Interleukin-15-induced CD56(+) myeloid dendritic cells combine potent tumor antigen presentation with direct tumoricidal potential

PLoS One. 2012;7(12):e51851. doi: 10.1371/journal.pone.0051851. Epub 2012 Dec 28.

Abstract

Dendritic cells (DCs) are the quintessential antigen-presenting cells of the human immune system and play a prime role in coordinating innate and adaptive immune responses, explaining the strong and still growing interest in their application for cancer immunotherapy. Much current research in the field of DC-based immunotherapy focuses on optimizing the culture conditions for in vitro DC generation in order to assure that DCs with the best possible immunogenic qualities are being used for immunotherapy. In this context, monocyte-derived DCs that are alternatively induced by interleukin-15 (IL-15 DCs) have attracted recent attention due to their superior immunostimulatory characteristics. In this study, we show that IL-15 DCs, in addition to potent tumor antigen-presenting function, possess tumoricidal potential and thus qualify for the designation of killer DCs. Notwithstanding marked expression of the natural killer (NK) cell marker CD56 on a subset of IL-15 DCs, we found no evidence of a further phenotypic overlap between IL-15 DCs and NK cells. Allostimulation and antigen presentation assays confirmed that IL-15 DCs should be regarded as bona fide myeloid DCs not only from the phenotypic but also from the functional point of view. Concerning their cytotoxic activity, we demonstrate that IL-15 DCs are able to induce apoptotic cell death of the human K562 tumor cell line, while sparing tumor antigen-specific T cells. The cytotoxicity of IL-15 DCs is predominantly mediated by granzyme B and, to a small extent, by tumor necrosis factor-α (TNF-α)-related apoptosis-inducing ligand (TRAIL) but is independent of perforin, Fas ligand and TNF-α. In conclusion, our data provide evidence of a previously unappreciated role for IL-15 in the differentiation of human monocytes towards killer DCs. The observation that IL-15 DCs have killer DC capacity lends further support to their implementation in DC-based immunotherapy protocols.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigen-Presenting Cells / immunology*
  • CD56 Antigen / immunology*
  • Cell Differentiation
  • Cytotoxicity, Immunologic / immunology*
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology*
  • Flow Cytometry
  • Granzymes / immunology
  • Granzymes / metabolism
  • Humans
  • Interleukin-15 / immunology*
  • Killer Cells, Natural / immunology
  • Monocytes / cytology
  • Monocytes / immunology
  • Myeloid Cells / immunology*
  • Neoplasms / immunology*
  • Neoplasms / metabolism
  • Neoplasms / pathology

Substances

  • CD56 Antigen
  • Interleukin-15
  • NCAM1 protein, human
  • Granzymes

Grants and funding

This work was supported in part by research grants of the Research Foundation Flanders (FWO Vlaanderen, www.fwo.be), the Belgian Foundation against Cancer (Stichting tegen Kanker, www.kanker.be), the Methusalem program of the Flemish Government attributed to Prof Herman Goossens (University of Antwerp, Belgium), the Interuniversity Attraction Pole program (IAP #P6/41) of the Belgian Government and the Belgian Hercules Foundation (www.herculesstichting.be). SA is a PhD fellow of the Research Foundation Flanders and received financial support from the Belgian Foundation against Cancer and the Belgian public utility foundation VOCATIO (www.vocatio.be). EL holds an Emmanuel van der Schueren Fellowship of the Flemish League against Cancer (Vlaamse Liga tegen Kanker, www.tegenkanker.be). JT was supported by a grant from The Netherlands Organization for Scientific Research (NWO ZonMW, www.zonmw.nl). YW is funded by a PhD grant of the Institute for the Promotion of Innovation through Science and Technology (IWT, www.iwt.be). NC and ELS are post-doctoral fellows of the Research Foundation Flanders. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.