Hepatocyte-derived IL-10 plays a crucial role in attenuating pathogenicity during the chronic phase of T. congolense infection

PLoS Pathog. 2020 Feb 3;16(2):e1008170. doi: 10.1371/journal.ppat.1008170. eCollection 2020 Feb.

Abstract

Bovine African Trypanosomosis is an infectious parasitic disease affecting livestock productivity and thereby impairing the economic development of Sub-Saharan Africa. The most important trypanosome species implicated is T. congolense, causing anemia as most important pathological feature. Using murine models, it was shown that due to the parasite's efficient immune evasion mechanisms, including (i) antigenic variation of the variable surface glycoprotein (VSG) coat, (ii) induction of polyclonal B cell activation, (iii) loss of B cell memory and (iv) T cell mediated immunosuppression, disease prevention through vaccination has so far been impossible. In trypanotolerant models a strong, early pro-inflammatory immune response involving IFN-γ, TNF and NO, combined with a strong humoral anti-VSG response, ensures early parasitemia control. This potent protective inflammatory response is counterbalanced by the production of the anti-inflammatory cytokine IL-10, which in turn prevents early death of the host from uncontrolled hyper-inflammation-mediated immunopathologies. Though at this stage different hematopoietic cells, such as NK cells, T cells and B cells as well as myeloid cells (i.e. alternatively activated myeloid cells (M2) or Ly6c- monocytes), were found to produce IL-10, the contribution of non-hematopoietic cells as potential IL-10 source during experimental T. congolense infection has not been addressed. Here, we report for the first time that during the chronic stage of T. congolense infection non-hematopoietic cells constitute an important source of IL-10. Our data shows that hepatocyte-derived IL-10 is mandatory for host survival and is crucial for the control of trypanosomosis-induced inflammation and associated immunopathologies such as anemia, hepatosplenomegaly and excessive tissue injury.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology
  • Chronic Disease
  • Disease Models, Animal
  • Female
  • Hepatocytes* / immunology
  • Hepatocytes* / parasitology
  • Hepatocytes* / pathology
  • Immune Evasion*
  • Interleukin-10 / immunology*
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / pathology
  • Lymphocyte Activation
  • Mice
  • Monocytes / immunology
  • Monocytes / pathology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / pathology
  • Trypanosoma congolense* / immunology
  • Trypanosoma congolense* / pathogenicity
  • Trypanosomiasis, African* / immunology
  • Trypanosomiasis, African* / pathology

Substances

  • IL10 protein, mouse
  • Interleukin-10

Grants and funding

This work was performed in frame of an Interuniversity Attraction Pole Program (PAIIAP N. P7/41, http://www.belspo.be/belspo/iap/index_en.stm) and was supported by the Strategic Research Program (SRP3 and SRP47, VUB) and a grant from the FWO (FWO G015016N). BS was supported by the Strategic Research Program (SRP3 and SRP47, VUB). JAVG is a member of the EU-COST action Mye-EUNITER. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.