Midgut expression of immune-related genes in Glossina palpalis gambiensis challenged with Trypanosoma brucei gambiense

Abstract

Tsetse flies from the subspecies Glossina morsitans morsitans and Glossina palpalis gambiensis, respectively, transmit Trypanosoma brucei rhodesiense and Trypanosoma brucei gambiense. The former causes the acute form of sleeping sickness, and the latter provokes the chronic form. Although several articles have reported G. m. morsitans gene expression following trypanosome infection, no comparable investigation has been performed for G. p. gambiensis. This report presents results on the differential expression of immune-related genes in G. p. gambiensis challenged with T. b. gambiense. The aim was to characterize transcriptomic events occurring in the tsetse gut during the parasite establishment step, which is the crucial first step in the parasite development cycle within its vector. The selected genes were chosen from those previously shown to be highly expressed in G. m. morsitans, to allow further comparison of gene expression in both Glossina species. Using quantitative PCR, genes were amplified from the dissected midguts of trypanosome-stimulated, infected, non-infected, and self-cleared flies at three sampling timepoints (3, 10, and 20 days) after a bloodmeal. At the 3-day sampling point, transferrin transcripts were significantly up-regulated in trypanosome-challenged flies versus flies fed on non-infected mice. In self-cleared flies, serpin-2 and thioredoxin peroxidase-3 transcripts were significantly up-regulated 10 days after trypanosome challenge, whereas nitric oxide synthase and chitin-binding protein transcripts were up-regulated after 20 days. Although the expression levels of the other genes were highly variable, the expression of immune-related genes in G. p. gambiensis appears to be a time-dependent process. The possible biological significance of these findings is discussed, and the results are compared with previous reports for G. m. morsitans.

RNA-seq de novo Assembly Reveals Differential Gene Expression in Glossina palpalis gambiensis Infected with Trypanosoma brucei gambiense vs. Non-Infected and Self-Cured Flies

“…We previously investigated 12 immune genes selected from those formerly reported by Lehane et al ( 2003 ) to be highly over-expressed in Glossina morsitans morsitans challenged with T. b. brucei (Hamidou Soumana et al, 2014c ). Nevertheless, deciphering the mechanisms that allow trypanosomes to adapt to the different tsetse fly microenvironments and thereby escape insect immune responses requires a more global approach.…”

Thioester‐containing proteins in the tsetse fly (Glossina) and their response to trypanosome infection

“…Our study revealed that the TEP expression profile in response to a trypanosome infection ( T. brucei brucei ) is strongly dissimilar in the two tsetse fly species, with only few genes up‐regulated in G. p. gambiensis flies in sharp contrast to G. m. morsitans flies. Significant differences between these two species in the midgut immune‐related response following trypanosome infection have been previously reported (Hamidou Soumana et al ., ). Similar to our results, no TEP genes were found to be differentially expressed in a recent comparative transcriptome analysis of T. b. gambiense‐ infected midgut (Hamidou Soumana et al ., ).…”

Protein abundance in the midgut of wild tsetse flies (Glossina palpalis palpalis) naturally infected by Trypanosoma congolense s.l.

“…The serine proteases are considered to be, together with other proteases, trypanosome virulence factors (Bossard et al, 2013). Thus, overexpression of serpins may result from the activation of the host immune response against serine proteases secreted in vivo by the invading parasite as shown by transcriptomic analyses (Hamidou Soumana, Tchicaya, et al, 2014; Matetovici et al, 2016; Ooi et al, 2015). Other proteins are also highly overrepresented, such as xanthine dehydrogenase (×6.6), alkyl hydroperoxide reductase (×4.7), eukaryotic translation initiation factor 3 (×3), proteasome subunit beta (×3) and membrane trafficking protein (×1.7), a key regulator of intracellular membrane trafficking, from the formation of transport vesicles to their fusion with the cellular membrane (Chatterjee & Major, 2001; Ferguson, 1999).…”