Characteristics of IL-17 induction by Schistosoma japonicum infection in C57BL/6 mouse liver

Immunology. 2013 Aug;139(4):523-32. doi: 10.1111/imm.12105.

Abstract

Schistosomiasis japonica is a severe tropical disease caused by the parasitic worm Schistosoma japonicum. Among the most serious pathological effects of S. japonicum infection are hepatic lesions (cirrhosis and fibrosis) and portal hypertension. Interleukin-17 (IL-17) is a pro-inflammatory cytokine involved in the pathogenesis of many inflammatory and infectious conditions, including schistosomiasis. We infected C57BL/6 mice with S. japonicum and isolated lymphocytes from the liver to identify cell subsets with high IL-17 expression and release using flow cytometry and ELISA. Expression and release of IL-17 was significantly higher in hepatic lymphocytes from infected mice compared with control mice in response to both non-specific stimulation with anti-CD3 monoclonal antibody plus/anti-CD28 monoclonal antibody and PMA plus ionomycin. We then compared IL-17 expression in three hepatic T-cell subsets, T helper, natural killer T and γδT cells, to determine the major source of IL-17 during infection. Interleukin-17 was induced in all three subsets by PMA + ionomycin, but γδT lymphocytes exhibited the largest increase in expression. We then established a mouse model to further investigate the role of IL-17 in granulomatous and fibrosing inflammation against parasite eggs. Reducing IL-17 activity using anti-IL-17A antibodies decreased infiltration of inflammatory cells and collagen deposition in the livers of infected C57BL/6 mice. The serum levels of soluble egg antigen (IL)-specific IgGs were enhanced by anti-IL-17A monoclonal antibody blockade, suggesting that IL-17 normally serves to suppress this humoral response. These findings suggest that γδT cells are the most IL-17-producing cells and that IL-17 contributes to granulomatous inflammatory and fibrosing reactions in S. japonicum-infected C57BL/6 mouse liver.

Keywords: Schistosoma japonicum; T helper type 17; interleukin-17; liver; natural killer T cell; γδT cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Antibodies, Neutralizing / pharmacology
  • Antibodies, Protozoan / blood
  • Cells, Cultured
  • Collagen Type III / metabolism
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Flow Cytometry
  • Granuloma / drug therapy
  • Granuloma / immunology
  • Granuloma / parasitology
  • Inflammation Mediators / metabolism*
  • Interleukin-17 / metabolism*
  • Ionomycin / pharmacology
  • Liver / drug effects
  • Liver / immunology*
  • Liver / parasitology
  • Liver / pathology
  • Liver Cirrhosis / drug therapy
  • Liver Cirrhosis / immunology
  • Liver Cirrhosis / parasitology
  • Mice
  • Mice, Inbred C57BL
  • Natural Killer T-Cells / immunology
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Schistosoma japonicum / immunology*
  • Schistosoma japonicum / pathogenicity
  • Schistosomiasis japonica / drug therapy
  • Schistosomiasis japonica / immunology*
  • Schistosomiasis japonica / parasitology
  • Schistosomiasis japonica / pathology
  • T-Lymphocyte Subsets / drug effects
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / parasitology
  • Th17 Cells / immunology
  • Up-Regulation

Substances

  • Antibodies, Monoclonal
  • Antibodies, Neutralizing
  • Antibodies, Protozoan
  • Collagen Type III
  • Il17a protein, mouse
  • Inflammation Mediators
  • Interleukin-17
  • Receptors, Antigen, T-Cell, gamma-delta
  • Ionomycin