Neonatal exposure to antigen induces a defective CD40 ligand expression that undermines both IL-12 production by APC and IL-2 receptor up-regulation on splenic T cells and perpetuates IFN-gamma-dependent T cell anergy

J Immunol. 2001 May 1;166(9):5594-603. doi: 10.4049/jimmunol.166.9.5594.

Abstract

T cell deletion and/or inactivation were considered the leading mechanisms for neonatal tolerance. However, recent investigations have indicated that immunity develops at the neonatal stage but evolves to guide later T cell responses to display defective and/or biased effector functions. Although neonatal-induced T cell modulation provides a useful approach to suppress autoimmunity, the mechanism underlying the biased function of the T cells remains unclear. In prior studies, we found that exposure of newborn mice to Ig-PLP1, a chimera expressing the encephalitogenic proteolipid protein (PLP) sequence 139-151, induced deviated Th2 lymph node cells producing IL-4 instead of IL-2 and anergic splenic T cells that failed to proliferate or produce IFN-gamma yet secreted significant amounts of IL-2. However, if assisted with IFN-gamma or IL-12, these anergic splenic T cells regained full responsiveness. The consequence of such biased/defective T cells responses was protection of the mice against experimental allergic encephalomyelitis. In this study, investigations were performed to delineate the mechanism underlying the novel form of IFN-gamma-dependent splenic anergy. Our findings indicate that CD40 ligand expression on these splenic T cells is defective, leading to noneffective cooperation between T lymphocytes and APCs and a lack of IL-12 production. More striking, this cellular system revealed a requirement for IL-2R expression for CD40 ligand-initiated, IL-12-driven progression of T cells into IFN-gamma production.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn / immunology*
  • Antigen-Presenting Cells / immunology*
  • Antigen-Presenting Cells / metabolism
  • CD40 Antigens / immunology
  • CD40 Antigens / metabolism
  • CD40 Ligand / biosynthesis*
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Clonal Anergy* / genetics
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Female
  • Immune Sera / metabolism
  • Injections, Intraperitoneal
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / physiology*
  • Interleukin-12 / biosynthesis*
  • Lymphocyte Activation / genetics
  • Male
  • Mice
  • Mice, Inbred Strains
  • Myelin Proteolipid Protein / administration & dosage
  • Myelin Proteolipid Protein / genetics
  • Myelin Proteolipid Protein / immunology*
  • Peptide Fragments / administration & dosage
  • Peptide Fragments / genetics
  • Peptide Fragments / immunology*
  • Receptors, Interleukin-2 / biosynthesis*
  • Receptors, Interleukin-2 / deficiency
  • Receptors, Interleukin-2 / physiology
  • Recombinant Fusion Proteins / administration & dosage
  • Recombinant Fusion Proteins / immunology
  • Spleen / cytology
  • Spleen / immunology
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism
  • Time Factors
  • Up-Regulation / genetics
  • Up-Regulation / immunology

Substances

  • CD40 Antigens
  • Immune Sera
  • Myelin Proteolipid Protein
  • Peptide Fragments
  • Receptors, Interleukin-2
  • Recombinant Fusion Proteins
  • myelin proteolipid protein (139-151)
  • CD40 Ligand
  • Interleukin-12
  • Interferon-gamma