Human blood BDCA-1 dendritic cells differentiate into Langerhans-like cells with thymic stromal lymphopoietin and TGF-β

Blood. 2014 Oct 9;124(15):2411-20. doi: 10.1182/blood-2014-04-568311. Epub 2014 Aug 11.

Abstract

The ontogeny of human Langerhans cells (LCs) remains poorly characterized, in particular the nature of LC precursors and the factors that may drive LC differentiation. Here we report that thymic stromal lymphopoietin (TSLP), a keratinocyte-derived cytokine involved in epithelial inflammation, cooperates with transforming growth factor (TGF)-β for the generation of LCs. We show that primary human blood BDCA-1(+), but not BDCA-3(+), dendritic cells (DCs) stimulated with TSLP and TGF-β harbor a typical CD1a(+)Langerin(+) LC phenotype. Electron microscopy established the presence of Birbeck granules, an intracellular organelle specific to LCs. LC differentiation was not observed from tonsil BDCA-1(+) and BDCA-3(+) subsets. TSLP + TGF-β LCs had a mature phenotype with high surface levels of CD80, CD86, and CD40. They induced a potent CD4(+) T-helper (Th) cell expansion and differentiation into Th2 cells with increased production of tumor necrosis factor-α and interleukin-6 compared with CD34-derived LCs. Our findings establish a novel LC differentiation pathway from BDCA-1(+) blood DCs with potential implications in epithelial inflammation. Therapeutic targeting of TSLP may interfere with tissue LC repopulation from circulating precursors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD1 / metabolism*
  • Cell Differentiation / drug effects*
  • Cell Differentiation / genetics
  • Cytokines / pharmacology*
  • Cytoplasmic Granules / drug effects
  • Cytoplasmic Granules / metabolism
  • Cytoplasmic Granules / ultrastructure
  • Dendritic Cells / cytology*
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Gene Expression Profiling
  • Glycoproteins / metabolism*
  • Humans
  • Langerhans Cells / cytology*
  • Langerhans Cells / drug effects
  • Langerhans Cells / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Phenotype
  • Skin / metabolism
  • Th2 Cells / cytology
  • Th2 Cells / drug effects
  • Th2 Cells / metabolism
  • Thymic Stromal Lymphopoietin
  • Transforming Growth Factor beta / pharmacology*

Substances

  • Antigens, CD1
  • CD1C protein, human
  • Cytokines
  • Glycoproteins
  • Transforming Growth Factor beta
  • Thymic Stromal Lymphopoietin