Mechanism of IL-10-induced T cell inactivation in allergic inflammation and normal response to allergens

Int Arch Allergy Immunol. 2001 Jan-Mar;124(1-3):180-2. doi: 10.1159/000053704.

Abstract

Background: Induction of specific unresponsiveness (tolerance/anergy) in peripheral T cells and recovery by cytokines from the tissue microenvironment represent two key steps in specific immunotherapy (SIT) with whole allergen or antigenic T cell peptides.

Methods: Antigen-specific T cell responses and molecular mechanisms of T cell inactivation were investigated during conventional SIT, T cell epitope peptide immunotherapy and natural exposure to bee venom in allergic and hyperimmune individuals.

Results: T cell unresponsiveness, initiated by autocrine action of IL-10, is characterized by suppressed proliferative and cytokine responses. The unresponsive T cells can be reactivated by different cytokines that may mimic the microenvironmental cytokine influence. IL-10 initiates peripheral tolerance by blocking the CD28 costimulatory signal in T cells. Coprecipitation experiments reveal that upon stimulation CD28 and IL-10 receptor are physically associated in T cells. Accordingly, IL-10 binding to its receptor inhibits CD28 tyrosine phosphorylation, the initial step of the CD28 signaling pathway. This leads to inhibition of phosphatidylinositol 3-kinase p85 binding to CD28. IL-10 only affects T cells that receive a stimulation with low numbers of triggered T cell receptors and that require costimulatory signals by CD28.

Conclusion: These data demonstrate the pivotal role of autocrine IL-10 and the interaction of its receptor with CD28 in the induction of T cell tolerance as an immunoregulatory mechanism controlling antigen-specific T cell responses.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Allergens / immunology
  • Bee Venoms / immunology
  • CD28 Antigens / metabolism
  • Clonal Anergy
  • Cytokines / biosynthesis
  • Desensitization, Immunologic*
  • Humans
  • Hypersensitivity / immunology*
  • Hypersensitivity / therapy*
  • Immunoglobulin E / biosynthesis
  • Interleukin-10 / pharmacology*
  • Mast Cells / immunology
  • Phosphatidylinositol 3-Kinases / metabolism
  • Receptors, Interleukin / metabolism
  • Receptors, Interleukin-10
  • T-Lymphocytes / immunology

Substances

  • Allergens
  • Bee Venoms
  • CD28 Antigens
  • Cytokines
  • Receptors, Interleukin
  • Receptors, Interleukin-10
  • Interleukin-10
  • Immunoglobulin E
  • Phosphatidylinositol 3-Kinases