Extracellular adenosine controls NKT-cell-dependent hepatitis induction

Eur J Immunol. 2014 Apr;44(4):1119-29. doi: 10.1002/eji.201343866. Epub 2014 Feb 19.

Abstract

Extracellular adenosine regulates inflammatory responses via the A2A adenosine receptor (A2AR). A2AR deficiency results in much exaggerated acute hepatitis, indicating nonredundancy of adenosine-A2AR pathway in inhibiting immune activation. To identify a critical target of immunoregulatory effect of extracellular adenosine, we focused on NKT cells, which play an indispensable role in hepatitis. An A2AR agonist abolished NKT-cell-dependent induction of acute hepatitis by concanavalin A (Con A) or α-galactosylceramide in mice, corresponding to downregulation of activation markers and cytokines in NKT cells and of NK-cell co-activation. These results show that A2AR signaling can downregulate NKT-cell activation and suppress NKT-cell-triggered inflammatory responses. Next, we hypothesized that NKT cells might be under physiological control of the adenosine-A2AR pathway. Indeed, both Con A and α-galactosylceramide induced more severe hepatitis in A2AR-deficient mice than in WT controls. Transfer of A2AR-deficient NKT cells into A2AR-expressing recipients resulted in exaggeration of Con A-induced liver damage, suggesting that NKT-cell activation is controlled by endogenous adenosine via A2AR, and this physiological regulatory mechanism of NKT cells is critical in the control of tissue-damaging inflammation. The current study suggests the possibility to manipulate NKT-cell activity in inflammatory disorders through intervention to the adenosine-A2AR pathway.

Keywords: A2A adenosine receptor; Adenosine; Hepatitis; Immunoregulation; NKT cell.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine / analogs & derivatives
  • Adenosine / immunology*
  • Adenosine / pharmacology
  • Adenosine A2 Receptor Agonists / immunology
  • Adenosine A2 Receptor Agonists / pharmacology
  • Adenosine A2 Receptor Antagonists / immunology
  • Adenosine A2 Receptor Antagonists / pharmacology
  • Animals
  • Cells, Cultured
  • Concanavalin A
  • Flow Cytometry
  • Galactosylceramides
  • Hepatitis, Animal / chemically induced
  • Hepatitis, Animal / genetics
  • Hepatitis, Animal / immunology*
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Natural Killer T-Cells / drug effects
  • Natural Killer T-Cells / immunology*
  • Natural Killer T-Cells / metabolism
  • Phenethylamines / immunology
  • Phenethylamines / pharmacology
  • Receptor, Adenosine A2A / immunology*
  • Receptor, Adenosine A2A / metabolism
  • Triazines / immunology
  • Triazines / pharmacology
  • Triazoles / immunology
  • Triazoles / pharmacology
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Adenosine A2 Receptor Agonists
  • Adenosine A2 Receptor Antagonists
  • Galactosylceramides
  • Phenethylamines
  • Receptor, Adenosine A2A
  • Triazines
  • Triazoles
  • Tumor Necrosis Factor-alpha
  • ZM 241385
  • alpha-galactosylceramide
  • Concanavalin A
  • 2-(4-(2-carboxyethyl)phenethylamino)-5'-N-ethylcarboxamidoadenosine
  • Interferon-gamma
  • Adenosine