The Immunomodulatory Effect of IrSPI, a Tick Salivary Gland Serine Protease Inhibitor Involved in Ixodes ricinus Tick Feeding

Blisnick, Adrien A.; Šimo, Ladislav; Grillon, Catherine; Fasani, Fabienne; Brûlé, Sébastien; Le Bonniec, Bernard; Prina, Eric; Marsot, Maud; Relmy, Anthony; Blaise-Boisseau, Sandra; Richardson, Jennifer; Bonnet, Sarah I.

doi:10.3390/vaccines7040148

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The Immunomodulatory Effect of IrSPI, a Tick Salivary Gland Serine Protease Inhibitor Involved in Ixodes ricinus Tick Feeding

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Sandra Blaise-Boisseau

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Jennifer Richardson

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Sarah I. Bonnet

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UMR BIPAR, Animal Health Laboratory, INRA, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94701 Maisons-Alfort CEDEX, France

Centre de Biophysique Moléculaire—UPR 4301 CNRS, 45000 Orléans, France

Plateforme de Biophysique moléculaire, Institut Pasteur, UMR 3528 CNRS, 75015 Paris, France

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INSERM UMR-S1140, Faculté de Pharmacie Université Paris Descartes, Sorbonne Paris Cité, 75270 Paris CEDEX 06, France

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Unité de Parasitologie moléculaire et Signalisation—INSERM U1201, Institut Pasteur, 75015 Paris, France

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Unité EPI, Animal Health Laboratory, INRA, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94701 Maisons-Alfort CEDEX, France

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UMR Virologie 1161, Animal Health Laboratory, INRA, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94701 Maisons-Alfort CEDEX, France

Author to whom correspondence should be addressed.

Vaccines 2019, 7(4), 148; https://doi.org/10.3390/vaccines7040148

Received: 5 August 2019 / Revised: 2 October 2019 / Accepted: 4 October 2019 / Published: 12 October 2019

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Abstract

Ticks are the most important vectors of pathogens affecting both domestic and wild animals worldwide. Hard tick feeding is a slow process—taking up to several days—and necessitates extended control over the host response. The success of the feeding process depends upon injection of tick saliva, which not only controls host hemostasis and wound healing, but also subverts the host immune response to avoid tick rejection that creates a favorable niche for the survival and propagation of diverse tick-borne pathogens. Here, we report on the molecular and biochemical features and functions of an Ixodes ricinus serine protease inhibitor (IrSPI). We characterize IrSPI as a Kunitz elastase inhibitor that is overexpressed in several tick organs—especially salivary glands—during blood-feeding. We also demonstrated that when IrSPI is injected into the host through saliva, it had no impact on tissue factor pathway-induced coagulation, fibrinolysis, endothelial cell angiogenesis or apoptosis, but the protein exhibits immunomodulatory activity. In particular, IrSPI represses proliferation of CD4⁺ T lymphocytes and proinflammatory cytokine secretion from both splenocytes and macrophages. Our study contributes valuable knowledge to tick-host interactions and provides insights that could be further exploited to design anti-tick vaccines targeting this immunomodulator implicated in I. ricinus feeding. View Full-Text

Keywords: Ixodes ricinus; tick–host–pathogen interactions; anti-tick vaccine; serine protease inhibitor; immunomodulator; macrophages; lymphocytes

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MDPI and ACS Style

Blisnick, A.A.; Šimo, L.; Grillon, C.; Fasani, F.; Brûlé, S.; Le Bonniec, B.; Prina, E.; Marsot, M.; Relmy, A.; Blaise-Boisseau, S.; Richardson, J.; Bonnet, S.I. The Immunomodulatory Effect of IrSPI, a Tick Salivary Gland Serine Protease Inhibitor Involved in Ixodes ricinus Tick Feeding. Vaccines 2019, 7, 148. https://doi.org/10.3390/vaccines7040148

AMA Style

Blisnick AA, Šimo L, Grillon C, Fasani F, Brûlé S, Le Bonniec B, Prina E, Marsot M, Relmy A, Blaise-Boisseau S, Richardson J, Bonnet SI. The Immunomodulatory Effect of IrSPI, a Tick Salivary Gland Serine Protease Inhibitor Involved in Ixodes ricinus Tick Feeding. Vaccines. 2019; 7(4):148. https://doi.org/10.3390/vaccines7040148

Chicago/Turabian Style

Blisnick, Adrien A., Ladislav Šimo, Catherine Grillon, Fabienne Fasani, Sébastien Brûlé, Bernard Le Bonniec, Eric Prina, Maud Marsot, Anthony Relmy, Sandra Blaise-Boisseau, Jennifer Richardson, and Sarah I. Bonnet. 2019. "The Immunomodulatory Effect of IrSPI, a Tick Salivary Gland Serine Protease Inhibitor Involved in Ixodes ricinus Tick Feeding" Vaccines 7, no. 4: 148. https://doi.org/10.3390/vaccines7040148

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