Cytokine-dependent regulation of dendritic cell differentiation in the splenic microenvironment

Eur J Immunol. 2014 Feb;44(2):500-10. doi: 10.1002/eji.201343820. Epub 2013 Dec 12.

Abstract

The DC-derived chemokine CCL17, a ligand of CCR4, has been shown to promote various inflammatory diseases such as atopic dermatitis, atherosclerosis, and inflammatory bowel disease. Under steady-state conditions, and even after systemic stimulation with LPS, CCL17 is not expressed in resident splenic DCs as opposed to CD8α⁻CD11b⁺ LN DCs, which produce large amounts of CCL17 in particular after maturation. Upon systemic NKT cell activation through α-galactosylceramide stimulation however, CCL17 can be upregulated in both CD8α⁻ and CD8α⁺ splenic DC subsets and enhances cross-presentation of exogenous antigens. Based on genome-wide expression profiling, we now show that splenic CD11b⁺ DCs are susceptible to IFN-γ-mediated suppression of CCL17, whereas LN CD11b⁺CCL17⁺ DCs downregulate the IFN-γR and are much less responsive to IFN-γ. Under inflammatory conditions, particularly in the absence of IFN-γ signaling in IFN-γRKO mice, CCL17 expression is strongly induced in a major proportion of splenic DCs by the action of GM-CSF in concert with IL-4. Our findings demonstrate that the local cytokine milieu and differential cytokine responsiveness of DC subsets regulate lymphoid organ specific immune responses at the level of chemokine expression.

Keywords: DCs; GM-CSF; IFN-γ receptor; IL-4; Spleen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD11b Antigen / immunology
  • CD11b Antigen / metabolism
  • Cell Differentiation / immunology*
  • Cellular Microenvironment / immunology*
  • Chemokine CCL17 / immunology
  • Chemokine CCL17 / metabolism
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism*
  • Granulocyte-Macrophage Colony-Stimulating Factor / immunology
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Interferon gamma Receptor
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism*
  • Interleukin-4 / immunology
  • Interleukin-4 / metabolism*
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Interferon / deficiency
  • Receptors, Interferon / immunology
  • Receptors, Interferon / metabolism*
  • Spleen / immunology
  • Spleen / metabolism*

Substances

  • CD11b Antigen
  • Ccl17 protein, mouse
  • Chemokine CCL17
  • Receptors, Interferon
  • Interleukin-4
  • Interferon-gamma
  • Granulocyte-Macrophage Colony-Stimulating Factor