Universal Chimeric Antigen Receptors for Multiplexed and Logical Control of T Cell Responses

Cell - Tập 173 - Trang 1426-1438.e11 - 2018
Jang Hwan Cho1,2, James J. Collins3,4,5,6,7,8, Wilson W. Wong1,2
1Department of Biomedical Engineering, Boston University, Boston, MA, 02215, USA
2Biological Design Center, Boston University, Boston, MA 02215, USA
3Synthetic Biology Center, MIT, Cambridge, MA 02139, USA
4Institute for Medical Engineering and Science, MIT, Cambridge, MA 02139, USA
5Department of Biological Engineering, MIT, Cambridge, MA 02139, USA
6Harvard-MIT Program in Health Sciences and Technology, Cambridge, MA 02139, USA
7Broad Institute of MIT and Harvard, 415 Main Street, Cambridge, MA, 02142, USA
8Wyss Institute for Biologically Inspired Engineering, Harvard University, 3 Blackfan Circle, Boston, MA 02115, USA

Tài liệu tham khảo

Bonifant, 2016, Toxicity and management in CAR T-cell therapy, Mol. Ther. Oncolytics, 3, 16011, 10.1038/mto.2016.11 Brentjens, 2011, Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias, Blood, 118, 4817, 10.1182/blood-2011-04-348540 Brentjens, 2013, CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia, Sci. Transl. Med., 5, 177ra38, 10.1126/scitranslmed.3005930 Brudno, 2016, Toxicities of chimeric antigen receptor T cells: recognition and management, Blood, 127, 3321, 10.1182/blood-2016-04-703751 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 Carter, 2001, Improving the efficacy of antibody-based cancer therapies, Nat. Rev. Cancer, 1, 118, 10.1038/35101072 Caruso, 2015, Tuning sensitivity of CAR to EGFR density limits recognition of normal tissue while maintaining potent antitumor activity, Cancer Res., 75, 3505, 10.1158/0008-5472.CAN-15-0139 Chen, 2013, Molecular mechanisms of T cell co-stimulation and co-inhibition, Nat. Rev. Immunol., 13, 227, 10.1038/nri3405 Chmielewski, 2004, T cell activation by antibody-like immunoreceptors: increase in affinity of the single-chain fragment domain above threshold does not increase T cell activation against antigen-positive target cells but decreases selectivity, J. Immunol., 173, 7647, 10.4049/jimmunol.173.12.7647 Davila, 2014, Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia, Sci. Transl. Med., 6, 224ra25, 10.1126/scitranslmed.3008226 Di Stasi, 2011, Inducible apoptosis as a safety switch for adoptive cell therapy, N. Engl. J. Med., 365, 1673, 10.1056/NEJMoa1106152 Fry, 2018, CD22-targeted CAR T cells induce remission in B-ALL that is naive or resistant to CD19-targeted CAR immunotherapy, Nat. Med., 24, 20, 10.1038/nm.4441 Fu, 2010, A simple and sensitive method for measuring tumor-specific T cell cytotoxicity, PLoS ONE, 5, e11867, 10.1371/journal.pone.0011867 Geller, 2013, Intraperitoneal delivery of human natural killer cells for treatment of ovarian cancer in a mouse xenograft model, Cytotherapy, 15, 1297, 10.1016/j.jcyt.2013.05.022 Glienke, 2015, Advantages and applications of CAR-expressing natural killer cells, Front. Pharmacol., 6, 21, 10.3389/fphar.2015.00021 Golubovskaya, 2016, Different Subsets of T Cells, Memory, Effector Functions, and CAR-T Immunotherapy, Cancers (Basel), 8, 10.3390/cancers8030036 Gould, 2005, Protective and therapeutic capacity of human single-chain Fv-Fc fusion proteins against West Nile virus, J. Virol., 79, 14606, 10.1128/JVI.79.23.14606-14613.2005 Grada, 2013, TanCAR: A Novel Bispecific Chimeric Antigen Receptor for Cancer Immunotherapy, Mol. Ther. Nucleic Acids, 2, e105, 10.1038/mtna.2013.32 Greenwald, 2005, The B7 family revisited, Annu. Rev. Immunol., 23, 515, 10.1146/annurev.immunol.23.021704.115611 Grupp, 2013, Chimeric antigen receptor-modified T cells for acute lymphoid leukemia, N. Engl. J. Med., 368, 1509, 10.1056/NEJMoa1215134 Haso, 2013, Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia, Blood, 121, 1165, 10.1182/blood-2012-06-438002 Hegde, 2013, Combinational targeting offsets antigen escape and enhances effector functions of adoptively transferred T cells in glioblastoma, Mol. Ther., 21, 2087, 10.1038/mt.2013.185 Hombach, 2006, Human CD4+ T cells lyse target cells via granzyme/perforin upon circumvention of MHC class II restriction by an antibody-like immunoreceptor, J. Immunol., 177, 5668, 10.4049/jimmunol.177.8.5668 Howland, 2000, The roles of CD28 and CD40 ligand in T cell activation and tolerance, J. Immunol., 164, 4465, 10.4049/jimmunol.164.9.4465 Hudecek, 2015, The nonsignaling extracellular spacer domain of chimeric antigen receptors is decisive for in vivo antitumor activity, Cancer Immunol. Res., 3, 125, 10.1158/2326-6066.CIR-14-0127 Kane, 2001, Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-gamma but not TH2 cytokines, Nat. Immunol., 2, 37, 10.1038/83144 Karin, 1997, AP-1 function and regulation, Curr. Opin. Cell Biol., 9, 240, 10.1016/S0955-0674(97)80068-3 Kawalekar, 2016, Distinct Signaling of Coreceptors Regulates Specific Metabolism Pathways and Impacts Memory Development in CAR T Cells, Immunity, 44, 380, 10.1016/j.immuni.2016.01.021 Kimchi-Sarfaty, 2013, Building better drugs: developing and regulating engineered therapeutic proteins, Trends Pharmacol. Sci., 34, 534, 10.1016/j.tips.2013.08.005 Klingemann, 2014, Are natural killer cells superior CAR drivers?, OncoImmunology, 3, e28147, 10.4161/onci.28147 Kloss, 2013, Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells, Nat. Biotechnol., 31, 71, 10.1038/nbt.2459 Kochenderfer, 2012, B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells, Blood, 119, 2709, 10.1182/blood-2011-10-384388 Kontermann, 2011, Strategies for extended serum half-life of protein therapeutics, Curr. Opin. Biotechnol., 22, 868, 10.1016/j.copbio.2011.06.012 Kudo, 2014, T lymphocytes expressing a CD16 signaling receptor exert antibody-dependent cancer cell killing, Cancer Res., 74, 93, 10.1158/0008-5472.CAN-13-1365 Lanitis, 2013, Chimeric antigen receptor T Cells with dissociated signaling domains exhibit focused antitumor activity with reduced potential for toxicity in vivo, Cancer Immunol. Res., 1, 43, 10.1158/2326-6066.CIR-13-0008 Lee, 2002, Intraperitoneal gene delivery mediated by a novel cationic liposome in a peritoneal disseminated ovarian cancer model, Gene Ther., 9, 859, 10.1038/sj.gt.3301704 Lengyel, 2014, Epithelial ovarian cancer experimental models, Oncogene, 33, 3619, 10.1038/onc.2013.321 Liu, 2015, Affinity-tuned ErbB2 or EGFR chimeric antigen receptor T cells exhibit an increased therapeutic index against tumors in mice, Cancer Res., 75, 3596, 10.1158/0008-5472.CAN-15-0159 Lucas, 1995, Naive CD28-deficient T cells can initiate but not sustain an in vitro antigen-specific immune response, J. Immunol., 154, 5757, 10.4049/jimmunol.154.11.5757 Luckheeram, 2012, CD4+T cells: differentiation and functions, Clin. Dev. Immunol., 2012, 925135, 10.1155/2012/925135 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 MacDonald, 2016, Alloantigen-specific regulatory T cells generated with a chimeric antigen receptor, J. Clin. Invest., 126, 1413, 10.1172/JCI82771 Maude, 2014, Chimeric antigen receptor T cells for sustained remissions in leukemia, N. Engl. J. Med., 371, 1507, 10.1056/NEJMoa1407222 Maude, 2014, Managing cytokine release syndrome associated with novel T cell-engaging therapies, Cancer J., 20, 119, 10.1097/PPO.0000000000000035 Morgan, 2010, Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2, Mol. Ther., 18, 843, 10.1038/mt.2010.24 Perna, 2016, Myeloid leukemia switch as immune escape from CD19 chimeric antigen receptor (CAR) therapy, Transl. Cancer Res., 5, S221, 10.21037/tcr.2016.08.15 Reinke, 2010, A synthetic coiled-coil interactome provides heterospecific modules for molecular engineering, J. Am. Chem. Soc., 132, 6025, 10.1021/ja907617a 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 Roybal, 2016, Precision Tumor Recognition by T Cells With Combinatorial Antigen-Sensing Circuits, Cell, 164, 770, 10.1016/j.cell.2016.01.011 Ruella, 2016, Dual CD19 and CD123 targeting prevents antigen-loss relapses after CD19-directed immunotherapies, J. Clin. Invest., 126, 3814, 10.1172/JCI87366 Sadelain, 2017, Therapeutic T cell engineering, Nature, 545, 423, 10.1038/nature22395 Scholler, 2012, Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells, Sci. Transl. Med., 4, 132ra53, 10.1126/scitranslmed.3003761 Scott, 2012, Antibody therapy of cancer, Nat. Rev. Cancer, 12, 278, 10.1038/nrc3236 Shaw, 2004, Characterization of intraperitoneal, orthotopic, and metastatic xenograft models of human ovarian cancer, Mol. Ther., 10, 1032, 10.1016/j.ymthe.2004.08.013 Skapenko, 2001, Antigen-independent Th2 cell differentiation by stimulation of CD28: regulation via IL-4 gene expression and mitogen-activated protein kinase activation, J. Immunol., 166, 4283, 10.4049/jimmunol.166.7.4283 Strohl, 2015, Fusion Proteins for Half-Life Extension of Biologics as a Strategy to Make Biobetters, BioDrugs, 29, 215, 10.1007/s40259-015-0133-6 Szlachcic, 2011, Longer action means better drug: tuning up protein therapeutics, Biotechnol. Adv., 29, 436, 10.1016/j.biotechadv.2011.03.005 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 Thompson, 2012, SYNZIP protein interaction toolbox: in vitro and in vivo specifications of heterospecific coiled-coil interaction domains, ACS Synth. Biol., 1, 118, 10.1021/sb200015u 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 Urbanska, 2012, A universal strategy for adoptive immunotherapy of cancer through use of a novel T-cell antigen receptor, Cancer Res., 72, 1844, 10.1158/0008-5472.CAN-11-3890 Vandenberghe, 1993, Ligation of the CD5 or CD28 molecules on resting human T cells induces expression of the early activation antigen CD69 by a calcium- and tyrosine kinase-dependent mechanism, Immunology, 78, 210 Vignali, 2008, How regulatory T cells work. Nat. Rev, Immunol., 8, 523 Vivier, 2008, Functions of natural killer cells, Nat. Immunol., 9, 503, 10.1038/ni1582 Wu, 2015, Remote control of therapeutic T cells through a small molecule-gated chimeric receptor, Science, 350, aab4077, 10.1126/science.aab4077 Yoon, 2017, FVIII-specific human chimeric antigen receptor T-regulatory cells suppress T- and B-cell responses to FVIII, Blood, 129, 238, 10.1182/blood-2016-07-727834 Zah, 2016, T Cells Expressing CD19/CD20 Bispecific Chimeric Antigen Receptors Prevent Antigen Escape by Malignant B Cells, Cancer Immunol. Res., 4, 498, 10.1158/2326-6066.CIR-15-0231 Zhao, 2015, Structural Design of Engineered Costimulation Determines Tumor Rejection Kinetics and Persistence of CAR T Cells, Cancer Cell, 28, 415, 10.1016/j.ccell.2015.09.004 Zhu, 2007, CD137 stimulation delivers an antigen-independent growth signal for T lymphocytes with memory phenotype, Blood, 109, 4882, 10.1182/blood-2006-10-043463 Zhu, 2011, Cell surface signaling molecules in the control of immune responses: a tide model, Immunity, 34, 466, 10.1016/j.immuni.2011.04.008