Bonnet, S. I. | Search bioRxiv

bioRxiv2023

The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review

The tick Ixodes ricinus is the most important vector species of infectious diseases in European France. Understanding its distribution, phenology, and host species use, along with the distribution and prevalence of associated pathogens at national scales is essential for developing prevention strategies. The aim of this paper is to provide a systematic map and narrative review of the existing knowledge on the eco-epidemiology of I. ricinus in France. Using literature published up to 2020, the present paper provides a distribution map for the species and a summary of environmental factors explaining observed geographical differences in phenology and temporal differences in abundance. The diversity of vertebrate host species used by this tick, along with their degree of infestation when available, are presented and discussed with respect to their potential contribution to the population dynamics of I. ricinus and the circulation of tick-borne zoonotic pathogens. Prevalence data of detected pathogens are summarised in different maps. Results from 187 identified references show that the species is present in most departments, but scarce under Mediterranean climate and in coastal habitats. Its phenology is generally bimodal with variations depending on climate. Abundance seems positively influenced by forest cover and host abundance. Rodents and ruminants are the most studied species groups, but the diversity of sampling protocols (e.g., location, season, exhaustivity of inspection) precluded direct comparisons between species groups. Data on pathogens are patchy, with most studies conducted near research units. Among pathogens, Borrelia burgdorferi sensu lato is the most searched for in ticks and seems more prevalent in north-eastern and central France. The review carried out here has made it possible to highlight the gaps in our knowledge of tick-host-pathogen interactions, their ecology and their distribution, and the need to address these gaps in order to optimize tick and tick-borne diseases prevention and control strategies.

ecology↗

bioRxiv2019

The immunomodulatory effect of IrSPI, a tick salivary gland serine protease inhibitor involved in Ixodes ricinus tick feeding

Ticks are strict hematophagous arthropods and are the most important vectors of pathogens affecting both domestic and wild animals worldwide. Moreover, they are second only to mosquitoes as vectors of human pathogens. Hard tick feeding is a slow process--taking up to several days for repletion prior to detachment--and necessitates extended control over the host response. The success of the feeding process depends upon injection of saliva by tick, which not only controls host haemostasis and wound healing, but also subverts the host immune response to avoid tick rejection during this long-lasting process. In turn, the manipulation of the host immune response creates a favourable niche for the survival and propagation of diverse tick-borne pathogens transmitted during feeding. Here, we report on the molecular and biochemical features and functions of IrSPI, an Ixodes ricinus salivary serine protease inhibitor involved in blood meal acquisition. Our results show that IrSPI harbours the typical conformational fold of Kunitz type I serine protease inhibitors and that it functionally inhibits the elastase and, to a lesser extent, chymotrypsin. We also show that IrSPI is injected into the host during feeding. Crucially, we found that IrSPI has no impact on tissue factor pathway-induced coagulation, fibrinolysis, apoptosis, or angiogenesis, but a strong effect on immune cells. IrSPI affects antigen-presenting macrophages by hampering IL-5 production. In addition, IrSPI represses proliferation of mitogen-stimulated CD4+ cells. The inhibition of T cell proliferation was associated with marked reductions in pro-inflammatory cytokine secretion. 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 successful I. ricinus tick feeding.\n\nAuthor summaryTicks are the most important vector influencing both human and animal health in Europe, where Ixodes ricinus is the most abundant tick species. Ticks feed on animal or human blood for an extended period, during which their saliva allows both feeding and pathogen transmission by interfering with native host responses. A better understanding of tick-host-pathogen interactions is central to the discovery of improved control methods. Within this context, we previously identified IrSPI as an I. ricinus salivary molecule implicated in both tick feeding and bacterial transmission. This serine protease inhibitor was almost characterised as an elastase inhibitor, and here, we show IrSPI overexpression in several tick organs--especially salivary glands--during blood feeding. We demonstrate that IrSPI is injected into the host through saliva, and despite having no impact on endothelial cell angiogenesis or apoptosis during blood feeding, we report an immunomodulatory role, whereby CD4+ T lymphocyte proliferation is repressed and where the cytokine secretion pattern of both splenocytes and macrophages is modified. Our study provides new insights into the complex armament developed by ticks to overcome the host response, and uncovers a potential vaccine target for disruption of feeding processes and pathogen transmission.

animal behavior and cognition↗