Abstract
Rhodnius prolixus is one important vector for the parasite Trypanosoma cruzi in Latin America, where Chagas disease is a significant health issue. Although R. prolixus is a model for investigations of vector–parasite interaction and transmission, not much has been done recently to further comprehend its protein digestion. In this work, gut proteolysis was characterized using new fluorogenic substrates, including optimum pH, inhibition profiles, and tissue and temporal expression patterns. Each protease possessed a particular tissue prevalence and activity cycle after feeding. Cathepsin L had a higher activity in the posterior midgut lumen, being characterized by a plateau of high activities during several days in the intermediate phase of digestion. Cathepsin D showed high activity levels in the tissue homogenates and in the luminal content of the posterior midgut, with a single peak 5 days after blood feeding. Aminopeptidases are highly associated with the midgut wall, where the highest activity is located. Assays with proteinaceous substrates as casein, hemoglobin, and serum albumin revealed different activity profiles, with some evidence of biphasic temporal proteolytic patterns. Cathepsin D genes are preferentially expressed in the anterior midgut, while cathepsin L genes are mainly located in the posterior portion of the midgut, with specific sets of genes being differently expressed in the initial, intermediate, or late phases of blood digestion.Significance StatementThis is the first description in a non-dipteran hematophagous species of a sequential protease secretion system based on midgut cathepsins instead of the most common insect digestive serine proteases (trypsins and chymotrypsins). The midgut of R. prolixus (Hemiptera) shows a different temporal expression of proteases in the initial, intermediate, and late stages of blood digestion. In this respect, a different timing in protease secretion may be an example of adaptative convergence in blood-sucking vectors from different orders. Expanding the knowledge about gut physiology in triatomine vectors may contribute to the development of new control strategies, aiming the blocking of parasite transmission.
Highlights
Rhodnius prolixus is an important vector of Trypanosoma cruzi, the etiological agent of Chagas disease that affects six to seven million people worldwide, mostly in Latin America (Coura, 2015)
The results provide evidences for the involvement of different proteases in the initial, intermediate or late stages of blood digestion and further the knowledge on the digestive physiology of R. prolixus
Gene C15 depicted a significantly higher expression in early digestion, and gene C16 gradually increased its relative expression, with a peak in the late digestion phase (Table 6). This is the first time that different pools of proteases involved in initial, intermediate, or late stages of blood digestion were described outside the order Diptera
Summary
Rhodnius prolixus (order Hemiptera, family Reduviidae, subfamily Triatominae) is an important vector of Trypanosoma cruzi, the etiological agent of Chagas disease that affects six to seven million people worldwide, mostly in Latin America (Coura, 2015). The use of lysosomal enzymes is thought to have risen after the hemipteran sap-sucking common ancestor lost its digestive serine proteases while adapting to sugar-rich food requiring little to no protein digestion (Terra and Ferreira, 2012). In this regard, these insects are supposed to have mobilized originally intracellular proteases to a secretory pathway in the evolutionary readaptation to other food sources, which required the regain of the ability to digest proteins (Terra and Ferreira, 2012)
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