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Babesia divergens glycosylphosphatidylinositols modulate blood coagulation and induce Th2-biased cytokine profiles in antigen presenting cells

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Date
12/2019
Author
Debierre-Grockiego, Françoise
Smith, Terry K.
Delbecq, Stéphane
Ducournau, Céline
Lantier, Louis
Schmidt, Jörg
Brès, Virginie
Dimier-Poisson, Isabelle
Schwarz, Ralph T.
Cornillot, Emmanuel
Keywords
Antigen presentation
Coagulation
Glycosylphosphatidylinositol
Interleukin
Major histocompatibility complex
QD Chemistry
QH301 Biology
RC0254 Neoplasms. Tumors. Oncology (including Cancer)
NDAS
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Abstract
Glycosylphosphatidylinositols (GPIs) are glycolipids described as toxins of protozoan parasites due to their inflammatory properties in mammalian hosts characterized by the production of interleukin (IL)-1, IL-12 and tumor necrosis factor (TNF)-α. In the present work, we studied the cytokines produced by antigen presenting cells in response to ten different GPI species extracted from Babesia divergens, responsible for babesiosis. Interestingly, B. divergens GPIs induced the production of anti-inflammatory cytokines (IL-2, IL-5) and of the regulatory cytokine IL-10 by macrophages and dendritic cells. In contrast to all protozoan GPIs studied until now, GPIs from B. divergens did not stimulate the production of TNF-α and IL-12, leading to a unique Th1/Th2 profile. Analysis of the carbohydrate composition of the B. divergens GPIs indicated that the di-mannose structure was different from the evolutionary conserved tri-mannose structure, which might explain the particular cytokine profile they induce. Expression of major histocompatibility complex (MHC) molecules on dendritic cells and apoptosis of mouse peritoneal cells were also analysed. B. divergens GPIs did not change expression of MHC class I, but decreased expression of MHC class II at the cell surface, while GPIs slightly increased the percentages of apoptotic cells. During pathogenesis of babesiosis, the inflammation-coagulation auto-amplification loop can lead to thrombosis and the effect of GPIs on coagulation parameters was investigated. Incubation of B. divergens GPIs with rat plasma ex vivo led to increase of fibrinogen levels and to prolonged activated partial thromboplastin time, suggesting a direct modulation of the extrinsic coagulation pathway by GPIs.
Citation
Debierre-Grockiego , F , Smith , T K , Delbecq , S , Ducournau , C , Lantier , L , Schmidt , J , Brès , V , Dimier-Poisson , I , Schwarz , R T & Cornillot , E 2019 , ' Babesia divergens glycosylphosphatidylinositols modulate blood coagulation and induce Th2-biased cytokine profiles in antigen presenting cells ' , Biochimie , vol. 167 , pp. 135-144 . https://doi.org/10.1016/j.biochi.2019.09.007
Publication
Biochimie
Status
Peer reviewed
DOI
https://doi.org/10.1016/j.biochi.2019.09.007
ISSN
0300-9084
Type
Journal article
Rights
Copyright © 2019 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Description
This work was supported by the the University of Tours (to IDP and FDG), the University of Montpellier (to SD and EC), the Deutsche Forschungsgemeinschaft (to RTS), the Wellcome Trust project grant 093228 (to TKS) and the Campus France/DAAD PHC PROCOPE 24931RE (to RTS and EC). The funding source has no involvement in the conduct of the research and preparation of the article.
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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/18813

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