Enhanced effector responses in activated CD8+ T cells deficient in diacylglycerol kinases

Cancer Res. 2013 Jun 15;73(12):3566-77. doi: 10.1158/0008-5472.CAN-12-3874. Epub 2013 Apr 10.

Abstract

Recent clinical trials have shown promise in the use of chimeric antigen receptor (CAR)-transduced T cells; however, augmentation of their activity may broaden their clinical use and improve their efficacy. We hypothesized that because CAR action requires proteins essential for T-cell receptor (TCR) signal transduction, deletion of negative regulators of these signaling pathways would enhance CAR signaling and effector T-cell function. We tested CAR activity and function in T cells that lacked one or both isoforms of diacylglycerol kinase (dgk) expressed highly in T cells, dgkα and dgkζ, enzymes that metabolize the second messenger diacylglycerol (DAG) and limit Ras/ERK activation. We found that primary murine T cells transduced with CARs specific for the human tumor antigen mesothelin showed greatly enhanced cytokine production and cytotoxicity when cocultured with a murine mesothelioma line that stably expresses mesothelin. In addition, we found that dgk-deficient CAR-transduced T cells were more effective in limiting the growth of implanted tumors, both concurrent with and after establishment of tumor. Consistent with our studies in mice, pharmacologic inhibition of dgks also augments function of primary human T cells transduced with CARs. These results suggest that deletion of negative regulators of TCR signaling enhances the activity and function of CAR-expressing T cells and identify dgks as potential targets for improving the clinical potential of CARs.

MeSH terms

  • Animals
  • Blotting, Western
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / transplantation
  • Cell Line, Tumor
  • Cells, Cultured
  • Diacylglycerol Kinase / genetics
  • Diacylglycerol Kinase / immunology*
  • Diacylglycerol Kinase / metabolism
  • Diglycerides / immunology
  • Diglycerides / metabolism
  • Flow Cytometry
  • GPI-Linked Proteins / immunology
  • HEK293 Cells
  • Humans
  • Immunotherapy, Adoptive
  • Isoenzymes / genetics
  • Isoenzymes / immunology
  • Isoenzymes / metabolism
  • Lymphocyte Activation / immunology*
  • Mesothelin
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms, Experimental / immunology
  • Neoplasms, Experimental / pathology
  • Neoplasms, Experimental / therapy
  • Receptors, Antigen, T-Cell / immunology*
  • Receptors, Antigen, T-Cell / metabolism
  • Signal Transduction / immunology

Substances

  • 1,2-diacylglycerol
  • Diglycerides
  • GPI-Linked Proteins
  • Isoenzymes
  • Msln protein, mouse
  • Receptors, Antigen, T-Cell
  • Diacylglycerol Kinase
  • Mesothelin