Thymic stromal lymphopoietin-activated plasmacytoid dendritic cells induce the generation of FOXP3+ regulatory T cells in human thymus

J Immunol. 2010 Mar 15;184(6):2999-3007. doi: 10.4049/jimmunol.0804106. Epub 2010 Feb 19.

Abstract

Human thymus contains major dendritic cell (DC) subsets, myeloid DCs (mDCs), and plasmacytoid DCs (pDCs). We previously showed that mDCs, educated by thymic stromal lymphopoietin (TSLP) produced by the epithelial cells of the Hassall's corpuscles, induced differentiation of CD4(+)CD25(-) thymocytes into Forkhead Box P3(+) (FOXP3(+)) regulatory T cells (T(R)) within the medulla of human thymus. In this study, we show that pDCs expressed the TSLP receptor and IL-7 receptor alpha complexes upon activation and became responsive to TSLP. TSLP-activated human pDCs secrete macrophage-derived chemokine CCL-22 and thymus- and activation-regulated chemokine CCL-17 but not Th1- or Th2-polarizing cytokines. TSLP-activated pDCs induced the generation of FOXP3(+) T(R) from CD4(+)CD8(-)CD25(-) thymocytes, which could be strongly inhibited by Th1-polarizing cytokine IL-12 or Th2-polarizing cytokine IL-4. Interestingly, the FOXP3(+) T(R) induced by the TSLP-pDCs expressed more IL-10 but less TGF-beta than that induced by the TSLP-mDCs. These data suggest that TSLP expressed by thymic epithelial cells can activate mDCs and pDCs to positively select the FOXP3(+) T(R) with different cytokine production potential in human thymus. The inability of TSLP to induce DC maturation without producing Th1- or Th2-polarizing cytokines may provide a thymic niche for T(R) development.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • B7-1 Antigen / biosynthesis
  • B7-2 Antigen / biosynthesis
  • Cell Differentiation / immunology*
  • Cells, Cultured
  • Chemokine CCL17 / metabolism
  • Chemokine CCL22 / metabolism
  • Child, Preschool
  • Coculture Techniques
  • Cytokines / physiology*
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Forkhead Transcription Factors / biosynthesis*
  • Humans
  • Infant
  • Infant, Newborn
  • Interleukin-7 Receptor alpha Subunit / biosynthesis
  • Receptors, Cytokine / biosynthesis
  • Stromal Cells / immunology
  • Stromal Cells / metabolism
  • T-Lymphocytes, Regulatory / cytology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism*
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Th2 Cells / immunology
  • Th2 Cells / metabolism
  • Thymic Stromal Lymphopoietin
  • Thymus Gland / cytology
  • Thymus Gland / immunology*
  • Thymus Gland / metabolism*

Substances

  • B7-1 Antigen
  • B7-2 Antigen
  • CCL17 protein, human
  • CCL22 protein, human
  • CRLF2 protein, human
  • Chemokine CCL17
  • Chemokine CCL22
  • Cytokines
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Interleukin-7 Receptor alpha Subunit
  • Receptors, Cytokine
  • Thymic Stromal Lymphopoietin