Distinct Signaling of Coreceptors Regulates Specific Metabolism Pathways and Impacts Memory Development in CAR T Cells

Basu, 2012, SILEC: a protocol for generating and using isotopically labeled coenzyme A mass spectrometry standards, Nat. Protoc., 7, 1, 10.1038/nprot.2011.421

Basu, 2011, Stable isotope labeling by essential nutrients in cell culture for preparation of labeled coenzyme A and its thioesters, Anal. Chem., 83, 1363, 10.1021/ac1027353

Beatty, 2014, Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce anti-tumor activity in solid malignancies, Cancer Immunol. Res., 2, 112, 10.1158/2326-6066.CIR-13-0170

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

Brocker, 2000, Chimeric Fv-zeta or Fv-epsilon receptors are not sufficient to induce activation or cytokine production in peripheral T cells, Blood, 96, 1999, 10.1182/blood.V96.5.1999

Carpenito, 2009, Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains, Proc. Natl. Acad. Sci. USA, 106, 3360, 10.1073/pnas.0813101106

Dang, 2011, Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1, Cell, 146, 772, 10.1016/j.cell.2011.07.033

Dotti, 2014, Design and development of therapies using chimeric antigen receptor-expressing T cells, Immunol. Rev., 257, 107, 10.1111/imr.12131

Düvel, 2010, Activation of a metabolic gene regulatory network downstream of mTOR complex 1, Mol. Cell, 39, 171, 10.1016/j.molcel.2010.06.022

Eshhar, 1993, Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors, Proc. Natl. Acad. Sci. USA, 90, 720, 10.1073/pnas.90.2.720

Ferrick, 2008, Advances in measuring cellular bioenergetics using extracellular flux, Drug Discov. Today, 13, 268, 10.1016/j.drudis.2007.12.008

Finlay, 2012, PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8+ T cells, J. Exp. Med., 209, 2441, 10.1084/jem.20112607

Frauwirth, 2002, The CD28 signaling pathway regulates glucose metabolism, Immunity, 16, 769, 10.1016/S1074-7613(02)00323-0

Grupp, 2013, Chimeric antigen receptor-modified T cells for acute lymphoid leukemia, N. Engl. J. Med., 368, 1509, 10.1056/NEJMoa1215134

Guedan, 2014, ICOS-based chimeric antigen receptors program bipolar TH17/TH1 cells, Blood, 124, 1070, 10.1182/blood-2013-10-535245

Hara, 1986, Human T cell activation. III. Rapid induction of a phosphorylated 28 kD/32 kD disulfide-linked early activation antigen (EA 1) by 12-o-tetradecanoyl phorbol-13-acetate, mitogens, and antigens, J. Exp. Med., 164, 1988, 10.1084/jem.164.6.1988

Hassan, 2002, Antitumor activity of SS(dsFv)PE38 and SS1(dsFv)PE38, recombinant antimesothelin immunotoxins against human gynecologic cancers grown in organotypic culture in vitro, Clin. Cancer Res., 8, 3520

June, 2015, Adoptive cellular therapy: a race to the finish line, Sci. Transl. Med., 7, 280ps7, 10.1126/scitranslmed.aaa3643

Kalos, 2013, Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology, Immunity, 39, 49, 10.1016/j.immuni.2013.07.002

Kalos, 2011, T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia, Sci. Transl. Med., 3, 95ra73, 10.1126/scitranslmed.3002842

Kershaw, 2006, A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer, Clin. Cancer Res., 12, 6106, 10.1158/1078-0432.CCR-06-1183

Kochenderfer, 2009, Construction and preclinical evaluation of an anti-CD19 chimeric antigen receptor, J. Immunother., 32, 689, 10.1097/CJI.0b013e3181ac6138

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

Ku, 2000, Control of homeostasis of CD8+ memory T cells by opposing cytokines, Science, 288, 675, 10.1126/science.288.5466.675

Kuwana, 1987, Expression of chimeric receptor composed of immunoglobulin-derived V regions and T-cell receptor-derived C regions, Biochem. Biophys. Res. Commun., 149, 960, 10.1016/0006-291X(87)90502-X

Lamers, 2006, Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience, J. Clin. Oncol., 24, e20, 10.1200/JCO.2006.05.9964

Lee, 2015, T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial, Lancet, 385, 517, 10.1016/S0140-6736(14)61403-3

Liao, 2013, Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy, Immunity, 38, 13, 10.1016/j.immuni.2013.01.004

Long, 2015, 4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors, Nat. Med., 21, 581, 10.1038/nm.3838

MacIver, 2013, Metabolic regulation of T lymphocytes, Annu. Rev. Immunol., 31, 259, 10.1146/annurev-immunol-032712-095956

Martinez-Forero, 2013, T cell costimulation with anti-CD137 monoclonal antibodies is mediated by K63-polyubiquitin-dependent signals from endosomes, J. Immunol., 190, 6694, 10.4049/jimmunol.1203010

Maude, 2014, Chimeric antigen receptor T cells for sustained remissions in leukemia, N. Engl. J. Med., 371, 1507, 10.1056/NEJMoa1407222

Maus, 2013, T Cells Expressing Chimeric Antigen Receptors Can Cause Anaphylaxis in Humans, Cancer Immunol. Res., 1, 26, 10.1158/2326-6066.CIR-13-0006

Maus, 2014, Adoptive immunotherapy for cancer or viruses, Annu. Rev. Immunol., 32, 189, 10.1146/annurev-immunol-032713-120136

Milone, 2009, Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo, Mol. Ther., 17, 1453, 10.1038/mt.2009.83

Mookerjee, 2010, Mitochondrial uncoupling and lifespan, Mech. Ageing Dev., 131, 463, 10.1016/j.mad.2010.03.010

Nicholls, 2009, Spare respiratory capacity, oxidative stress and excitotoxicity, Biochem. Soc. Trans., 37, 1385, 10.1042/BST0371385

Nicholson, 1997, Construction and characterisation of a functional CD19 specific single chain Fv fragment for immunotherapy of B lineage leukaemia and lymphoma, Mol. Immunol., 34, 1157, 10.1016/S0161-5890(97)00144-2

Pearce, 2013, Metabolic pathways in immune cell activation and quiescence, Immunity, 38, 633, 10.1016/j.immuni.2013.04.005

Pearce, 2009, Enhancing CD8 T-cell memory by modulating fatty acid metabolism, Nature, 460, 103, 10.1038/nature08097

Pipkin, 2010, Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells, Immunity, 32, 79, 10.1016/j.immuni.2009.11.012

Porter, 2015, Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia, Sci. Transl. Med., 7, 303ra139, 10.1126/scitranslmed.aac5415

Sabbagh, 2008, ERK-dependent Bim modulation downstream of the 4-1BB-TRAF1 signaling axis is a critical mediator of CD8 T cell survival in vivo, J. Immunol., 180, 8093, 10.4049/jimmunol.180.12.8093

Sadelain, 2013, The basic principles of chimeric antigen receptor design, Cancer Discov., 3, 388, 10.1158/2159-8290.CD-12-0548

Schluns, 2003, Cytokine control of memory T-cell development and survival, Nat. Rev. Immunol., 3, 269, 10.1038/nri1052

van der Windt, 2012, Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development, Immunity, 36, 68, 10.1016/j.immuni.2011.12.007

van der Windt, 2013, CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability, Proc. Natl. Acad. Sci. USA, 110, 14336, 10.1073/pnas.1221740110

Wang, 2012, Metabolic checkpoints in activated T cells, Nat. Immunol., 13, 907, 10.1038/ni.2386

Worth, 2014, Inhibition of neuronal cell mitochondrial complex I with rotenone increases lipid β-oxidation, supporting acetyl-coenzyme A levels, J. Biol. Chem., 289, 26895, 10.1074/jbc.M114.591354

Yadava, 2007, Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone, J. Neurosci., 27, 7310, 10.1523/JNEUROSCI.0212-07.2007

Zhao, 2010, Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor, Cancer Res., 70, 9053, 10.1158/0008-5472.CAN-10-2880