Dataset Information

Serine Protease Inhibitors in Ticks: An Overview of Their Role in Tick Biology and Tick-Borne Pathogen Transmission.

ABSTRACT: New tick and tick-borne pathogen control approaches that are both environmentally sustainable and which provide broad protection are urgently needed. Their development, however, will rely on a greater understanding of tick biology, tick-pathogen, and tick-host interactions. The recent advances in new generation technologies to study genomes, transcriptomes, and proteomes has resulted in a plethora of tick biomacromolecular studies. Among these, many enzyme inhibitors have been described, notably serine protease inhibitors (SPIs), whose importance in various tick biological processes is only just beginning to be fully appreciated. Among the multiple active substances secreted during tick feeding, SPIs have been shown to be directly involved in regulation of inflammation, blood clotting, wound healing, vasoconstriction and the modulation of host defense mechanisms. In light of these activities, several SPIs were examined and were experimentally confirmed to facilitate tick pathogen transmission. In addition, to prevent coagulation of the ingested blood meal within the tick alimentary canal, SPIs are also involved in blood digestion and nutrient extraction from the meal. The presence of SPIs in tick hemocytes and their involvement in tick innate immune defenses have also been demonstrated, as well as their implication in hemolymph coagulation and egg development. Considering the involvement of SPIs in multiple crucial aspects of tick-host-pathogen interactions, as well as in various aspects of the tick parasitic lifestyle, these molecules represent highly suitable and attractive targets for the development of effective tick control strategies. Here we review the current knowledge regarding this class of inhibitors in tick biology and tick-borne pathogen transmission, and their potential as targets for future tick control trials.

SUBMITTER: Blisnick AA

PROVIDER: S-EPMC5438962 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Serine Protease Inhibitors in Ticks: An Overview of Their Role in Tick Biology and Tick-Borne Pathogen Transmission.

Blisnick Adrien A AA Foulon Thierry T Bonnet Sarah I SI

Frontiers in cellular and infection microbiology 20170522

New tick and tick-borne pathogen control approaches that are both environmentally sustainable and which provide broad protection are urgently needed. Their development, however, will rely on a greater understanding of tick biology, tick-pathogen, and tick-host interactions. The recent advances in new generation technologies to study genomes, transcriptomes, and proteomes has resulted in a plethora of tick biomacromolecular studies. Among these, many enzyme inhibitors have been described, notably ...[more]

PMID: 28589099

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Project description:BackgroundThe majority of vector-borne infections occur in the tropics, including Africa, but molecular eco-epidemiological studies are seldom reported from these regions. In particular, most previously published data on ticks in Ethiopia focus on species distribution, and only a few molecular studies on the occurrence of tick-borne pathogens or on ecological factors influencing these. The present study was undertaken to evaluate, if ticks collected from cattle in different Ethiopian biotopes harbour (had access to) different pathogens.MethodsIn South-Western Ethiopia 1032 hard ticks were removed from cattle grazing in three kinds of tick biotopes. DNA was individually extracted from one specimen of both sexes of each tick species per cattle. These samples were molecularly analysed for the presence of tick-borne pathogens.ResultsAmblyomma variegatum was significantly more abundant on mid highland, than on moist highland. Rhipicephalus decoloratus was absent from savannah lowland, where virtually only A. cohaerens was found. In the ticks Coxiella burnetii had the highest prevalence on savannah lowland. PCR positivity to Theileria spp. did not appear to depend on the biotope, but some genotypes were unique to certain tick species. Significantly more A. variegatum specimens were rickettsia-positive, than those of other tick species. The presence of rickettsiae (R. africae) appeared to be associated with mid highland in case of A. variegatum and A. cohaerens. The low level of haemoplasma positivity seemed to be equally distributed among the tick species, but was restricted to one biotope type.ConclusionsThe tick biotope, in which cattle are grazed, will influence not only the tick burden of these hosts, but also the spectrum of pathogens in their ticks. Thus, the presence of pathogens with alternative (non-tick-borne) transmission routes, with transstadial or with transovarial transmission by ticks appeared to be associated with the biotope type, with the tick species, or both, respectively.

Project description:Serine protease inhibitors (serpins) are a diverse family of proteins that is conserved across taxa. The diversity of Amblyomma americanum serpins (AAS) is far more complex than previously thought as revealed by discovery of 57 and 33 AAS transcripts that are respectively expressed in male and female A. americanum ticks, with 30 found in both. While distinct reproductively, both male and female metastriate ticks, such as A. americanum, require a blood meal. Thus, 30 AAS sequences found in both male and female ticks could play important role(s) in regulating tick feeding and thus represent attractive candidates for anti-tick vaccine development. Of significant interest, 19 AAS sequences expressed in male and female ticks are also part of the 48 AAS sequences expressed in fed female tick salivary glands or midguts; two organs through which the tick interacts with host blood and immune response factors. Considered the most important domain for serpin function, the reactive center loop (RCL) is further characterized by a single 'P1' site amino acid residue, which is central to determining the protease regulated by the serpin. In this study, a diversity of 17 different P1 site amino acid residues were predicted, suggesting that A. americanum serpins potentially regulate a large number of proteolytic pathways. Our data also indicate that some serpins in this study could regulate target protease common to all tick species, in that more than 40% of AAS show 58-97% inter-species amino acid conservation. Of significance, 24% of AAS showed 62-100% inter-species conservation within the functional RCL domain, with 10 RCLs showing ?90-100% conservation. In vertebrates, serpins with basic residues at the P1 site regulate key host defense pathways, which the tick must evade to feed successfully. Interestingly, we found that AAS sequences with basic or polar uncharged residues at the putative P1 site are more likely to be conserved across tick species. Another notable observation from our data is that AAS sequences found only in female ticks and those found in both males and females, but not those found only in male ticks, were highly conserved in other tick species. While descriptive, this study provides the basis for more in-depth studies exploring the roles of serpins in tick feeding physiology.

Project description:BackgroundElucidating which wildlife species significantly contribute to the maintenance of Ixodes ricinus populations and the enzootic cycles of the pathogens they transmit is imperative in understanding the driving forces behind the emergence of tick-borne diseases. Here, we aimed to quantify the relative contribution of four mustelid species in the life-cycles of I. ricinus and Borrelia burgdorferi (sensu lato) in forested areas and to investigate their role in the transmission of other tick-borne pathogens. Road-killed badgers, pine martens, stone martens and polecats were collected in Belgium and the Netherlands. Their organs and feeding ticks were tested for the presence of tick-borne pathogens.ResultsIxodes hexagonus and I. ricinus were found on half of the screened animals (n = 637). Pine martens had the highest I. ricinus burden, whereas polecats had the highest I. hexagonus burden. We detected DNA from B. burgdorferi (s.l.) and Anaplasma phagocytophilum in organs of all four mustelid species (n = 789), and Neoehrlichia mikurensis DNA was detected in all species, except badgers. DNA from B. miyamotoi was not detected in any of the investigated mustelids. From the 15 larvae of I. ricinus feeding on pine martens (n = 44), only one was positive for B. miyamotoi DNA, and all tested negative for B. burgdorferi (s.l.), N. mikurensis and A. phagocytophilum. The two feeding larvae from the investigated polecats (n = 364) and stone martens (n = 39) were negative for all four pathogens. The infection rate of N. mikurensis was higher in feeding nymphs collected from mustelids compared to questing nymphs, but not for B. burgdorferi (s.l.), B. miyamotoi or A. phagocytophilum.ConclusionsAlthough all stages of I. ricinus can be found on badgers, polecats, pine and stone martens, their relative contribution to the life-cycle of I. ricinus in forested areas is less than 1%. Consequently, the relative contribution of mustelids to the enzootic cycles of I. ricinus-borne pathogens is negligible, despite the presence of these pathogens in organs and feeding ticks. Interestingly, all four mustelid species carried all stages of I. hexagonus, potentially maintaining enzootic cycles of this tick species apart from the cycle involving hedgehogs as main host species.

Dataset Information

Serine Protease Inhibitors in Ticks: An Overview of Their Role in Tick Biology and Tick-Borne Pathogen Transmission.

Publications

Serine Protease Inhibitors in Ticks: An Overview of Their Role in Tick Biology and Tick-Borne Pathogen Transmission.

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