Failed Disruption of Tick Feeding, Viability, and Molting after Immunization of Mice and Sheep with Recombinant Ixodes ricinus Salivary Proteins IrSPI and IrLip1.

Consuelo Almazán,Martine Cote,Nicolas Versillé,Jennifer Richardson,Sarah I Bonnet,Jennifer Maye,Sabine Rakotobe,Lisa Fourniol,Sandy Peltier,Jérémie Bornères,Ladislav Šimo

doi:10.3390/vaccines8030475

Abstract

To identify potential vaccine candidates against Ixodes ricinus and tick-borne pathogen transmission, we have previously sequenced the salivary gland transcriptomes of female ticks infected or not with Bartonella henselae. The hypothesized potential of both IrSPI (I. ricinus serine protease inhibitor) and IrLip1 (I. ricinus lipocalin 1) as protective antigens decreasing tick feeding and/or the transmission of tick-borne pathogens was based on their presumed involvement in dampening the host immune response to tick feeding. Vaccine endpoints included tick larval and nymphal mortality, feeding, and molting in mice and sheep. Whether the antigens were administered individually or in combination, the vaccination of mice or sheep elicited a potent antigen-specific antibody response. However, and contrary to our expectations, vaccination failed to afford protection against the infestation of mice and sheep by I. ricinus nymphs and larvae, respectively. Rather, vaccination with IrSPI and IrLip1 appeared to enhance tick engorgement and molting and decrease tick mortality. To the best of our knowledge, these observations represent the first report of induction of vaccine-mediated enhancement in relation to anti-tick vaccination.

Highlights

Worldwide, vector-borne diseases (VBD) account for more than 17% of all infectious diseases in humans, causing 1 billion cases and 1 million deaths per year [1]
In order to identify genes involved in either tick feeding or the vector competence of I. ricinus, we have previously identified transcripts induced in female tick salivary gland (SG) tissue in response to colonization by Bartonella henselae [28]
Tick mortality was evaluated according to the number of attached nymphs

Summary

Introduction

Vector-borne diseases (VBD) account for more than 17% of all infectious diseases in humans, causing 1 billion cases and 1 million deaths per year [1]. Vaccines 2020, 8, 475 the most prevalent TBD is Lyme borreliosis, with an estimated 85,000 cases each year [5], but many other zoonotic pathogens can be acquired by tick bites. In this last regard, recent transcriptomic studies using next-generation sequencing (NGS) techniques have led to the identification of several unexpected bacteria, viruses, and parasites in I. ricinus ticks from Eastern France, some of them representing potential pathogens for humans or animals [6,7,8]. The intensification of human and animal movements and socioeconomic and environmental changes have led to the redistribution of certain tick species—that is, an extension of seasonal transmission periods and geographical distribution, as well as the appearance of TBD in previously unaffected areas, highlighting the urgent need to find better methods of control [9,10,11,12]

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Conclusion