Early Post-Prandial Regulation of Protein Expression in the Midgut of Chagas Disease Vector Rhodnius prolixus Highlights New Potential Targets for Vector Control Strategy

Chagas disease is a vector-borne parasitic disease caused by the flagellated protozoan Trypanosoma cruzi and transmitted to humans by a large group of bloodsucking triatomine bugs. Triatomine insects, such as Rhodnius prolixus, ingest a huge amount of blood in a single meal. Their midgut represents an important interface for triatomine–trypanosome interactions. Furthermore, the development of parasites and their vectorial transmission are closely linked to the blood feeding and digestion; thus, an understanding of their physiology is essential for the development of new strategies to control triatomines. In this study, we used label-free quantitative proteomics to identify and analyze the early effect of blood feeding on protein expression in the midgut of Rhodnius prolixus. We both identified and quantified 124 proteins in the anterior midgut (AM) and 40 in the posterior midgut (PM), which vary significantly 6 h after feeding. The detailed analysis of these proteins revealed their predominant involvement in the primary function of hematophagy, including proteases, proteases inhibitors, amino acids metabolism, primary metabolites processing, and protein folding. Interestingly, our proteomics data show a potential role of the AM in protein digestion. Moreover, proteins related to detoxification processes and innate immunity, which are largely accepted to be triggered by blood ingestion, were mildly modulated. Surprisingly, one third of blood-regulated proteins in the AM have unknown function. This work contributes to the improvement of knowledge on the digestive physiology of triatomines in the early hours post-feeding. It provides key information for selecting new putative targets for the development of triatomine control tools and their potential role in the vector competence, which could be applied to other vector species.

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Ultrastructural changes in posterior midgut cells associated with blood feeding in adult female Rhodnius prolixus Stal (Hemiptera: Reduviidae)

Canadian Journal of Zoology ◽

10.1139/z83-339 ◽

1983 ◽

Vol 61 (11) ◽

pp. 2574-2586 ◽

Cited By ~ 57

Author(s):

P. F. Billingsley ◽

A. E. R. Downe

Keyword(s):

Endoplasmic Reticulum ◽

Rough Endoplasmic Reticulum ◽

Blood Meal ◽

Apical Cell ◽

Blood Feeding ◽

Rhodnius Prolixus ◽

Ultrastructural Changes ◽

Dense Matrix ◽

Apical Surface ◽

Posterior Midgut

Modifications of posterior midgut cells of Rhodnius prolixus following a meal of rabbit blood are described. Prominent stacks and whorls of rough endoplasmic reticulum become redistributed following a blood meal but later reform during the postfeeding period. Lysosomes undergo internal structural changes and apparent fluctuations in their number per cell as a result of blood meal ingestion. Before blood feeding, the apical surface of the midgut cells show a typical arrangement of a plasma membrane covered on the lumenal surface by a glycocalyx. After a blood meal, a more complex organisation appears, consisting of two plasma membranes separated by an electron-dense matrix. The lumenal apical membrane proliferates during the digestion period to form loosely organised extracellular membrane layers which may function as a peritrophic membrane. Changes in the rough endoplasmic reticulum and lysosomes and modifications to the apical cell surface appear to coincide with previously described proteinase activity cycles in the posterior midgut of R. prolixus. The implications of these results are discussed and are compared with similar ultrastructural events from haematophagous Diptera.

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Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1506226112 ◽

2015 ◽

Vol 112 (48) ◽

pp. 14936-14941 ◽

Cited By ~ 167

Author(s):

Rafael D. Mesquita ◽

Raquel J. Vionette-Amaral ◽

Carl Lowenberger ◽

Rolando Rivera-Pomar ◽

Fernando A. Monteiro ◽

...

Keyword(s):

Chagas Disease ◽

Model Organism ◽

Blood Feeding ◽

Rhodnius Prolixus ◽

Insect Vector ◽

Protein Coding ◽

Putative Gene ◽

Imd Pathway ◽

Genomic Analyses ◽

Codon Use

Rhodnius prolixus not only has served as a model organism for the study of insect physiology, but also is a major vector of Chagas disease, an illness that affects approximately seven million people worldwide. We sequenced the genome of R. prolixus, generated assembled sequences covering 95% of the genome (∼702 Mb), including 15,456 putative protein-coding genes, and completed comprehensive genomic analyses of this obligate blood-feeding insect. Although immune-deficiency (IMD)-mediated immune responses were observed, R. prolixus putatively lacks key components of the IMD pathway, suggesting a reorganization of the canonical immune signaling network. Although both Toll and IMD effectors controlled intestinal microbiota, neither affected Trypanosoma cruzi, the causal agent of Chagas disease, implying the existence of evasion or tolerance mechanisms. R. prolixus has experienced an extensive loss of selenoprotein genes, with its repertoire reduced to only two proteins, one of which is a selenocysteine-based glutathione peroxidase, the first found in insects. The genome contained actively transcribed, horizontally transferred genes from Wolbachia sp., which showed evidence of codon use evolution toward the insect use pattern. Comparative protein analyses revealed many lineage-specific expansions and putative gene absences in R. prolixus, including tandem expansions of genes related to chemoreception, feeding, and digestion that possibly contributed to the evolution of a blood-feeding lifestyle. The genome assembly and these associated analyses provide critical information on the physiology and evolution of this important vector species and should be instrumental for the development of innovative disease control methods.

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Colonization of Rhodnius prolixus gut by Trypanosoma cruzi involves an extensive parasite killing

Parasitology ◽

10.1017/s0031182015001857 ◽

2016 ◽

Vol 143 (4) ◽

pp. 434-443 ◽

Cited By ~ 29

Author(s):

ROBERTA CARVALHO FERREIRA ◽

RAFAEL LUIS KESSLER ◽

MARCELO GUSTAVO LORENZO ◽

RAFAELA MAGALHÃES MACEDO PAIM ◽

LUCIANA DE LIMA FERREIRA ◽

...

Keyword(s):

Trypanosoma Cruzi ◽

Population Size ◽

Chagas Disease ◽

Intestinal Tract ◽

Parasite Load ◽

Rhodnius Prolixus ◽

Insect Vector ◽

Posterior Midgut ◽

Development And Differentiation ◽

Anterior Midgut

SUMMARYTrypanosoma cruzi, the etiological agent of Chagas disease, is ingested by triatomines during their bloodmeal on an infected mammal. Aiming to investigate the development and differentiation of T. cruzi inside the intestinal tract of Rhodnius prolixus at the beginning of infection we fed insects with cultured epimastigotes and blood trypomastigotes from infected mice to determine the amount of recovered parasites after ingestion. Approximately 20% of the ingested parasites was found in the insect anterior midgut (AM) 3 h after feeding. Interestingly, a significant reduction (80%) in the numbers of trypomastigotes was observed after 24 h of infection suggesting that parasites were killed in the AM. Moreover, few parasites were found in that intestinal portion after 96 h of infection. The evaluation of the numbers of parasites in the posterior midgut (PM) at the same periods showed a reduced parasite load, indicating that parasites were not moving from the AM. Additionally, incubation of blood trypomastigotes with extracts from R. prolixus AMs revealed that components of this tissue could induce significant death of T. cruzi. Finally, we observed that differentiation from trypomastigotes to epimastigotes is not completed in the AM; instead we suggest that trypomastigotes change to intermediary forms before their migration to the PM, where differentiation to epimastigotes takes place. The present work clarifies controversial points concerning T. cruzi development in insect vector, showing that parasite suffers a drastic decrease in population size before epimastigonesis accomplishment in PM.

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Potential role of CD4+CD25HIGH regulatory T cells in morbidity in Chagas disease

Frontiers in Bioscience ◽

10.2741/2273 ◽

2007 ◽

Vol 12 (1) ◽

pp. 2797 ◽

Cited By ~ 49

Author(s):

Fernanda Fortes Araujo

Keyword(s):

T Cells ◽

Regulatory T Cells ◽

Chagas Disease ◽

Potential Role

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Silencing the odorant receptor co-receptor RproOrco affects the physiology and behavior of the Chagas disease vector Rhodnius prolixus

Insect Biochemistry and Molecular Biology ◽

10.1016/j.ibmb.2015.02.012 ◽

2016 ◽

Vol 69 ◽

pp. 82-90 ◽

Cited By ~ 27

Author(s):

Thiago A. Franco ◽

Daniele S. Oliveira ◽

Monica F. Moreira ◽

Walter S. Leal ◽

Ana C.A. Melo

Keyword(s):

Chagas Disease ◽

Odorant Receptor ◽

Rhodnius Prolixus ◽

Disease Vector ◽

And Behavior

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Experimental Infection of Amblyomma americanum (Acari: Ixodidae) With Bourbon Virus (Orthomyxoviridae: Thogotovirus)

Journal of Medical Entomology ◽

10.1093/jme/tjaa191 ◽

2020 ◽

Author(s):

Marvin S Godsey ◽

Dominic Rose ◽

Kristin L Burkhalter ◽

Nicole Breuner ◽

Angela M Bosco-Lauth ◽

...

Keyword(s):

Infectious Virus ◽

Vector Competence ◽

Blood Feeding ◽

Human Case ◽

Amblyomma Americanum ◽

Live Virus ◽

Active Life ◽

Series Of Experiments ◽

Transstadial Transmission ◽

Very High

Abstract Following the recent discovery of Bourbon virus (BRBV) as a human pathogen, and the isolation of the virus from Amblyomma americanum (L.) collected near the location of a fatal human case, we undertook a series of experiments to assess the laboratory vector competence of this tick species for BRBV. Larval ticks were infected using an immersion technique, and transstadial transmission of virus to the nymphal and then to the adult stages was demonstrated. Transstadially infected nymphs transmitted virus to adult ticks at very high rates during cofeeding, indicating the presence of infectious virus in the saliva of engorging ticks. Vertical transmission by transstadially infected females to their progeny occurred, but at a low rate. Rabbits fed on by infected ticks of all active life stages developed high titers of antibody to the virus, demonstrating host exposure to BRBV antigens/live virus during tick blood feeding. These results demonstrate that A. americanum is a competent vector of BRBV and indicate that cofeeding could be critical for enzootic maintenance.

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