T cell receptor binding kinetics required for T cell activation depend on the density of cognate ligand on the antigen-presenting cell

Proc Natl Acad Sci U S A. 2005 Mar 29;102(13):4824-9. doi: 10.1073/pnas.0500922102. Epub 2005 Mar 16.

Abstract

CD8(+) T cells recognize peptides of eight to nine amino acid residues long in the context of MHC class I molecules on the surface of antigen-presenting cells (APCs). This recognition event is highly sensitive, as evidenced by the fact that T cells can be activated by cognate peptide/MHC complex (pMHC) at extremely low densities (1-50 molecules). High sensitivity is particularly valuable for detection of antigens at low density, such as those derived from tumor cells and intracellular pathogens, which can down-modulate cognate pMHCs from the surface of APCs to evade recognition by the adaptive immune system. T cell activation is only triggered in response to interactions between the T cell receptor (TCR) and the pMHC ligand that reach a specific half-life threshold. However, interactions with excessively long half-lives result in impaired T cell activation. Thus, efficient T cell activation by pMHC on the surface of APCs requires an optimal dwell time of TCR-pMHC interaction. Here, we show that, although this is a requirement at low cognate pMHC density on the APC surface, at high epitope density there is no impairment of T cell activation by extended TCR-pMHC dwell times. This observation was predicted by mathematical simulations for T cell activation by pMHC at different densities and supported by experiments performed on APCs selected for varied expression of cognate pMHC. According to these results, effective T cell activation depends on a complex interplay between inherent TCR-pMHC binding kinetics and the epitope density on the APC.

Publication types

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

MeSH terms

  • Antigen-Presenting Cells / metabolism*
  • Cells, Cultured
  • Epitopes, T-Lymphocyte / metabolism*
  • Flow Cytometry
  • H-2 Antigens / metabolism
  • Histocompatibility Antigens Class I / metabolism*
  • Humans
  • Hybridomas / immunology
  • Kinetics
  • Ligands
  • Lymphocyte Activation / physiology*
  • Models, Immunological*
  • Protein Binding
  • Receptors, Antigen, T-Cell / metabolism*

Substances

  • Epitopes, T-Lymphocyte
  • H-2 Antigens
  • H-2Kb protein, mouse
  • Histocompatibility Antigens Class I
  • Ligands
  • Receptors, Antigen, T-Cell