Abstract
Rhodnius prolixus expresses nitric oxide synthase (NOS) in the cytosol of the salivary gland (SG) cells. The NO produced is stored in the SG lumen bound to NO-carrier haemeproteins called nitrophorins (NPs). NPs bind tightly to NO in the acidic SG lumen, but release NO when the pH becomes high, e.g., at the host skin (pH~7.4). NO elicits potent and transient relaxation of vascular smooth muscle. Here, we investigated the role of salivary NO in the R. prolixus feeding behaviour and the salivary vasodilator activity of the host microcirculation. NOS knockdown in R. prolixus changed the SG colour, decreased the number of NO-loaded NPs and caused impairment of feeding performance. When salivary gland extracts (SGEs) were obtained from NOS- and NPs-knockdown insects and prepared in pH 5.0 solution and injected (i.v.) into mice via the tail vein, no vasodilation was observed, whereas SGEs from control insects caused long-term venodilation in the mouse skin. SGs disrupted directly in PBS (pH 7.4) containing BSA produced long-term vasodilation compared to the controls without BSA due to the possible formation of nitroso-albumin, suggesting that host serum albumin extends the NO half-life when NO is injected into the host skin by triatomine during their blood-feeding.
Highlights
The triatomine Rhodnius prolixus feeds on blood during all postembryonic stages
nitric oxide synthase (NOS) expression was observed in multiple organs suggesting that nitric oxide (NO) may perform different functions in various biological processes
NO activity have been associated with insect immune responses against pathogens, which can stimulate NOS expression in haemocytes and other insect organs[17,18]
Summary
The triatomine Rhodnius prolixus feeds on blood during all postembryonic stages. In addition to being an important vector of the protozoan parasite Trypanosoma cruzi, the etiological agent of Chagas’ disease, R. prolixus has been widely studied as a classical insect model. Saliva provides a wide and redundant repertoire of biomolecules with anti-haemostatic activities, such as anticoagulants, platelet aggregation inhibitors and vasodilators, which are capable of facilitating the blood meal[3]. Among several molecules already identified in R. prolixus and in the bed bug Cimex lectularius saliva, nitric oxide (NO) is important due to its vasodilator and antiplatelet activities[6]. In the R. prolixus salivary glands (SG), nitric oxide is reversibly bound to lipocalins called nitrophorins (NPs), which correspond to an abundant group of haemeproteins responsible for conferring the typical reddish colour of the SGs. NPs are NO-carrying haemeproteins that tightly bind NO in the low-pH environment of the salivary gland lumen (pH ≤ 6) and release NO when the pH increases, as occurs when saliva is secreted in the host skin, in which the pH is approximately 7.49. S-nitroso-albumin is the major S-nitrosothiol that circulates in plasma and probably acts as an NO reservoir, slowly releasing NO as the thiol concentration increases[13,14]
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