Transient inhibition of interleukin 4 signaling by T cell receptor ligation

J Exp Med. 2000 Oct 16;192(8):1125-34. doi: 10.1084/jem.192.8.1125.

Abstract

Interleukin (IL)-4 and IL-12 together with T cell receptor (TCR) engagement are crucial for the differentiation of CD4(+) T cells into T helper (Th)2 or Th1 cells, respectively. Although IL-4 receptors (IL-4Rs) but not IL-12Rs are expressed on naive CD4(+) T cells, IL-4 has no apparent advantage over IL-12 in driving naive T cell differentiation when the cells are primed with both IL-4 and IL-12 in vitro. It was found that IL-4-induced phosphorylation of Janus kinases 1 and 3, IL-4R alpha, signal transducer and activator of transcription 6, and insulin receptor substrate 2 was strikingly but transiently inhibited by TCR ligation both in conventional and TCR transgenic T cells. TCR engagement also blocked the expression of an IL-4-inducible gene. Signals induced by other cytokines, including IL-2, IL-6, and interferon alpha, but not by insulin-like growth factor 1, were also blocked by TCR engagement. The capacity of various inhibitors to reverse TCR-mediated inhibition of IL-4 signaling suggested that activation of the Ras-mitogen-activated protein kinase pathway and of the calcineurin pathway contribute to desensitizing IL-4R. IL-4 responsiveness returned at about the time ( approximately 12 h) that IL-12-mediated signaling was first observed. Thus, through different mechanisms, neither IL-4R nor IL-12R has any clear advantage in polarizing cells; rather, the availability of cytokine is probably the limiting factor in this process.

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / cytology
  • CD4-Positive T-Lymphocytes / immunology*
  • Cell Differentiation
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / immunology
  • Interferon-alpha / pharmacology
  • Interleukin-12 / immunology
  • Interleukin-12 / pharmacology
  • Interleukin-2 / pharmacology
  • Interleukin-4 / immunology*
  • Interleukin-4 / pharmacology
  • Interleukin-6 / pharmacology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred Strains
  • Mice, Knockout
  • Mice, Transgenic
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Signal Transduction / immunology*
  • Spleen / immunology
  • Th1 Cells / cytology
  • Th1 Cells / immunology
  • Th2 Cells / cytology
  • Th2 Cells / immunology

Substances

  • DNA-Binding Proteins
  • Interferon-alpha
  • Interleukin-2
  • Interleukin-6
  • Rag2 protein, mouse
  • Receptors, Antigen, T-Cell
  • V(D)J recombination activating protein 2
  • Interleukin-12
  • Interleukin-4