 and CTLA4 in myelodysplastic syndromes is enhanced by treatment with hypomethylating agents. Leukemia. 2014;28:1280–8.
58. L.Zhang, T.F.Gajewski, J.Kline PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood. 2009;114:1545–52.
59. S.Mumprecht, C.Schurch, J.Schwaller, M.Solenthaler, A.F.Ochsenbein Programmed death 1 signaling on chronic myeloid leukemia specific T cells results in T-cell exhaustion and disease progression. Blood. 2009;114:1528–36.
60. D.J.1.Andorsky, R.E.Yamada, J.Said, G.S.Pinkus, D.J.Betting, J.M.Timmerman Programmed death ligand 1 is expressed by non-Hodgkin lymphomas and inhibits the activity of tumor-associated T cells. Clin Cancer Res. 2011;17:4232–44.
61. S.M.Ansell, M.Stenson, T.M.Habermann, D.F.Jelinek, T.E.Witzig. Cd4+ T-cell immune response to large B-cell non-Hodgkin's lymphoma predicts patient outcome. J Clin Oncol. 2001;19:720–6.
62. T.Guillaume, D.B.Rubinstein, M.Symann Immune reconstitution and immunotherapy after autologous hematopoietic stem cell transplantation. Blood. 1998;92:1471–90.
63. L.F.Porrata, M.R.Litzow, S.N.Markovic Immune reconstitution after autologous hematopoietic stem cell transplantation. Mayo Clin Proc. 2001;76:407–12.
64. P.Bachireddy, U.Hainz, M.Rooney, O.Pozdnyakova, J.Aldridge, W.Zhang Reversal of in situ T-cell exhaustion during effective human antileukemia responses to donor lymphocyte infusion. Blood. 2014;123:1412–21.
65. S.E.Sandner, M.R.Clarkson, A.D.Salama, A.Sanchez-Fueyo, D.C.HabichtDomenig C.,. Role of the programmed death-1 pathway in regulation of alloimmune responses in vivo. J Immunol. 2005;174:3408–15.
66. E.Ozkaynak, L.Wang, A.Goodearl, K.McDonald, S.Qin, T.O'Keefe,. Programmed death-1 targeting can promote allograft survival. J Immunol. 2002;169:6546–53.
67. T.Ito, T.Ueno, M.R.Clarkson, X.Yuan, M.M.Jurewicz, H.Yagita,. Analysis of the role of negative T cell costimulatory pathways in CD4 and CD8 T cell-mediated alloimmune responses in vivo. J Immunol. 2005;174:6648–56.
68. T.Yamazaki, H.Akiba, H.Iwai, H.Matsuda, M.Aoki, Y.Tanno,. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol. 2002;169:5538–45.
69. S.Nakae, H.Suto, M.Iikura, M.Kakurai, J.D.Sedgwick, M.Tsai,. Mast cells enhance T cell activation:importance of mast cell costimulatory molecules and secreted TNF. J Immunol. 2006;176:2238–48.
70. A.Saha, K.Aoyama, P.A.Taylor, B.H.Koehn, R.G.Veenstra, A.Panoskaltsis-Mortari Host programmed death ligand 1 is dominant over programmed death ligand 2 expression in regulating graft-versus-host disease lethality. Blood. 2013;122:3062–73.
71. H.Fujiwara, Y.Maeda, K.Kobayashi, H.Nishimori, K.Matsuoka, N.Fujii,. Programmed death-1 pathway in host tissues ameliorates Th17/Th1-mediated experimental chronic graft-versus-host disease. J Immunol. 2014;193:2565–73.
72. A.Bashey, B.Medina, S.Corringham, M.Pasek, E.Carrier, L.Vrooman,. CTLA4 blockade with ipilimumab to treat relapse of malignancy after allogeneic hematopoietic cell transplantation. Blood. 2009;113:1581–8.
73. J.Zhou, A.Bashey, R.Zhong, S.Corringham, K.Messer CTLA-4 blockade following relapse of malignancy after allogeneic stem cell transplantation is associated with T cell activation but not with increased levels of T regulatory cells. Biol Blood Marrow Transplant. 2011;17:682–92.
74. K.C.Soares, A.A.Rucki, A.A.Wu, K.Olino, Q.Xiao, Y.Chai,. PD-1/PD-L1 blockade together with vaccine therapy facilitates effector T-cell infiltration into pancreatic tumors. J Immunother. 2015;38:1–11.
75. C.Twyman-Saint Victor, A.J.Rech, A.Maity, R.Rengan, K.E.Pauken, E.Stelekati,. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature. 2015;520:373–7.
76. W.Jing, J.A.Gershan, J.Weber, D.Tlomak, C.McOlash Sabatos-Peyton,. Combined immune checkpoint protein blockade and low dose whole body irradiation as immunotherapy for myeloma. J Immunother Cancer. 2015;3:2.
77. J.D.Wolchok, H.Kluger, M.K.Callahan, M.A.Postow, N.A.Rizvi, A.M.Lesokhin,. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;362:122–33.
78. J.D.Wolchok, A.Hoos, S.O’Day, J.S.Weber, O.Hamid, C.Lebbé,. Guidelines for the evaluation of immune therapy activity in solid tumors:immune-related response criteria. Clin Cancer Res. 2009;15:7412–20.