Comparative proteomic analysis of the hemolymph and salivary glands ofRhodnius prolixusandR. colombiensisreveals candidates associated with differential lytic activity againstTrypanosoma cruziI andT. cruziII
Authors: Barbosa Hamilton J. , Quevedo Yazmin Suárez , Torres Arlid Meneses , Veloza Gustavo A. Gaitán , Martínez Julio C. Carranza , Urrea-Montes Daniel A. , Robello-Porto Carlos , Vallejo Gustavo A. 
Published: June 2023

Background

Immune response of triatomines plays an important role in the success or failure of transmission ofT. cruzi. Studies on parasite–vector interaction have shown the presence of trypanolytic factors and have been observed to be differentially expressed among triatomines, which affects the transmission of someT. cruzistrains or DTUs (Discrete Typing Units).

Methodology/Principal Findings

Trypanolytic factors were detected in the hemolymph and saliva ofR. prolixusagainst epimastigotes and trypomastigotes ofT. cruziII. To identify the components of the immune response that could be involved in this lytic activity, a comparative proteomic analysis was carried out, detecting 120 proteins in the hemolymph ofR. prolixusand 107 inR. colombiensis. In salivary glands, 1103 proteins were detected inR. prolixusand 853 inR. colombiensis. A higher relative abundance of lysozyme, prolixin, nitrophorins, and serpin as immune response proteins was detected in the hemolymph ofR. prolixus. Among theR. prolixussalivary proteins, a higher relative abundance of nitrophorins, lipocalins, and triabins was detected. The higher relative abundance of these immune factors inR. prolixussupports their participation in the lytic activity onT. cruziII, but not onT. cruziI, which is resistant to lysis by hemolymph and salivary proteins ofR. prolixusdue to mechanisms of evading oxidative stress caused by immune factors.

Conclusions/Significance

T. cruziI is a DTU distributed from the southern United States to the center of Chile and Argentina, and its successful spread across this range could be related to resistance to oxidative stress in vectors. Future proteomic and transcriptomic studies on vectors and the interactions of the intestinal microbiota with parasites will help to confirm the determinants of successful or failed vector transmission ofT. cruziDTUs in different parts of the Western Hemisphere.

Author summary

Some factors can facilitate or preventT. cruzitransmission, i.e. vector immunity. Our work has managed to detect a stronger immune response againstT. cruziII inR. prolixussaliva and haemolymph, compared to that ofR. colombiensis. Proteins from both species’ saliva and haemolymph were analysed for studying factors which might have been involved in such response; most proteins were detected in both species’ haemolymph, thereby indicating common immune mechanisms. Three proteins having oxidative immune activity were only expressed inR. prolixus. Lipocalin diversity and abundance predominated inR. prolixussaliva; these proteins are involved in nitric oxide metabolism and their role in immunity could be key in host defence againstT. cruzi. Recognising the components modulating parasite transmission in a vector helps in understanding how such factors act independently and how they would act synergistically againstT. cruzi, thereby enabling us to establish tools regarding Chaga’s disease epidemiology, aimed at predictingT. cruzidistribution and creating transmission control mechanisms.