Rapidly Switchable Universal CAR-T Cells for Treatment of CD123-Positive Leukemia

Molecular Therapy - Oncolytics - Tập 17 - Trang 408-420 - 2020
Simon Loff1, Josephine Dietrich2, Jan-Erik Meyer2, Julia Riewaldt2, Johannes Spehr2, Malte von Bonin3,4, Cordula Gründer1, Mridula Swayampakula1, Kristin Franke1, Anja Feldmann5, Michael Bachmann6,5,4,7, Gerhard Ehninger1,2, Armin Ehninger1,2, Marc Cartellieri1,2
1GEMoaB Monoclonals GmbH, 01307 Dresden, Germany
2Cellex Patient Treatment GmbH, 01307 Dresden, Germany
3Medical Clinic and Policlinic I, University Hospital “Carl Gustav Carus,” TU Dresden, 01307 Dresden, Germany
4German Cancer Consortium “Carl Gustav Carus,” TU Dresden, 01307 Dresden, Germany
5Helmholtz-Zentrum Dresden-Rossendorf, Institute of Radiopharmaceutical Cancer Research, 01328 Dresden, Germany
6University Cancer Center “Carl Gustav Carus,” TU Dresden, Tumor Immunology, 01307 Dresden, Germany
7National Center for Tumor Diseases, “Carl Gustav Carus,” TU Dresden, 01307 Dresden, Germany

Tài liệu tham khảo

Ferrara, 2006, Pathophysiology of graft-versus-host disease, Semin. Hematol., 43, 3, 10.1053/j.seminhematol.2005.09.001 Dykewicz, 2001, Summary of the Guidelines for Preventing Opportunistic Infections among Hematopoietic Stem Cell Transplant Recipients, Clin. Infect. Dis., 33, 139, 10.1086/321805 Coiffier, 2002, CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma, N. Engl. J. Med., 346, 235, 10.1056/NEJMoa011795 Jin, 2009, Monoclonal antibody-mediated targeting of CD123, IL-3 receptor α chain, eliminates human acute myeloid leukemic stem cells, Cell Stem Cell, 5, 31, 10.1016/j.stem.2009.04.018 Kantarjian, 2017, Blinatumomab versus chemotherapy for advanced acute lymphoblastic leukemia, N. Engl. J. Med., 376, 836, 10.1056/NEJMoa1609783 Neelapu, 2017, Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma, N. Engl. J. Med., 377, 2531, 10.1056/NEJMoa1707447 Park, 2018, Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia, N. Engl. J. Med., 378, 449, 10.1056/NEJMoa1709919 Schuster, 2017, Chimeric antigen receptor T cells in refractory B-cell lymphomas, N. Engl. J. Med., 377, 2545, 10.1056/NEJMoa1708566 Gardner, 2017, Intent-to-treat leukemia remission by CD19 CAR T cells of defined formulation and dose in children and young adults, Blood, 129, 3322, 10.1182/blood-2017-02-769208 Maude, 2014, Chimeric antigen receptor T cells for sustained remissions in leukemia, N. Engl. J. Med., 371, 1507, 10.1056/NEJMoa1407222 Bach, 2017, FDA Approval of tisagenlecleucel: promise and complexities of a $475 000 cancer drug, JAMA, 318, 1861, 10.1001/jama.2017.15218 Turtle, 2016, CD19 CAR-T cells of defined CD4+:CD8+ composition in adult B cell ALL patients, J. Clin. Invest., 126, 2123, 10.1172/JCI85309 Locke, 2017, Phase 1 results of ZUMA-1: a multicenter study of KTE-C19 anti-CD19 CAR T cell therapy in refractory aggressive lymphoma, Mol. Ther., 25, 285, 10.1016/j.ymthe.2016.10.020 Grupp, 2016, Analysis of a global registration trial of the efficacy and safety of CTL019 in pediatric and young adults with relapsed/refractory acute lymphoblastic leukemia (ALL), Blood, 128, 221, 10.1182/blood.V128.22.221.221 DeFrancesco, 2017, CAR-T’s forge ahead, despite Juno deaths, Nat. Biotechnol., 35, 6, 10.1038/nbt0117-6b Venkataraman, 2011, Characteristic CD103 and CD123 expression pattern defines hairy cell leukemia: usefulness of CD123 and CD103 in the diagnosis of mature B-cell lymphoproliferative disorders, Am. J. Clin. Pathol., 136, 625, 10.1309/AJCPKUM9J4IXCWEU Fromm, 2011, Flow cytometric analysis of CD123 is useful for immunophenotyping classical Hodgkin lymphoma, Cytometry B Clin. Cytom., 80, 91, 10.1002/cyto.b.20561 Chaperot, 2001, Identification of a leukemic counterpart of the plasmacytoid dendritic cells, Blood, 97, 3210, 10.1182/blood.V97.10.3210 Del Giudice, 2004, The diagnostic value of CD123 in B-cell disorders with hairy or villous lymphocytes, Haematologica, 89, 303 Ruella, 2016, Dual CD19 and CD123 targeting prevents antigen-loss relapses after CD19-directed immunotherapies, J. Clin. Invest., 126, 3814, 10.1172/JCI87366 Ehninger, 2014, Distribution and levels of cell surface expression of CD33 and CD123 in acute myeloid leukemia, Blood Cancer J., 4, e218, 10.1038/bcj.2014.39 Taussig, 2005, Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia, Blood, 106, 4086, 10.1182/blood-2005-03-1072 Sato, 1993, Expression and factor-dependent modulation of the interleukin-3 receptor subunits on human hematopoietic cells, Blood, 82, 752, 10.1182/blood.V82.3.752.752 Manz, 2002, Prospective isolation of human clonogenic common myeloid progenitors, Proc. Natl. Acad. Sci. USA, 99, 11872, 10.1073/pnas.172384399 Korpelainen, 1996, IL-3 receptor expression, regulation and function in cells of the vasculature, Immunol. Cell Biol., 74, 1, 10.1038/icb.1996.1 Brizzi, 1993, Interleukin 3 stimulates proliferation and triggers endothelial-leukocyte adhesion molecule 1 gene activation of human endothelial cells, J. Clin. Invest., 91, 2887, 10.1172/JCI116534 Gill, 2014, Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells, Blood, 123, 2343, 10.1182/blood-2013-09-529537 Mardiros, 2013, T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia, Blood, 122, 3138, 10.1182/blood-2012-12-474056 Al-Hussaini, 2016, Targeting CD123 in acute myeloid leukemia using a T-cell-directed dual-affinity retargeting platform, Blood, 127, 122, 10.1182/blood-2014-05-575704 Cartellieri, 2016, Switching CAR T cells on and off: a novel modular platform for retargeting of T cells to AML blasts, Blood Cancer J., 6, e458, 10.1038/bcj.2016.61 Bachmann, 2017, Retargeting of UniCAR T cells with an in vivo synthesized target module directed against CD19 positive tumor cells, Oncotarget, 9, 7487, 10.18632/oncotarget.23556 Albert, 2017, A novel nanobody-based target module for retargeting of T lymphocytes to EGFR-expressing cancer cells via the modular UniCAR platform, OncoImmunology, 6, e1287246, 10.1080/2162402X.2017.1287246 Feldmann, 2017, Retargeting of T lymphocytes to PSCA- or PSMA positive prostate cancer cells using the novel modular chimeric antigen receptor platform technology “UniCAR”, Oncotarget, 8, 31368, 10.18632/oncotarget.15572 Mitwasi, 2017, Development of novel target modules for retargeting of UniCAR T cells to GD2 positive tumor cells, Oncotarget, 8, 108584, 10.18632/oncotarget.21017 Pishali Bejestani, 2017, Characterization of a switchable chimeric antigen receptor platform in a pre-clinical solid tumor model, OncoImmunology, 6, e1342909, 10.1080/2162402X.2017.1342909 Mahnke, 2013, The who’s who of T-cell differentiation: human memory T-cell subsets, Eur. J. Immunol., 43, 2797, 10.1002/eji.201343751 Bonifant, 2016, CD123-engager T cells as a novel immunotherapeutic for acute myeloid leukemia, Mol. Ther., 24, 1615, 10.1038/mt.2016.116 Mardiros, 2015, T cells expressing CD123 chimeric antigen receptors for treatment of acute myeloid leukemia, Curr. Opin. Hematol., 22, 484, 10.1097/MOH.0000000000000190 Budde, 2017, Remissions of acute myeloid leukemia and blastic plasmacytoid dendritic cell neoplasm following treatment with CD123-specific CAR T cells: a first-in-human clinical trial, Blood, 130, 811, 10.1182/blood.V130.Suppl_1.811.811 Koristka, 2014, Flexible antigen-specific redirection of human regulatory T cells via a novel universal chimeric antigen receptor system, Blood, 124, 3494, 10.1182/blood.V124.21.3494.3494 Bonifant, 2016, Toxicity and management in CAR T-cell therapy, Mol. Ther. Oncolytics, 3, 16011, 10.1038/mto.2016.11 Bonnet, 1997, Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell, Nat. Med., 3, 730, 10.1038/nm0797-730 Lapidot, 1994, A cell initiating human acute myeloid leukaemia after transplantation into SCID mice, Nature, 367, 645, 10.1038/367645a0 Hope, 2004, Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity, Nat. Immunol., 5, 738, 10.1038/ni1080 Jordan, 2000, The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells, Leukemia, 14, 1777, 10.1038/sj.leu.2401903 Blair, 1998, Most acute myeloid leukemia progenitor cells with long-term proliferative ability in vitro and in vivo have the phenotype CD34+/CD71−/HLA-DR−, Blood, 92, 4325, 10.1182/blood.V92.11.4325 Venton, 2016, Aldehyde dehydrogenases inhibition eradicates leukemia stem cells while sparing normal progenitors, Blood Cancer J., 6, e469, 10.1038/bcj.2016.78 Crews, 2016, RNA splicing modulation selectively impairs leukemia stem cell maintenance in secondary human AML, Cell Stem Cell, 19, 599, 10.1016/j.stem.2016.08.003 Taussig, 2008, Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells, Blood, 112, 568, 10.1182/blood-2007-10-118331 Cox, 2004, Characterization of acute lymphoblastic leukemia progenitor cells, Blood, 104, 2919, 10.1182/blood-2004-03-0901 Tettamanti, 2013, Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor, Br. J. Haematol., 161, 389, 10.1111/bjh.12282 Pizzitola, 2014, Chimeric antigen receptors against CD33/CD123 antigens efficiently target primary acute myeloid leukemia cells in vivo, Leukemia, 28, 1596, 10.1038/leu.2014.62 Tamada, 2012, Redirecting gene-modified T cells toward various cancer types using tagged antibodies, Clin. Cancer Res., 18, 6436, 10.1158/1078-0432.CCR-12-1449 Rodgers, 2016, Switch-mediated activation and retargeting of CAR-T cells for B-cell malignancies, Proc. Natl. Acad. Sci. USA, 113, E459, 10.1073/pnas.1524155113 Ma, 2016, Versatile strategy for controlling the specificity and activity of engineered T cells, Proc. Natl. Acad. Sci. USA, 113, E450, 10.1073/pnas.1524193113 Chichili, 2015, A CD3×CD123 bispecific DART for redirecting host T cells to myelogenous leukemia: preclinical activity and safety in nonhuman primates, Sci. Transl. Med., 7, 289ra82, 10.1126/scitranslmed.aaa5693 Uy, 2019, Flotetuzumab, an investigational CD123 × CD3 bispecific Dart® protein, in salvage therapy for primary refractory and early relapsed acute myeloid leukemia (AML) patients, Blood, 134, 733, 10.1182/blood-2019-122073 Uy, 2018, Phase 1 cohort expansion of flotetuzumab, a CD123×CD3 bispecific DART® protein in patients with relapsed/refractory acute myeloid leukemia (AML), Blood, 132, 764, 10.1182/blood-2018-99-117085 Nijmeijer, 2009, Long-term culture of primary human lymphoblastic leukemia cells in the absence of serum or hematopoietic growth factors, Exp. Hematol., 37, 376, 10.1016/j.exphem.2008.11.002 Koristka, 2013, Retargeting of regulatory T cells to surface-inducible autoantigen La/SS-B, J. Autoimmun., 42, 105, 10.1016/j.jaut.2013.01.002 Cartellieri, 2014, A novel ex vivo isolation and expansion procedure for chimeric antigen receptor engrafted human T cells, PLoS ONE, 9, e93745, 10.1371/journal.pone.0093745 Meinke, 1996, Activation of different Stat5 isoforms contributes to cell-type-restricted signaling in response to interferons, Mol. Cell. Biol., 16, 6937, 10.1128/MCB.16.12.6937