A glycosylphosphatidylinositol-based treatment alleviates trypanosomiasis-associated immunopathology

J Immunol. 2007 Sep 15;179(6):4003-14. doi: 10.4049/jimmunol.179.6.4003.

Abstract

The GPI-anchored trypanosome variant surface glycoprotein (VSG) triggers macrophages to produce TNF, involved in trypanosomiasis-associated inflammation and the clinical manifestation of sleeping sickness. Aiming at inhibiting immunopathology during experimental Trypanosoma brucei infections, a VSG-derived GPI-based treatment approach was developed. To achieve this, mice were exposed to the GPI before an infectious trypanosome challenge. This GPI-based strategy resulted in a significant prolonged survival and a substantial protection against infection-associated weight loss, liver damage, acidosis, and anemia; the latter was shown to be Ab-independent and correlated with reduced macrophage-mediated RBC clearance. In addition, GPI-based treatment resulted in reduced circulating serum levels of the inflammatory cytokines TNF and IL-6, abrogation of infection-induced LPS hypersensitivity, and an increase in circulating IL-10. At the level of trypanosomiasis-associated macrophage activation, the GPI-based treatment resulted in an impaired secretion of TNF by VSG and LPS pulsed macrophages, a reduced expression of the inflammatory cytokine genes TNF, IL-6, and IL-12, and an increased expression of the anti-inflammatory cytokine gene IL-10. In addition, this change in cytokine pattern upon GPI-based treatment was associated with the expression of alternatively activated macrophage markers. Finally, the GPI-based treatment also reduced the infection-associated pathology in Trypanosoma congolense and Trypanosoma evansi model systems as well as in tsetse fly challenge experiments, indicating potential field applicability for this intervention strategy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anemia / therapy
  • Animals
  • Antigens, CD1 / physiology
  • Antigens, CD1d
  • B-Lymphocyte Subsets / drug effects
  • B-Lymphocyte Subsets / pathology
  • Disease Models, Animal
  • Glycosylphosphatidylinositols / therapeutic use*
  • Inflammation Mediators / therapeutic use
  • Lymphopenia / immunology
  • Lymphopenia / parasitology
  • Lymphopenia / therapy
  • Macrophage Activation / drug effects
  • Macrophage Activation / immunology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Signal Transduction / drug effects
  • Signal Transduction / immunology
  • Trypanosoma brucei brucei / chemistry
  • Trypanosoma brucei brucei / immunology*
  • Trypanosoma brucei brucei / pathogenicity
  • Trypanosomiasis, African / immunology*
  • Trypanosomiasis, African / pathology*
  • Trypanosomiasis, African / therapy
  • Variant Surface Glycoproteins, Trypanosoma / therapeutic use

Substances

  • Antigens, CD1
  • Antigens, CD1d
  • Glycosylphosphatidylinositols
  • Inflammation Mediators
  • Variant Surface Glycoproteins, Trypanosoma