The time spent engorging blood was similar for mosquitoes treated with dsGFP or dsLIPS (right) (F(2,76) = 0.6828, p = 0.5083). dsLIPS-injected females spent longer time searching under the skin for a blood vessel (center) (Welch’s ANOVA W(2,53) = 45.59, p < 0.0001 Dunnett’s T3 multiple comparison: dsLIPS1+dsLIPS2 versus dsGFP, p < 0.0001 dsLIPS2 versus dsGFP, p < 0.0001). Females injected with dsLIPS showed increased feeding time (F(2, 76) = 8.297 p = 0.0006 Tukey’s multiple comparison: dsLIPS1 + dsLIPS2 versus dsGFP, p = 0.0016 dsLIPS2 versus dsGFP, p = 0.0017). Before applying a statistical analysis for hypothesis testing, the data have been log 10-transformed because raw data were not normally distributed, and the new log-transformed data have been used for subsequent analysis and presented in the graph. After 3 days (on day 4), the ability of females to feed has been tested by measuring the time spent in feeding (left). albopictus females have been injected with dsRNA-matching GFP as control ( dsGFP, light blue) or LIPS-1 and LIPS-2 ( dsLIPS- 1 + dsLIPS- 2, orange dsLIPS-2, green) soon after emergence from pupal case. Gray boxes have been also used in the column showing the tissue-specific expression because some of the genes (such as apyrase) are heavily overexpressed in the female salivary glands, but their expression is not exactly restricted to this tissue. In the case of SGE analysis, some of the proteins have been identified in the SGE from 1-day-old females, and the boxes are colored in gray. The boxes are blue when the protein has been identified either in the extracts (SGE) and/or in the expectorated saliva, if homologous proteins have been reported in the Aedes aegypti saliva, if the expression of its gene is restricted to the female salivary glands at adult stage, if the protein has been previously recognized as immunogen and/or as a possible allergen and if the function of the protein has been characterized or suggested. (C) List of the identified proteins in either saliva or salivary glands homogenates derived from the LC-MS/MS analysis coupled with the available information from literature. Results LIPS are prominent factors in the Aedes female saliva Furthermore, our study deepens the knowledge of the feeding mechanism in mosquitoes, opening new ways to target and alter the mosquito feeding process. These findings point at the multifunctional role of mosquito saliva and of the mouth’s cuticle, which is not merely an external exoskeleton forming strong structures, allowing the insect, for example, to feed or sting, but it is also a site of key molecular interactions governing the animal biology. We found that the LIPS-2:Cp19 interaction induces a change in the morphology of the cuticle and affects mosquito intradermal probing before blood engorgement. We demonstrate that a salivary protein secreted during the initial phases of the biting process, which we named labrum-interacting protein of the saliva 2 (LIPS-2), directly interacts with a cuticular protein at the tip of the labrum (Cp19). In this study, we show that saliva components can establish a feedback mechanism in Aedes mosquitoes through protein-protein interactions occurring at the tip of the labrum. Our study identifies an additional role of mosquito saliva and underlines that the external cuticle is a possible site of key molecular interactions affecting the insect biology and its vector competence. Upon interaction, the morphology of the labral cuticle changes, and this modification is most likely sensed by proprioceptive neurons. The N-terminal domain interacts with a cuticular protein (Cp19) located at the tip of the mosquito labrum. LIPS show a new all-helical protein fold constituted by two domains. We identified LIPS proteins in the saliva of Aedes mosquitoes that promote feeding in the vertebrate skin. Here, we describe the initial trigger of an unprecedented feedback signaling pathway in Aedes mosquitoes affecting feeding behavior. Its efficiency is further enhanced by the insect saliva, although through unclear mechanisms. The mosquito proboscis is an efficient microelectromechanical system, which allows the insect to feed on vertebrate blood quickly and painlessly.
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