Requirement of CD28 signaling in homeostasis/survival of TGF-beta converted CD4+CD25+ Tregs from thymic CD4+CD25- single positive T cells

Transplantation. 2006 Oct 15;82(7):953-64. doi: 10.1097/01.tp.0000232330.46688.37.

Abstract

Background: The thymus is a major organ that generates "natural" CD4+CD25+ T regulatory cells (Tregs). However, the detailed pathway(s) by which Tregs are developed remain a mystery. CD28-/- mice have profound decrease in Tregs, but the underlying molecular events remain largely undefined.

Methods: CD4+CD25+ thymocytes from wildtype and CD28-/- mice were cultured with T-cell receptor (TCR) and transforming growth factor (TGF)-beta stimulation to generate CD25+ Tregs and their phenotype and function were studied in vitro and in vivo.

Results: TGF-beta induced Foxp3 expression in thymic CD4+CD25+ cells and converted them to CD25+ Tregs. The converted Tregs expressed high levels of CD25, whereas the non-suppressive CD4+ T cells from the control cultures expressed CD25(low). CD28-/- thymic CD4+CD25+ cells showed transit lower levels of Foxp3 upon TCR and TGF-beta stimulation early in culture, but the defect in Foxp3 expression was restored to normal levels after 60-72 hr. Consequently, TGF-beta converted CD28-/- CD25+ cells to CD25+ Tregs that were indistinguishable from those of the wildtype mice. However, the total number of TGF-beta converted CD28-/- Tregs was significantly lower than that of wildtype mice. In vivo, TGF-beta converted CD28-/- CD25+ Tregs were less viable than those from the wildtype mice. Importantly, TGF-beta induced alloantigen specific CD4+CD25+ Tregs from thymic CD25-SP cells which also required CD28 to maintain their survival.

Conclusions: TGF-beta and TCR co-stimulation converts thymic CD4+CD25+ T cells into CD4+CD25+ Tregs by inducing Foxp3, and the contribution of CD28 stimulation to this process is mainly through maintaining survival of the induced Tregs.

MeSH terms

  • Adoptive Transfer
  • Animals
  • CD28 Antigens / physiology*
  • CD4-Positive T-Lymphocytes / drug effects
  • CD4-Positive T-Lymphocytes / immunology
  • Cell Culture Techniques
  • Cell Survival
  • Coculture Techniques
  • DNA Primers
  • Forkhead Transcription Factors / genetics
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / immunology
  • Interleukin-2 Receptor alpha Subunit / deficiency
  • Interleukin-2 Receptor alpha Subunit / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Reverse Transcriptase Polymerase Chain Reaction
  • Spleen / immunology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology*
  • Thymus Gland / immunology
  • Transforming Growth Factor beta / pharmacology

Substances

  • CD28 Antigens
  • DNA Primers
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Interleukin-2 Receptor alpha Subunit
  • Transforming Growth Factor beta