Therapeutic Targeting of Follicular T Cells with Chimeric Antigen Receptor-Expressing Natural Killer Cells

Crotty, 2011, Follicular helper CD4 T cells (TFH), Annu. Rev. Immunol., 29, 621, 10.1146/annurev-immunol-031210-101400 Vinuesa, 2016, Follicular Helper T Cells, Annu. Rev. Immunol., 34, 335, 10.1146/annurev-immunol-041015-055605 Victora, 2012, Germinal centers, Annu. Rev. Immunol., 30, 429, 10.1146/annurev-immunol-020711-075032 Tangye, 2013, The good, the bad and the ugly - TFH cells in human health and disease, Nat. Rev. Immunol., 13, 412, 10.1038/nri3447 Craft, 2012, Follicular helper T cells in immunity and systemic autoimmunity, Nat. Rev. Rheumatol., 8, 337, 10.1038/nrrheum.2012.58 Vinuesa, 2009, Dysregulation of germinal centres in autoimmune disease, Nat. Rev. Immunol., 9, 845, 10.1038/nri2637 Blanco, 2016, T follicular helper (Tfh) cells in lupus: activation and involvement in SLE pathogenesis, Eur. J. Immunol., 46, 281, 10.1002/eji.201545760 Choi, 2015, Circulating follicular helper-like T cells in systemic lupus erythematosus: association with disease activity, Arthritis Rheumatol., 67, 988, 10.1002/art.39020 Vinuesa, 2005, A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity, Nature, 435, 452, 10.1038/nature03555 Linterman, 2009, Follicular helper T cells are required for systemic autoimmunity, J. Exp. Med., 206, 561, 10.1084/jem.20081886 Kobayashi, 2017, Follicular helper T cells mediate IgE antibody response to airborne allergens, J. Allergy Clin. Immunol., 139, 300, 10.1016/j.jaci.2016.04.021 Ahearne, 2014, Follicular helper T-cells: expanding roles in T-cell lymphoma and targets for treatment, Br. J. Haematol., 166, 326, 10.1111/bjh.12941 Barrett, 2014, Chimeric antigen receptor therapy for cancer, Annu. Rev. Med., 65, 333, 10.1146/annurev-med-060512-150254 Guedan, 2018, Engineering and Design of Chimeric Antigen Receptors, Mol. Ther. Methods Clin. Dev., 12, 145, 10.1016/j.omtm.2018.12.009 Anwer, 2017, Donor origin CAR T cells: graft versus malignancy effect without GVHD, a systematic review, Immunotherapy, 9, 123, 10.2217/imt-2016-0127 Neelapu, 2018, Chimeric antigen receptor T-cell therapy - assessment and management of toxicities, Nat. Rev. Clin. Oncol., 15, 47, 10.1038/nrclinonc.2017.148 Daher, 2018, Next generation natural killer cells for cancer immunotherapy: the promise of genetic engineering, Curr. Opin. Immunol., 51, 146, 10.1016/j.coi.2018.03.013 Li, 2018, Human iPSC-Derived Natural Killer Cells Engineered with Chimeric Antigen Receptors Enhance Anti-tumor Activity, Cell Stem Cell, 23, 181, 10.1016/j.stem.2018.06.002 Liu, 2020, Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors, N. Engl. J. Med., 382, 545, 10.1056/NEJMoa1910607 Tang, 2018, First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia, Am. J. Cancer Res., 8, 1083 Siegler, 2018, Off-the-Shelf CAR-NK Cells for Cancer Immunotherapy, Cell Stem Cell, 23, 160, 10.1016/j.stem.2018.07.007 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 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 Butte, 2008, Interaction of human PD-L1 and B7-1, Mol. Immunol., 45, 3567, 10.1016/j.molimm.2008.05.014 Cheng, 2013, Structure and interactions of the human programmed cell death 1 receptor, J. Biol. Chem., 288, 11771, 10.1074/jbc.M112.448126 Klingemann, 2016, Natural Killer Cells for Immunotherapy - Advantages of the NK-92 Cell Line over Blood NK Cells, Front. Immunol., 7, 91, 10.3389/fimmu.2016.00091 March, 2010, Use of transfected Drosophila S2 cells to study NK cell activation, Methods Mol. Biol., 612, 67, 10.1007/978-1-60761-362-6_6 Herman, 1991, Identification of the staphylococcal enterotoxin A superantigen binding site in the beta 1 domain of the human histocompatibility antigen HLA-DR, Proc. Natl. Acad. Sci. USA, 88, 9954, 10.1073/pnas.88.22.9954 Gunawan, 2017, A Novel Human Systemic Lupus Erythematosus Model in Humanised Mice, Sci. Rep., 7, 16642, 10.1038/s41598-017-16999-7 Tsokos, 2016, New insights into the immunopathogenesis of systemic lupus erythematosus, Nat. Rev. Rheumatol., 12, 716, 10.1038/nrrheum.2016.186 Wu, 2011, Natural killer T cells in health and disease, Front. Biosci. (Schol. Ed.), 3, 236 Blanco, 2005, Increase in activated CD8+ T lymphocytes expressing perforin and granzyme B correlates with disease activity in patients with systemic lupus erythematosus, Arthritis Rheum., 52, 201, 10.1002/art.20745 Locci, 2013, Human circulating PD-1+CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses, Immunity, 39, 758, 10.1016/j.immuni.2013.08.031 Zhang, 2015, Circulating CXCR5+CD4+helper T cells in systemic lupus erythematosus patients share phenotypic properties with germinal center follicular helper T cells and promote antibody production, Lupus, 24, 909, 10.1177/0961203314567750 Linterman, 2011, Foxp3+ follicular regulatory T cells control the germinal center response, Nat. Med., 17, 975, 10.1038/nm.2425 Xie, 2019, Follicular regulatory T cells inhibit the development of granzyme B-expressing follicular helper T cells, JCI Insight, 4, 128076, 10.1172/jci.insight.128076 Essig, 2017, Roquin Suppresses the PI3K-mTOR Signaling Pathway to Inhibit T Helper Cell Differentiation and Conversion of Treg to Tfr Cells, Immunity, 47, 1067, 10.1016/j.immuni.2017.11.008 Sage, 2016, Suppression by TFR cells leads to durable and selective inhibition of B cell effector function, Nat. Immunol., 17, 1436, 10.1038/ni.3578 Clement, 2019, Follicular regulatory T cells control humoral and allergic immunity by restraining early B cell responses, Nat. Immunol., 20, 1360, 10.1038/s41590-019-0472-4 Yamazaki, 2002, Expression of programmed death 1 ligands by murine T cells and APC, J. Immunol., 169, 5538, 10.4049/jimmunol.169.10.5538 Curran, 2019, PD-1 immunobiology in systemic lupus erythematosus, J. Autoimmun., 97, 1, 10.1016/j.jaut.2018.10.025 Liu, 2006, Immune cell transcriptome datasets reveal novel leukocyte subset-specific genes and genes associated with allergic processes, J. Allergy Clin. Immunol., 118, 496, 10.1016/j.jaci.2006.04.040 Shi, 2011, A novel monoclonal antibody against human CD80 and its immune protection in a mouse lupus-like disease, Int. J. Immunopathol. Pharmacol., 24, 583, 10.1177/039463201102400304 Liarski, 2014, Cell distance mapping identifies functional T follicular helper cells in inflamed human renal tissue, Sci. Transl. Med., 6, 230ra46, 10.1126/scitranslmed.3008146 Rao, 2017, Pathologically expanded peripheral T helper cell subset drives B cells in rheumatoid arthritis, Nature, 542, 110, 10.1038/nature20810 Taylor, 2018, T follicular helper-like cells contribute to skin fibrosis, Sci. Transl. Med., 10, eaaf5307, 10.1126/scitranslmed.aaf5307 He, 2016, Follicular CXCR5- expressing CD8(+) T cells curtail chronic viral infection, Nature, 537, 412, 10.1038/nature19317 Huot, 2017, Natural killer cells migrate into and control simian immunodeficiency virus replication in lymph node follicles in African green monkeys, Nat. Med., 23, 1277, 10.1038/nm.4421 Ayala, 2017, CXCR5-Dependent Entry of CD8 T Cells into Rhesus Macaque B-Cell Follicles Achieved through T-Cell Engineering, J. Virol., 91, e02507-16, 10.1128/JVI.02507-16 Wunderlich, 2010, AML xenograft efficiency is significantly improved in NOD/SCID-IL2RG mice constitutively expressing human SCF, GM-CSF and IL-3, Leukemia, 24, 1785, 10.1038/leu.2010.158 Han, 2015, CAR-Engineered NK Cells Targeting Wild-Type EGFR and EGFRvIII Enhance Killing of Glioblastoma and Patient-Derived Glioblastoma Stem Cells, Sci. Rep., 5, 11483, 10.1038/srep11483 Somanchi, 2011, Expansion, purification, and functional assessment of human peripheral blood NK cells, J. Vis. Exp., 2540 Wunderlich, 2013, AML cells are differentially sensitive to chemotherapy treatment in a human xenograft model, Blood, 121, e90, 10.1182/blood-2012-10-464677