Abstract
The interaction between Rhodnius prolixus and Trypanosoma cruzi has huge medical importance because it responds to the transmission of Chagas disease, a neglected tropical disease that affects about eight million people worldwide. It is known that trypanosomatid pathogens depend on active lipid endocytosis from the insect host to meet growth and differentiation requirements. However, until now, knowledge on how the parasite affects the lipid physiology of individual insect organs was largely unknown. Herein, the biochemical and molecular dynamics of the triatomine R. prolixus lipid metabolism in response to T. cruzi acute infection were investigated. A qRT-PCR approach was used to determine the expression profile of 12 protein-coding genes involved in R. prolixus lipid physiology. In addition, microscopic and biochemical assays revealed the lipid droplet profile and the levels of the different identified lipid classes. Finally, spectrometry analyses were used to determine fatty acid and sterol composition and their modulation towards the infection. T. cruzi infection downregulated the transcript levels of protein-coding genes for lipid biosynthetic and degrading pathways in individual triatomine organs. On the other hand, upregulation of lipid receptor transcripts indicates an attempt to capture more lipids from hemolymphatic lipoproteins. Consequently, several lipid classes (such as monoacylglycerol, diacylglycerol, triacylglycerol, cholesteryl ester, phosphatidylcholine, and phosphatidylethanolamine) were involved in the response to the parasite challenge, although modulating only the insect fat body. T. cruzi never leaves the insect gut and yet it modulates non-infected tissues, suggesting that the association between the parasite and the vector organs is reached by cell signaling molecules. This hypothesis raises several intriguing issues to inspire future studies in the parasite-vector interaction field.
Highlights
Insects are vectors of the most prevalent human diseases
The Low-Density Lipoprotein Receptors (LDLR) family has as a defining structural characteristic the presence of an ectodomain containing three types of protein modules: LDL receptor type A (LA), Epidermal Growth factor (EGF), and LDL receptor type B (LY – containing the YWTD motif) modules [35]
The protein encoded by the RPRC011390 gene exhibited 67% identity against the lipophorin receptor from Locusta migratoria (e-value 0.0, coverage 95%), presenting the unique set of sequence motifs of the C-terminal domains that characterize insect Lp receptor (LpR) [36]
Summary
About eight million people worldwide are estimated to be affected by Chagas disease in Latin America, where this neglected tropical disease remains a major social and health problem [1] Triatomine bugs, such as Rhodnius prolixus (Insecta: Hemiptera), are hematophagous insects and play a role in the transmission of Trypanosoma cruzi parasites, the causative agent of Chagas disease, during the ingestion of the blood meal. In addition to the blood-feeding, lipids can be produced by non-lipid substrates through de novo FA synthesis This metabolic pathway requires the consecutive action of two enzymes. Cholesterol (CO) and cholesteryl ester (CE) derivatives are remarkably important, and not synthesized by trypanosomatids, being constantly acquired through the uptake of host lipoproteins [21, 22] Both male and female hematophagous Hemiptera feed on blood, presenting the same potential as vector insects. The success of R. prolixus and T. cruzi interaction appears to be reached by cell signaling molecules that communicate the parasite retained in the closed gut environment with other insect organs
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