PD-L1 checkpoint blockade prevents immune dysfunction and leukemia development in a mouse model of chronic lymphocytic leukemia

Schreiber, 2011, Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion., Science, 331, 1565, 10.1126/science.1203486 Pardoll, 2012, The blockade of immune checkpoints in cancer immunotherapy., Nat Rev Cancer, 12, 252, 10.1038/nrc3239 Greaves, 2013, The role of B7 family molecules in hematologic malignancy., Blood, 121, 734, 10.1182/blood-2012-10-385591 Wherry, 2011, T cell exhaustion., Nat Immunol, 12, 492, 10.1038/ni.2035 Burkhardt, 2013, Autologous CLL cell vaccination early after transplant induces leukemia-specific T cells., J Clin Invest, 123, 3756, 10.1172/JCI69098 Riches, 2013, T cells from CLL patients exhibit features of T-cell exhaustion but retain capacity for cytokine production., Blood, 121, 1612, 10.1182/blood-2012-09-457531 Rezvany, 2003, Leukemia-associated monoclonal and oligoclonal TCR-BV use in patients with B-cell chronic lymphocytic leukemia., Blood, 101, 1063, 10.1182/blood-2002-03-0746 Riches, 2013, Understanding the immunodeficiency in chronic lymphocytic leukemia: potential clinical implications., Hematol Oncol Clin North Am, 27, 207, 10.1016/j.hoc.2013.01.003 Ramsay, 2008, Chronic lymphocytic leukemia T cells show impaired immunological synapse formation that can be reversed with an immunomodulating drug., J Clin Invest, 118, 2427 Ramsay, 2012, Multiple inhibitory ligands induce impaired T-cell immunologic synapse function in chronic lymphocytic leukemia that can be blocked with lenalidomide: establishing a reversible immune evasion mechanism in human cancer., Blood, 120, 1412, 10.1182/blood-2012-02-411678 Brusa, 2013, The PD-1/PD-L1 axis contributes to T-cell dysfunction in chronic lymphocytic leukemia., Haematologica, 98, 953, 10.3324/haematol.2012.077537 te Raa, 2014, CMV-specific CD8+ T-cell function is not impaired in chronic lymphocytic leukemia., Blood, 123, 717, 10.1182/blood-2013-08-518183 Jitschin, 2014, CLL-cells induce IDOhi CD14+HLA-DRlo myeloid-derived suppressor cells that inhibit T-cell responses and promote TRegs., Blood, 124, 750, 10.1182/blood-2013-12-546416 Bichi, 2002, Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression., Proc Natl Acad Sci USA, 99, 6955, 10.1073/pnas.102181599 Gorgun, 2009, E(μ)-TCL1 mice represent a model for immunotherapeutic reversal of chronic lymphocytic leukemia-induced T-cell dysfunction., Proc Natl Acad Sci USA, 106, 6250, 10.1073/pnas.0901166106 Hofbauer, 2011, Development of CLL in the TCL1 transgenic mouse model is associated with severe skewing of the T-cell compartment homologous to human CLL., Leukemia, 25, 1452, 10.1038/leu.2011.111 McDermott, 2013, PD-1 as a potential target in cancer therapy., Cancer Med, 2, 662, 10.1002/cam4.106 Ansell, 2015, PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma., N Engl J Med, 372, 311, 10.1056/NEJMoa1411087 Zhang, 2009, PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model., Blood, 114, 1545, 10.1182/blood-2009-03-206672 Sakuishi, 2010, Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity., J Exp Med, 207, 2187, 10.1084/jem.20100643 Deng, 2014, Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice., J Clin Invest, 124, 687, 10.1172/JCI67313 Paterson, 2011, The programmed death-1 ligand 1:B7-1 pathway restrains diabetogenic effector T cells in vivo., J Immunol, 187, 1097, 10.4049/jimmunol.1003496 Burger, 2000, Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1., Blood, 96, 2655, 10.1182/blood.V96.8.2655 Swirski, 2009, Identification of splenic reservoir monocytes and their deployment to inflammatory sites., Science, 325, 612, 10.1126/science.1175202 Maffei, 2013, The monocytic population in chronic lymphocytic leukemia shows altered composition and deregulation of genes involved in phagocytosis and inflammation., Haematologica, 98, 1115, 10.3324/haematol.2012.073080 Ziegler-Heitbrock, 2010, Nomenclature of monocytes and dendritic cells in blood., Blood, 116, e74, 10.1182/blood-2010-02-258558 Yrlid, 2006, Relationships between distinct blood monocyte subsets and migrating intestinal lymph dendritic cells in vivo under steady-state conditions., J Immunol, 176, 4155, 10.4049/jimmunol.176.7.4155 Arnold, 2007, Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis., J Exp Med, 204, 1057, 10.1084/jem.20070075 Herishanu, 2013, Biology of chronic lymphocytic leukemia in different microenvironments: clinical and therapeutic implications., Hematol Oncol Clin North Am, 27, 173, 10.1016/j.hoc.2013.01.002 Loke, 2003, PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells., Proc Natl Acad Sci U S A, 100, 5336, 10.1073/pnas.0931259100 Wintterle, 2003, Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis., Cancer Res, 63, 7462 Chen, 2007, B7-H1 up-regulation on myeloid dendritic cells significantly suppresses T cell immune function in patients with chronic hepatitis B., J Immunol, 178, 6634, 10.4049/jimmunol.178.10.6634 Görgün, 2005, Chronic lymphocytic leukemia cells induce changes in gene expression of CD4 and CD8 T cells., J Clin Invest, 115, 1797, 10.1172/JCI24176 Curiel, 2003, Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity., Nat Med, 9, 562, 10.1038/nm863 Wilcox, 2009, B7-H1 (PD-L1, CD274) suppresses host immunity in T-cell lymphoproliferative disorders., Blood, 114, 2149, 10.1182/blood-2009-04-216671 Spranger, 2014, 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, 3, 10.1186/2051-1426-2-3 Yu, 2012, Simultaneous inhibition of two regulatory T-cell subsets enhanced Interleukin-15 efficacy in a prostate tumor model., Proc Natl Acad Sci USA, 109, 6187, 10.1073/pnas.1203479109 Wainwright, 2014, Durable therapeutic efficacy utilizing combinatorial blockade against IDO, CTLA-4, and PD-L1 in mice with brain tumors., Clin Cancer Res, 20, 5290, 10.1158/1078-0432.CCR-14-0514 Motz, 2013, Deciphering and reversing tumor immune suppression., Immunity, 39, 61, 10.1016/j.immuni.2013.07.005 Berger, 2008, 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, 14, 3044, 10.1158/1078-0432.CCR-07-4079 Westin, 2014, Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial., Lancet Oncol, 15, 69, 10.1016/S1470-2045(13)70551-5