T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription

J Exp Med. 2006 Mar 20;203(3):755-66. doi: 10.1084/jem.20052165. Epub 2006 Mar 6.

Abstract

T helper type 1 (Th1) development is facilitated by interrelated changes in key intracellular factors, particularly signal transducer and activator of transcription (STAT)4, T-bet, and GATA-3. Here we show that CD4+ cells from T-bet-/- mice are skewed toward Th2 differentiation by high endogenous GATA-3 levels but exhibit virtually normal Th1 differentiation provided that GATA-3 levels are regulated at an early stage by anti-interleukin (IL)-4 blockade of IL-4 receptor (R) signaling. In addition, under these conditions, Th1 cells from T-bet-/- mice manifest IFNG promotor accessibility as detected by histone acetylation and deoxyribonuclease I hypersensitivity. In related studies, we show that the negative effect of GATA-3 on Th1 differentiation in T-bet-/- cells arises from its ability to suppress STAT4 levels, because if this is prevented by a STAT4-expressing retrovirus, normal Th1 differentiation is observed. Finally, we show that retroviral T-bet expression in developing and established Th2 cells leads to down-regulation of GATA-3 levels. These findings lead to a model of T cell differentiation that holds that naive T cells tend toward Th2 differentiation through induction of GATA-3 and subsequent down-regulation of STAT4/IL-12Rbeta2 chain unless GATA-3 levels or function is regulated by T-bet. Thus, the principal function of T-bet in developing Th1 cells is to negatively regulate GATA-3 rather than to positively regulate the IFNG gene.

MeSH terms

  • Acetylation
  • Animals
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Cells, Cultured
  • Down-Regulation / genetics
  • Down-Regulation / immunology*
  • GATA3 Transcription Factor / genetics
  • GATA3 Transcription Factor / immunology*
  • GATA4 Transcription Factor / genetics
  • GATA4 Transcription Factor / immunology
  • Histones / genetics
  • Histones / immunology
  • Humans
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology*
  • Mice
  • Mice, Knockout
  • Protein Processing, Post-Translational / genetics
  • Protein Processing, Post-Translational / immunology
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin / immunology
  • Receptors, Interleukin-12
  • Retroviridae
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • T-Box Domain Proteins
  • Th1 Cells / immunology*
  • Th2 Cells / immunology
  • Transcription Factors / deficiency
  • Transcription Factors / immunology*
  • Transcription, Genetic / genetics
  • Transcription, Genetic / immunology
  • Transduction, Genetic / methods

Substances

  • GATA3 Transcription Factor
  • GATA4 Transcription Factor
  • Gata3 protein, mouse
  • Histones
  • Receptors, Interleukin
  • Receptors, Interleukin-12
  • T-Box Domain Proteins
  • T-box transcription factor TBX21
  • Transcription Factors
  • Interferon-gamma