THEMIS-SHP1 Recruitment by 4-1BB Tunes LCK-Mediated Priming of Chimeric Antigen Receptor-Redirected T Cells

Cancer Cell. 2020 Feb 10;37(2):216-225.e6. doi: 10.1016/j.ccell.2019.12.014. Epub 2020 Jan 30.

Abstract

Chimeric antigen receptor (CAR) T cell costimulation mediated by CD28 and 4-1BB is essential for CAR-T cell-induced tumor regression. However, CD28 and 4-1BB differentially modulate kinetics, metabolism and persistence of CAR-T cells, and the mechanisms governing these differences are not fully understood. We found that LCK recruited into the synapse of CD28-encoding CAR by co-receptors causes antigen-independent CAR-CD3ζ phosphorylation and increased antigen-dependent T cell activation. In contrast, the synapse formed by 4-1BB-encoding CAR recruits the THEMIS-SHP1 phosphatase complex that attenuates CAR-CD3ζ phosphorylation. We further demonstrated that the CAR synapse can be engineered to recruit either LCK to enhance the kinetics of tumor killing of 4-1BB CAR-T cells or SHP1 to tune down cytokine release of CD28 CAR-T cells.

Keywords: 4-1BB; CAR-CD3ζ; CAR-Ts; CD28; chimeric antigen receptor; cytokine release syndrome (CRS); druggable engineering; kinase; phosphatase; phosphorylation; synapse.

Publication types

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

MeSH terms

  • Animals
  • CD28 Antigens / immunology
  • Cell Line, Tumor
  • Cytokines / metabolism
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Lymphocyte Activation / immunology
  • Mice, Transgenic
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / metabolism*
  • Receptors, Antigen, T-Cell / immunology
  • Receptors, Chimeric Antigen / metabolism*
  • T-Lymphocytes / immunology
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / metabolism

Substances

  • CD28 Antigens
  • Cytokines
  • Intercellular Signaling Peptides and Proteins
  • Intracellular Signaling Peptides and Proteins
  • Receptors, Antigen, T-Cell
  • Receptors, Chimeric Antigen
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • themis protein, mouse
  • thymocyte-expressed molecule involved in selection, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6