Dendritic cell-secreted lipocalin2 induces CD8+ T-cell apoptosis, contributes to T-cell priming and leads to a TH1 phenotype

PLoS One. 2014 Jul 10;9(7):e101881. doi: 10.1371/journal.pone.0101881. eCollection 2014.

Abstract

Lipocalin 2 (LCN2), which is highly expressed by dendritic cells (DCs) when treated with dexamethasone (Dex) and lipopolysaccharide (LPS), plays a key role in the defence against bacteria and is also involved in the autocrine apoptosis of T-cells. However, the function of LCN2 when secreted by DCs is unknown: this is a critical gap in our understanding of the regulation of innate and adaptive immune systems. Tolerance, stimulation and suppression are functions of DCs that facilitate the fine-tuning of the immune responses and which are possibly influenced by LCN2 secretion. We therefore examined the role of LCN2 in DC/T-cell interaction. WT or Lcn2-/- bone marrow-derived DCs were stimulated with LPS or LPS+IFN-γ with and without Dex and subsequently co-cultured with T-cells from ovalbumin-specific TCR transgenic (OT-I and OT-II) mice. We found that CD8+ T-cell apoptosis was highly reduced when Lcn2-/- DCs were compared with WT. An in vivo CTL assay, using LPS-treated DCs, showed diminished killing ability in mice that had received Lcn2-/- DCs compared with WT DCs. As a consequence, we analysed T-cell proliferation and found that LCN2 participates in T-cell-priming in a dose-dependent manner and promotes a TH1 microenvironment. DC-secreted LCN2, whose function has previously been unknown, may in fact have an important role in regulating the balance between TH1 and TH2. Our results yield insights into DC-secreted LCN2 activity, which could play a pivotal role in cellular immune therapy and in regulating immune responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute-Phase Proteins / deficiency
  • Acute-Phase Proteins / genetics
  • Acute-Phase Proteins / metabolism*
  • Animals
  • Apoptosis / drug effects
  • Apoptosis / immunology*
  • CD8-Positive T-Lymphocytes / cytology*
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology*
  • Cellular Microenvironment / drug effects
  • Cellular Microenvironment / immunology
  • Cytokines / metabolism
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism*
  • Female
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / immunology
  • Immunization
  • Interferon-gamma / pharmacology
  • Lipocalin-2
  • Lipocalins / genetics
  • Lipocalins / metabolism*
  • Lipopolysaccharides / pharmacology
  • Mice
  • Oncogene Proteins / deficiency
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism*
  • Phenotype*
  • Th1 Cells / cytology*
  • Th1 Cells / drug effects
  • Th1 Cells / immunology

Substances

  • Acute-Phase Proteins
  • Cytokines
  • Lipocalin-2
  • Lipocalins
  • Lipopolysaccharides
  • Oncogene Proteins
  • Lcn2 protein, mouse
  • Interferon-gamma

Grants and funding

This work was supported by St. Anna Kinderkrebsforschung. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.