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PLoS Negl Trop Dis. 2017 Nov 20;11(11):e0006057. doi: 10.1371/journal.pntd.0006057. eCollection 2017 Nov.

Molecular characterization of tsetse's proboscis and its response to Trypanosoma congolense infection.

Author information

1
Department of Biochemistry, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, Kikuyu. Kenya.
2
Department of Biomedical Science and Technology, School of Public Health and Community Development, Maseno University, Private Bag, Maseno, Kenya.
3
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, United States of America.
4
Department of Agriculture, School of Agriculture and Food Science, Meru University of Science and Technology, Meru, Kenya.
5
Centre for Geographic Medicine Research-Coast, Kenya Medical Research Institute, Kilifi. Kenya.
6
Department of Medical Biochemistry, School of Medicine, Maseno University, Private Bag, Maseno, Kenya.

Abstract

Tsetse flies (Glossina spp.) transmit parasitic African trypanosomes (Trypanosoma spp.), including Trypanosoma congolense, which causes animal African trypanosomiasis (AAT). AAT detrimentally affects agricultural activities in sub-Saharan Africa and has negative impacts on the livelihood and nutrient availability for the affected communities. After tsetse ingests an infectious blood meal, T. congolense sequentially colonizes the fly's gut and proboscis (PB) organs before being transmitted to new mammalian hosts during subsequent feedings. Despite the importance of PB in blood feeding and disease transmission, little is known about its molecular composition, function and response to trypanosome infection. To bridge this gap, we used RNA-seq analysis to determine its molecular characteristics and responses to trypanosome infection. By comparing the PB transcriptome to whole head and midgut transcriptomes, we identified 668 PB-enriched transcripts that encoded proteins associated with muscle tissue, organ development, chemosensation and chitin-cuticle structure development. Moreover, transcripts encoding putative mechanoreceptors that monitor blood flow during tsetse feeding and interact with trypanosomes were also expressed in the PB. Microscopic analysis of the PB revealed cellular structures associated with muscles and cells. Infection with T. congolense resulted in increased and decreased expression of 38 and 88 transcripts, respectively. Twelve of these differentially expressed transcripts were PB-enriched. Among the transcripts induced upon infection were those encoding putative proteins associated with cell division function(s), suggesting enhanced tissue renewal, while those suppressed were associated with metabolic processes, extracellular matrix and ATP-binding as well as immunity. These results suggest that PB is a muscular organ with chemosensory and mechanosensory capabilities. The mechanoreceptors may be point of PB-trypanosomes interactions. T. congolense infection resulted in reduced metabolic and immune capacity of the PB. The molecular knowledge on the composition and putative functions of PB forms the foundation to identify new targets to disrupt tsetse's ability to feed and parasite transmission.

PMID:
29155830
PMCID:
PMC5695773
DOI:
10.1371/journal.pntd.0006057
[Indexed for MEDLINE]
Free PMC Article

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