Abstract
Using the blood-sucking kissing bug, Rhodnius prolixus as an experimental model, we have studied the involvement of insulin-like peptides (ILPs) and adipokinetic hormone (AKH) signaling in carbohydrate metabolism, focusing on the regulation of the trehalose-specific facilitated transporter (Rhopr-TRET), particularly in the ovaries. We find that trehalose stores in ovaries increase after feeding, synchronously with the beginning of vitellogenesis, but that the transcript expression of enzymes involved in trehalose synthesis show no changes between unfed and blood-fed animals. However, an eightfold increase in Rhopr-TRET transcript expression is observed in the ovaries post-blood meal. In vivo and ex vivo assays using exogenous insulins and Rhopr-AKH, reveal that Rhopr-TRET is up-regulated in ovaries by both peptide families. In accordance with these results, when ILP and AKH signaling cascades are impaired using RNA interference, Rhopr-TRET transcript is down-regulated. In addition, trehalose injection induces an up-regulation of Rhopr-TRET transcript expression and suggests an activation of insulin signaling. Overall, the results support the hypothesis of a direct trehalose uptake by ovaries from the hemolymph through Rhopr-TRET, regulated by ILP and/or AKH. We also show that Rhopr-TRET may work cooperatively with AKH signaling to support the release of trehalose from the ovaries into the hemolymph during the unfed (starved) condition. In conclusion, the results indicate that in females of R. prolixus, trehalose metabolism and its hormonal regulation by ILP and AKH play critical roles in adapting to different nutritional conditions and physiological states.
Highlights
Carbohydrates represent one of the main energy reserves in animal cells, which is why they participate as essential factors in various biological processes of all multicellular organisms (Brosnan, 1999)
We demonstrate that Rhopr-trehalose-specific facilitated transporter (TRET) could work cooperatively with the R. prolixus adipokinetic hormone (AKH) (Rhopr-AKH) signaling pathway to promote the release of trehalose from the fat body and ovaries to the hemolymph during starvation
We used females at 10 days post-ecdysis for in vivo assays because (a) we previously demonstrated that unfed females of R. prolixus are in a sensitized state to respond to an increase of insulin-like peptides (ILPs) levels by rapidly activating ILP signaling (Leyria et al, 2020a), and (b) food deprivation is the main stimulus for the release of AKH, which works as a metabolic stimulator leading to both carbohydrate and lipid mobilization (Bednáøová et al, 2013; Alves-Bezerra et al, 2016) and, the tissues should be sensitized to respond rapidly to AKH stimulation
Summary
Carbohydrates represent one of the main energy reserves in animal cells, which is why they participate as essential factors in various biological processes of all multicellular organisms (Brosnan, 1999). Blood-sucking insects usually need to process a large amount of blood in a short time to provide energy to support the optimal progress of physiological events related to growth, development, and reproduction They often have to overcome long periods of starvation between successful gorging (Millen and Beckel, 1970; Foster, 1995). We demonstrate that Rhopr-TRET could work cooperatively with the R. prolixus AKH (Rhopr-AKH) signaling pathway to promote the release of trehalose from the fat body and ovaries to the hemolymph during starvation Overall, these results show that in R. prolixus, carbohydrate metabolism and its hormonal regulation may play critical roles in adapting to different physiological conditions, including reproduction and starvation
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