Induction of T cell anergy by low numbers of agonist ligands

J Immunol. 1999 Jun 1;162(11):6401-9.

Abstract

Engagement of TCR by its ligand, the MHC/peptide complex, causes T cell activation. T cells respond positively to stimulation with agonists, and are inhibited by antagonist MHC/peptide ligands. Failure to induce proper conformational changes in the TCR or fast TCR/MHC dissociation are the leading models proposed to explain anergy induction by antagonist ligands. In this study, we demonstrate that presentation of between 1 and 10 complexes of agonist/MHC II by unfixed APC induces T cell anergy that persists up to 7 days and has characteristics similar to anergy induced by antagonist ligand or TCR occupancy without costimulation. Furthermore, anergy-inducing doses of hemagglutinin 306-318 peptide led to the engagement of less than 1000 TCR/CD3 complexes. Thus, engagement of a subthreshold number of TCR by either a low density of agonist/MHC or a 2-3 orders of magnitude higher density of antagonist/MHC causes anergy. Moreover, we show that anergy induced by low agonist concentrations is inhibited in the presence of IL-2 or cyclosporin A, suggesting involvement of the calcineurin signaling pathway.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Clonal Anergy / drug effects
  • Clonal Anergy / immunology*
  • Clone Cells
  • Cyclosporine / pharmacology
  • Cytokines / biosynthesis
  • Dose-Response Relationship, Immunologic
  • Down-Regulation / immunology
  • HLA-DR1 Antigen / analysis
  • Hemagglutinin Glycoproteins, Influenza Virus
  • Hemagglutinins, Viral / analysis
  • Hemagglutinins, Viral / immunology
  • Hemagglutinins, Viral / pharmacology
  • Humans
  • Immunosuppressive Agents / pharmacology
  • Interleukin-2 / pharmacology
  • Ligands
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation / immunology
  • Macromolecular Substances
  • Orthomyxoviridae / immunology
  • Peptide Fragments / analysis
  • Peptide Fragments / immunology
  • Peptide Fragments / pharmacology
  • Receptors, Antigen, T-Cell / agonists*
  • Receptors, Antigen, T-Cell / antagonists & inhibitors
  • Receptors, Antigen, T-Cell / biosynthesis
  • Receptors, Antigen, T-Cell / metabolism*
  • Receptors, Interleukin-2 / biosynthesis
  • T-Lymphocytes / chemistry
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism*
  • Time Factors
  • Up-Regulation / immunology

Substances

  • Cytokines
  • HLA-DR1 Antigen
  • Hemagglutinin Glycoproteins, Influenza Virus
  • Hemagglutinins, Viral
  • Immunosuppressive Agents
  • Interleukin-2
  • Ligands
  • Macromolecular Substances
  • Peptide Fragments
  • Receptors, Antigen, T-Cell
  • Receptors, Interleukin-2
  • influenza hemagglutinin (306-318)
  • Cyclosporine