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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 | 2022 Jan

REPOSITORIES: biostudies-literature

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

Chacón Francisco F Muñoz-San Martín Catalina C Bacigalupo Antonella A Álvarez-Duhart Bárbara B Solís Rigoberto R Cattan Pedro E PE

Insects 20220110 1

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 rel ...[more]

PMID: 35055920

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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:BackgroundVector infection prevalence is a key component of vectorial capacity and transmission risk. Optical microscopy observation (OM) of fecal drops has been the classic method for detecting Trypanosoma cruzi infection in triatomine bugs until the advent of polymerase chain reaction (PCR)-based techniques. However, agreement among OM- and PCR-based techniques has been highly heterogeneous.MethodsWe used hierarchical site-occupancy models accounting for imperfect detection to estimate method-specific detection probabilities of T. cruzi infection in field-collected Triatoma infestans and to assess whether T. cruzi infection varied with triatomine developmental stage and collection ecotope. We also performed a scoping review of the literature on comparisons between OM and PCR for T. cruzi infection diagnosis in triatomines. Triatomines were collected before vector control interventions in Pampa del Indio houses (Argentine Chaco) and examined by OM. We amplified the variable regions of the kinetoplastid minicircle genome (vkDNA-PCR) in DNA extracted from the rectal ampoules of 64 OM-positive and 65 OM-negative T. infestans.ResultsvkDNA-PCR detected T. cruzi infection in 59 (92.2%) OM-positive bugs and in 19 (29.2%) OM-negative triatomines in blind tests. The overall prevalence of infection, as determined by a positive test result by either vkDNA-PCR or OM, was 64.3% [95% confidence interval (95% CI) 55.8-72.1%]. Detection probability of T. cruzi infection by vkDNA-PCR (92%, 95% CI 83-97%) was substantially higher than for OM (76%, 95% CI 65-84%). Infection was minimal (26.2%) in peridomestic nymphs and maximal in domestic adult triatomines (81.7%). In the literature review encompassing 26 triatomine species from 11 countries, inter-method agreement ranged from 28.6% to 100%. The lowest agreement was observed in Rhodnius sp. and Panstrongylus lutzi and the highest among Triatoma sp., with wide variability in the protocols and outcomes of molecular diagnosis in comparison with OM.ConclusionsOur study provides a synthesis on the different sources (both biological and technical) of variation of the outcomes of OM- and PCR-based diagnosis of T. cruzi infection in triatomines and identifies new research needs for diagnostic improvement.

Dataset Information

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

Publications

<i>Trypanosoma cruzi</i> Parasite Load Modulates the Circadian Activity Pattern of <i>Triatoma infestans</i>.

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