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Parasit Vectors. 2017 Dec 19;10(1):614. doi: 10.1186/s13071-017-2569-7.

Tsetse fly (Glossina pallidipes) midgut responses to Trypanosoma brucei challenge.

Bateta R1,2,3, Wang J4,5,6, Wu Y4, Weiss BL4, Warren WC7, Murilla GA8,4, Aksoy S4, Mireji PO9,10,11,12.

Author information

1
Department of Biochemistry, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, P.O. Box 362, Kikuyu, Kenya. batetarw@yahoo.com.
2
Department of Biochemistry and Molecular Biology, Egerton University, P.O. Box 536, Njoro, Kenya. batetarw@yahoo.com.
3
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA. batetarw@yahoo.com.
4
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.
5
State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai, 200433, China.
6
Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai, 200433, China.
7
McDonnell Genome Institute, Washington University School of Medicine, 4444 Forest Park Ave., Campus Box 8501, St Louis, MO, 63108, USA.
8
Department of Biochemistry, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, P.O. Box 362, Kikuyu, Kenya.
9
Department of Biochemistry, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, P.O. Box 362, Kikuyu, Kenya. mireji.paul@gmail.com.
10
Department of Biochemistry and Molecular Biology, Egerton University, P.O. Box 536, Njoro, Kenya. mireji.paul@gmail.com.
11
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA. mireji.paul@gmail.com.
12
Centre for Geographic Medicine Research - Coast, Kenya Medical Research Institute, P. O. Box 428-80108, Kilifi, Kenya. mireji.paul@gmail.com.

Abstract

BACKGROUND:

Tsetse flies (Glossina spp.) are the prominent vector of African trypanosome parasites (Trypanosoma spp.) in sub-Saharan Africa, and Glossina pallidipes is the most widely distributed species in Kenya. This species displays strong resistance to infection by parasites, which are typically eliminated in the midgut shortly after acquisition from the mammalian host. Although extensive molecular information on immunity for the related species Glossina morsitans morsitans exists, similar information is scarce for G. pallidipes.

METHODS:

To determine temporal transcriptional responses of G. pallidipes to Trypanosoma brucei brucei challenge, we conducted Illumina based RNA-seq on midgut organ and carcass from teneral females G. pallidipes at 24 and 48 h post-challenge (hpc) with T. b. brucei relative to their respective controls that received normal blood meals (without the parasite). We used a suite of bioinformatics tools to determine differentially expressed and enriched transcripts between and among tissues, and to identify expanded transcripts in G. pallidipes relative to their orthologs G. m. morsitans.

RESULTS:

Midgut transcripts induced at 24 hpc encoded proteins were associated with lipid remodelling, proteolysis, collagen metabolism, apoptosis, and cell growth. Midgut transcripts induced at 48 hpc encoded proteins linked to embryonic growth and development, serine endopeptidases and proteosomal degradation of the target protein, mRNA translation and neuronal development. Temporal expression of immune responsive transcripts at 48 relative to 24 hpc was pronounced, indicative of a gradual induction of host immune responses the following challenge. We also searched for G. m. morsitans orthologous groups that may have experienced expansions in the G. pallidipes genome. We identified ten expanded groups in G. pallidipes with putative immunity-related functions, which may play a role in the higher refractoriness exhibited by this species.

CONCLUSIONS:

There appears to be a lack of strong immune responses elicited by gut epithelia of teneral adults. This in combination with a compromised peritrophic matrix at this stage during the initial phase of T. b. brucei challenge may facilitate the increased parasite infection establishment noted in teneral flies relative to older adults. Although teneral flies are more susceptible than older adults, the majority of tenerals are still able to eliminate parasite infections. Hence, robust responses elicited at a later time point, such as 72 hpc, may clear parasite infections from the majority of flies. The expanded G. m. morsitans orthologous groups in G. pallidipes may also be functionally associated with the enhanced refractoriness to trypanosome infections reported in G. pallidipes relative to G. m. morsitans.

KEYWORDS:

Challenge; Glossina pallidipes; Immunity; Trypanosoma brucei brucei

PMID:
29258576
PMCID:
PMC5738168
DOI:
10.1186/s13071-017-2569-7
[Indexed for MEDLINE]
Free PMC Article

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