Α-galactosylceramide analogs with weak agonist activity for human iNKT cells define new candidate anti-inflammatory agents

PLoS One. 2010 Dec 17;5(12):e14374. doi: 10.1371/journal.pone.0014374.

Abstract

CD1d-restricted natural killer T cells with invariant T cell receptor α chains (iNKT cells) are a unique lymphocyte subset that responds to recognition of specific lipid and glycolipid antigens. They are conserved between mice and humans and exert various immunoregulatory functions through their rapid secretion of a variety of cytokines and secondary activation of dendritic cells, B cells and NK cells. In the current study, we analyzed the range of functional activation states of human iNKT cells using a library of novel analogs of α-galactosylceramide (αGalCer), the prototypical iNKT cell antigen. Measurement of cytokines secreted by human iNKT cell clones over a wide range of glycolipid concentrations revealed that iNKT cell ligands could be classified into functional groups, correlating with weak versus strong agonistic activity. The findings established a hierarchy for induction of different cytokines, with thresholds for secretion being consistently lowest for IL-13, higher for interferon-γ (IFNγ), and even higher for IL-4. These findings suggested that human iNKT cells can be intrinsically polarized to selective production of IL-13 by maintaining a low level of activation using weak agonists, whereas selective polarization to IL-4 production cannot be achieved through modulating the strength of the activating ligand. In addition, using a newly designed in vitro system to assess the ability of human iNKT cells to transactivate NK cells, we found that robust secondary induction of interferon-γ secretion by NK cells was associated with strong but not weak agonist ligands of iNKT cells. These results indicate that polarization of human iNKT cell responses to Th2-like or anti-inflammatory effects may best be achieved through selective induction of IL-13 and suggest potential discrepancies with findings from mouse models that may be important in designing iNKT cell-based therapies in humans.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Inflammatory Agents / pharmacology*
  • CD40 Ligand / metabolism
  • Drug Design
  • Enzyme-Linked Immunosorbent Assay / methods
  • Flow Cytometry / methods
  • Galactosylceramides / agonists
  • Galactosylceramides / chemistry*
  • Glycolipids / chemistry
  • HeLa Cells
  • Humans
  • Interleukin-13 / metabolism
  • Interleukin-4 / metabolism
  • Leukocytes, Mononuclear / cytology
  • Models, Chemical
  • Natural Killer T-Cells / drug effects*
  • Th2 Cells / metabolism

Substances

  • Anti-Inflammatory Agents
  • Galactosylceramides
  • Glycolipids
  • Interleukin-13
  • alpha-galactosylceramide
  • CD40 Ligand
  • Interleukin-4