Phosphoenolpyruvate Is a Metabolic Checkpoint of Anti-tumor T Cell Responses

Cell. 2015 Sep 10;162(6):1217-28. doi: 10.1016/j.cell.2015.08.012. Epub 2015 Aug 27.

Abstract

Activated T cells engage aerobic glycolysis and anabolic metabolism for growth, proliferation, and effector functions. We propose that a glucose-poor tumor microenvironment limits aerobic glycolysis in tumor-infiltrating T cells, which suppresses tumoricidal effector functions. We discovered a new role for the glycolytic metabolite phosphoenolpyruvate (PEP) in sustaining T cell receptor-mediated Ca(2+)-NFAT signaling and effector functions by repressing sarco/ER Ca(2+)-ATPase (SERCA) activity. Tumor-specific CD4 and CD8 T cells could be metabolically reprogrammed by increasing PEP production through overexpression of phosphoenolpyruvate carboxykinase 1 (PCK1), which bolstered effector functions. Moreover, PCK1-overexpressing T cells restricted tumor growth and prolonged the survival of melanoma-bearing mice. This study uncovers new metabolic checkpoints for T cell activity and demonstrates that metabolic reprogramming of tumor-reactive T cells can enhance anti-tumor T cell responses, illuminating new forms of immunotherapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Calcium / metabolism
  • Endoplasmic Reticulum / metabolism
  • Glycolysis
  • Hexokinase / metabolism
  • Immunotherapy
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Melanoma / immunology*
  • Melanoma / therapy*
  • Mice
  • Monitoring, Immunologic*
  • NFATC Transcription Factors / metabolism
  • Phosphoenolpyruvate / metabolism*
  • Receptors, Antigen, T-Cell / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism
  • Signal Transduction
  • Transforming Growth Factor beta / immunology
  • Tumor Microenvironment*

Substances

  • NFATC Transcription Factors
  • Receptors, Antigen, T-Cell
  • Transforming Growth Factor beta
  • Phosphoenolpyruvate
  • Hexokinase
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Calcium

Associated data

  • SRA/SRP058700