A Regulatory Feedback between Plasmacytoid Dendritic Cells and Regulatory B Cells Is Aberrant in Systemic Lupus Erythematosus

Immunity. 2016 Mar 15;44(3):683-697. doi: 10.1016/j.immuni.2016.02.012. Epub 2016 Mar 8.

Abstract

Signals controlling the generation of regulatory B (Breg) cells remain ill-defined. Here we report an "auto"-regulatory feedback mechanism between plasmacytoid dendritic cells (pDCs) and Breg cells. In healthy individuals, pDCs drive the differentiation of CD19(+)CD24(hi)CD38(hi) (immature) B cells into IL-10-producing CD24(+)CD38(hi) Breg cells and plasmablasts, via the release of IFN-α and CD40 engagement. CD24(+)CD38(hi) Breg cells conversely restrained IFN-α production by pDCs via IL-10 release. In systemic lupus erythematosus (SLE), this cross-talk was compromised; pDCs promoted plasmablast differentiation but failed to induce Breg cells. This defect was recapitulated in healthy B cells upon exposure to a high concentration of IFN-α. Defective pDC-mediated expansion of CD24(+)CD38(hi) Breg cell numbers in SLE was associated with altered STAT1 and STAT3 activation. Both altered pDC-CD24(+)CD38(hi) Breg cell interactions and STAT1-STAT3 activation were normalized in SLE patients responding to rituximab. We propose that alteration in pDC-CD24(+)CD38(hi) Breg cell interaction contributes to the pathogenesis of SLE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Antigens, CD / metabolism
  • Antirheumatic Agents / administration & dosage
  • B-Lymphocytes, Regulatory / drug effects
  • B-Lymphocytes, Regulatory / immunology*
  • Cell Communication / drug effects
  • Cell Differentiation / drug effects
  • Cells, Cultured
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology*
  • Female
  • Homeostasis / drug effects
  • Humans
  • Interferon-gamma / metabolism
  • Interleukin-10 / metabolism
  • Lupus Erythematosus, Systemic / drug therapy
  • Lupus Erythematosus, Systemic / immunology*
  • Male
  • Middle Aged
  • Rituximab / administration & dosage
  • STAT1 Transcription Factor / metabolism
  • STAT3 Transcription Factor / metabolism
  • Transcriptional Activation / drug effects
  • Young Adult

Substances

  • Antigens, CD
  • Antirheumatic Agents
  • STAT1 Transcription Factor
  • STAT3 Transcription Factor
  • Interleukin-10
  • Rituximab
  • Interferon-gamma