Immunomodulatory effects of Amblyomma variegatum saliva on bovine cells: Characterization of cellular responses and identification of molecular determinants

Rodrigues Valérie, Fernandez Bernard, Vercoutere Arthur, Chamayou Léo, Andersen Alexandre, Vigy Oana, Demettre Edith, Seveno Martial, Aprelon Rosalie, Giraud-Girard Ken, Stachurski Frédéric, Loire Etienne, Vachiéry Nathalie, Holzmuller Philippe. 2018. Immunomodulatory effects of Amblyomma variegatum saliva on bovine cells: Characterization of cellular responses and identification of molecular determinants. Frontiers in Cellular and Infection Microbiology, 7:521, 18 p.

Journal article ; Article de recherche ; Article de revue à facteur d'impact
Published version - Anglais
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Quartile : Q2, Sujet : MICROBIOLOGY / Quartile : Q2, Sujet : IMMUNOLOGY

Abstract : The tropical bont tick, Amblyomma variegatum, is a tick species of veterinary importance and is considered as one of major pest of ruminants in Africa and in the Caribbean. It causes direct skin lesions, transmits heartwater, and reactivates bovine dermatophilosis. Tick saliva is reported to affect overall host responses through immunomodulatory and anti-inflammatory molecules, among other bioactive molecules. The general objective of this study was to better understand the role of saliva in interaction between the Amblyomma tick and the host using cellular biology approaches and proteomics, and to discuss its impact on disease transmission and/or activation. We first focused on the immuno-modulating effects of semi-fed A. variegatum female saliva on bovine peripheral blood mononuclear cells (PBMC) and monocyte-derived macrophages in vitro. We analyzed its immuno-suppressive properties by measuring the effect of saliva on PBMC proliferation, and observed a significant decrease in ConA-stimulated PBMC lymphoproliferation. We then studied the effect of saliva on bovine macrophages using flow cytometry to analyze the expression of MHC-II and co-stimulation molecules (CD40, CD80, and CD86) and by measuring the production of nitric oxide (NO) and pro- or anti-inflammatory cytokines. We observed a significant decrease in the expression of MHC-II, CD40, and CD80 molecules, associated with decreased levels of IL-12-p40 and TNF-α and increased level of IL-10, which could explain the saliva-induced modulation of NO. To elucidate these immunomodulatory effects, crude saliva proteins were analyzed using proteomics with an Orbitrap Elite mass spectrometer. Among the 336 proteins identified in A. variegatum saliva, we evidenced bioactive molecules exhibiting anti-inflammatory, immuno-modulatory, and anti-oxidant properties (e.g., serpins, phospholipases A2, heme lipoprotein). We also characterized an intriguing ubiquitination complex that could be involved in saliva-induced immune modulation of the host. We propose a model for the interaction between A. variegatum saliva and host immune cells that could have an effect during tick feeding by favoring pathogen dissemination or activation by reducing the efficiency of host immune response to the corresponding tick-borne diseases. (Résumé d'auteur)

Classification Agris : L73 - Animal diseases

Champ stratégique Cirad : Axe 4 (2014-2018) - Santé des animaux et des plantes

Agence(s) de financement européenne(s) : European Regional Development Fund

Projet(s) de financement européen(s) : Surveillance, diagnosis, control and impact of infectious diseases of humans, animals and plants in tropical islands

Auteurs et affiliations

  • Rodrigues Valérie, CIRAD-BIOS-UMR ASTRE (FRA)
  • Fernandez Bernard, CIRAD-BIOS-UMR ASTRE (FRA)
  • Vercoutere Arthur, Université de Montpellier (FRA)
  • Chamayou Léo, Université de Montpellier (FRA)
  • Andersen Alexandre, Université de Montpellier (FRA)
  • Vigy Oana, Institut de génomique fonctionnelle (FRA)
  • Demettre Edith, CNRS (FRA)
  • Seveno Martial, CNRS (FRA)
  • Aprelon Rosalie, CIRAD-BIOS-UMR ASTRE (GLP)
  • Giraud-Girard Ken, CIRAD-BIOS-UMR ASTRE (GLP)
  • Stachurski Frédéric, CIRAD-BIOS-UMR ASTRE (FRA)
  • Loire Etienne, CIRAD-BIOS-UMR ASTRE (FRA)
  • Vachiéry Nathalie, CIRAD-BIOS-UMR ASTRE (FRA)
  • Holzmuller Philippe, CIRAD-BIOS-UMR ASTRE (FRA) ORCID: 0000-0002-8919-9081 - auteur correspondant

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