CD39 mediated regulation of Th17-cell effector function is impaired in juvenile autoimmune liver disease

J Autoimmun. 2016 Aug:72:102-12. doi: 10.1016/j.jaut.2016.05.005. Epub 2016 May 20.

Abstract

Background & aims: T-helper-type 17 (Th17) cells are involved in autoimmune tissue damage. CD39 is an ectonucleotidase that catalyzes extracellular ATP/ADP hydrolysis, culminating in the generation of immunosuppressive adenosine. Functional CD39 expression confers immunosuppressive properties upon immune cells. As the proportion of CD39 lymphocytes is decreased in juvenile autoimmune liver disease (AILD), we have explored whether decreased CD39 expression is present on Th17 cells and whether this phenomenon is associated with heightened effector function and inflammation.

Methods: Thirty-eight patients with juvenile AILD (22 autoimmune hepatitis and 16 autoimmune sclerosing cholangitis), 8 disease controls (DC) and 16 healthy subjects (HS) were studied. Peripheral blood cell phenotype was determined by flow cytometry; ability to suppress by inhibition of cell proliferation/effector cytokine production; ectoenzymatic activity by thin layer chromatography; expression of adenosine receptor, adenosine deaminase (ADA) and phosphodiesterases (PDE) by quantitative real-time PCR or by Western Blot.

Results: CD39(+) Th17 (Th17(CD39+)) cells from HS appear activated and contain high frequencies of lymphocytes producing regulatory cytokines. In AILD, however, Th17(CD39+) cells are markedly diminished and fail to generate AMP/adenosine, thereby limiting control of both target cell proliferation and IL-17 production. When compared to HS, Th17 cells from AILD patients also show lower A2A adenosine receptor expression while displaying similar levels of PDE4A, PDE4B and ADA. Only rare Th17(CD39+) cells are observed by liver immunohistochemistry.

Conclusions: Th17(CD39+) cells in juvenile AILD are both quantitatively decreased and qualitatively deficient. Low levels CD39 and A2A expression may contribute to the perpetuation of Th17 cell effector properties and unfettered inflammation in this disease.

Keywords: ATP; Adenosine; Autoimmune liver disease; CD39; Th17 cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Deaminase / genetics
  • Adenosine Deaminase / immunology
  • Adenosine Deaminase / metabolism
  • Adolescent
  • Adult
  • Antigens, CD / immunology*
  • Antigens, CD / metabolism
  • Apyrase / immunology*
  • Apyrase / metabolism
  • Blotting, Western
  • Cell Proliferation
  • Child
  • Child, Preschool
  • Cholangitis, Sclerosing / immunology*
  • Female
  • Flow Cytometry
  • Gene Expression / immunology
  • Hepatitis, Autoimmune / immunology*
  • Humans
  • Immunohistochemistry
  • Infant
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism
  • Male
  • Phosphoric Diester Hydrolases / genetics
  • Phosphoric Diester Hydrolases / immunology
  • Phosphoric Diester Hydrolases / metabolism
  • Receptor, Adenosine A2A / genetics
  • Receptor, Adenosine A2A / immunology
  • Receptor, Adenosine A2A / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism
  • Young Adult

Substances

  • Antigens, CD
  • Interleukin-17
  • Receptor, Adenosine A2A
  • Phosphoric Diester Hydrolases
  • Adenosine Deaminase
  • Apyrase
  • CD39 antigen