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Trypanosoma cruzi Parasite Load Modulates the Circadian Activity Pattern of Triatoma infestans.

ABSTRACT: American trypanosomiasis is a disease caused by the flagellate protozoan Trypanosoma cruzi, which is transmitted mainly in endemic areas by blood-sucking triatomine vectors. Triatoma infestans is the most important vector in the southern cone of South America, exhibiting a nocturnal host-seeking behavior. It has been previously documented that the parasite produces changes in some triatomine species, but this is the first time that the behavior of a vector has been evaluated in relation to its parasite load. After comparing the movement events and distance traveled of infected and non-infected T. infestans, we evaluated the change produced by different T. cruzi parasite loads on its circadian locomotor activity. We observed differences between infected and non-infected triatomines, and a significant relation between the parasite load and the increase in locomotor activity of T. infestans, which was accentuated during the photophase. This could have direct implications on the transmission of T. cruzi, as the increased movement and distance traveled could enhance the contact of the vector with the host, while increasing the predation risk for the vector, which could both constitute a risk for vectorial and oral transmission to mammals.

SUBMITTER: Chacon F

PROVIDER: S-EPMC8777832 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundTrypanosoma cruzi, the agent of Chagas disease, is a protozoan parasite transmitted to humans by blood-sucking triatomine vectors. However, and despite its utmost biological and epidemiological relevance, T. cruzi development inside the digestive tract of the insect remains a poorly understood process.Methods/principle findingsHere we showed that Gp35/50 kDa mucins, the major surface glycoproteins from T. cruzi insect-dwelling forms, are involved in parasite attachment to the internal cuticle of the triatomine rectal ampoule, a critical step leading to its differentiation into mammal-infective forms. Experimental evidence supporting this conclusion could be summarized as follows: i) native and recombinant Gp35/50 kDa mucins directly interacted with hindgut tissues from Triatoma infestans, as assessed by indirect immunofluorescence assays; ii) transgenic epimastigotes over-expressing Gp35/50 kDa mucins on their surface coat exhibited improved attachment rates (~2-3 fold) to such tissues as compared to appropriate transgenic controls and/or wild-type counterparts; and iii) certain chemically synthesized compounds derived from Gp35/50 kDa mucins were able to specifically interfere with epimastigote attachment to the inner lining of T. infestans rectal ampoules in ex vivo binding assays, most likely by competing with or directly blocking insect receptor(s). A solvent-exposed peptide (smugS peptide) from the Gp35/50 kDa mucins protein scaffolds and a branched, Galf-containing trisaccharide (Galfβ1-4[Galpβ1-6]GlcNAcα) from their O-linked glycans were identified as main adhesion determinants for these molecules. Interestingly, exogenous addition of a synthetic Galfβ1-4[Galpβ1-6]GlcNAcα derivative or of oligosaccharides containing this structure impaired the attachment of Dm28c but not of CL Brener epimastigotes to triatomine hindgut tissues; which correlates with the presence of Galf residues on the Gp35/50 kDa mucins' O-glycans on the former but not the latter parasite clone.Conclusion/significanceThese results provide novel insights into the mechanisms underlying T. cruzi-triatomine interplay, and indicate that inter-strain variations in the O-glycosylation of Gp35/50 kDa mucins may lead to differences in parasite differentiation and hence, in parasite transmissibility to the mammalian host. Most importantly, our findings point to Gp35/50 kDa mucins and/or the Galf biosynthetic pathway, which is absent in mammals and insects, as appealing targets for the development of T. cruzi transmission-blocking strategies.

Project description:BackgroundTriatomine elimination efforts and the interruption of domestic transmission of Trypanosoma cruzi are hampered by pyrethroid resistance. Fluralaner, a long-lasting ectoparasiticide administered to dogs, substantially reduced site infestation and abundance of pyrethroid-resistant Triatoma infestans Klug (Heteroptera: Reduviidae) in an ongoing 10-month trial in Castelli (Chaco Province, Argentina). We assessed the effects of fluralaner on vector infection with T. cruzi and blood meal sources stratified by ecotope and quantified its medium-term effects on site infestation and triatomine abundance.MethodsWe conducted a placebo-controlled, before-and-after efficacy trial of fluralaner in 28 infested sites over a 22-month period. All dogs received either an oral dose of fluralaner (treated group) or placebo (control group) at 0 month post-treatment [MPT]. Placebo-treated dogs were rescue-treated with fluralaner at 1 MPT, as were all eligible dogs at 7 MPT. Site-level infestation and abundance were periodically assessed by timed manual searches with a dislodging aerosol. Vector infection was mainly determined by kDNA-PCR and blood meal sources were determined by enzyme-linked immunosorbent assay.ResultsIn fluralaner-treated households, site infestation dropped from 100% at 0 MPT to 18-19% over the period 6-22 MPT while mean abundance plummeted from 5.5 to 0.6 triatomines per unit effort. In control households, infestation dropped similarly post-treatment. The overall prevalence of T. cruzi infection steadily decreased from 13.8% at 0-1 MPT (baseline) to 6.4% and subsequently 2.3% thereafter, while in domiciles, kitchens and storerooms it dropped from 17.4% to 4.7% and subsequently 3.3% thereafter. Most infected triatomines occurred in domiciles and had fed on humans. Infected-bug abundance plummeted after fluralaner treatment and remained marginal or nil thereafter. The human blood index of triatomines collected in domiciles, kitchens and storerooms highly significantly fell from 42.9% at baseline to 5.3-9.1% over the period 6-10 MPT, increasing to 36.8% at 22 MPT. Dog blood meals occurred before fluralaner administration only. The cat blood index increased from 9.9% at baseline to 57.9-72.7% over the period 6-10 MPT and dropped to 5.3% at 22 MPT, whereas chicken blood meals rose from 39.6% to 63.2-88.6%.ConclusionFluralaner severely impacted infestation- and transmission-related indices over nearly 2 years, causing evident effects at 1 MPT, and deserves larger efficacy trials.

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Trypanosoma cruzi Parasite Load Modulates the Circadian Activity Pattern of Triatoma infestans.

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