Optogenetic control shows that kinetic proofreading regulates the activity of the T cell receptor

Elife. 2019 Apr 5:8:e42475. doi: 10.7554/eLife.42475.

Abstract

The immune system distinguishes between self and foreign antigens. The kinetic proofreading (KPR) model proposes that T cells discriminate self from foreign ligands by the different ligand binding half-lives to the T cell receptor (TCR). It is challenging to test KPR as the available experimental systems fall short of only altering the binding half-lives and keeping other parameters of the interaction unchanged. We engineered an optogenetic system using the plant photoreceptor phytochrome B (PhyB) as a ligand to selectively control the dynamics of ligand binding to the TCR by light. This opto-ligand-TCR system was combined with the unique property of PhyB to continuously cycle between the binding and non-binding states under red light, with the light intensity determining the cycling rate and thus the binding duration. Mathematical modeling of our experimental datasets showed that indeed the ligand-TCR interaction half-life is the decisive factor for activating downstream TCR signaling, substantiating KPR.

Keywords: A. thaliana; T cells; dynamics; human; immunology; inflammation; ligand-receptor; optogenetics; signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens / metabolism*
  • Humans
  • Jurkat Cells
  • Kinetics
  • Light
  • Models, Theoretical
  • Optogenetics / methods
  • Phytochrome B / metabolism*
  • Protein Binding
  • Receptors, Antigen, T-Cell / metabolism*
  • Signal Transduction*
  • T-Lymphocytes / immunology*

Substances

  • Antigens
  • Receptors, Antigen, T-Cell
  • Phytochrome B