Abstract
Tsetse flies are the notorious transmitters of African trypanosomiasis, a disease caused by the Trypanosoma parasite that affects humans and livestock on the African continent. Metacyclic infection rates in natural tsetse populations with Trypanosoma brucei, including the two human-pathogenic subspecies, are very low, even in epidemic situations. Therefore, the infected fly/host contact frequency is a key determinant of the transmission dynamics. As an obligate blood feeder, tsetse flies rely on their complex salivary potion to inhibit host haemostatic reactions ensuring an efficient feeding. The results of this experimental study suggest that the parasite might promote its transmission through manipulation of the tsetse feeding behavior by modifying the saliva composition. Indeed, salivary gland Trypanosoma brucei-infected flies display a significantly prolonged feeding time, thereby enhancing the likelihood of infecting multiple hosts during the process of a single blood meal cycle. Comparison of the two major anti-haemostatic activities i.e. anti-platelet aggregation and anti-coagulation activity in these flies versus non-infected tsetse flies demonstrates a significant suppression of these activities as a result of the trypanosome-infection status. This effect was mainly related to the parasite-induced reduction in salivary gland gene transcription, resulting in a strong decrease in protein content and related biological activities. Additionally, the anti-thrombin activity and inhibition of thrombin-induced coagulation was even more severely hampered as a result of the trypanosome infection. Indeed, while naive tsetse saliva strongly inhibited human thrombin activity and thrombin-induced blood coagulation, saliva from T. brucei-infected flies showed a significantly enhanced thrombinase activity resulting in a far less potent anti-coagulation activity. These data clearly provide evidence for a trypanosome-mediated modification of the tsetse salivary composition that results in a drastically reduced anti-haemostatic potential and a hampered feeding performance which could lead to an increase of the vector/host contact and parasite transmission in field conditions.
Highlights
Tsetse flies (Diptera: Glossinidae) are obligate blood feeding insects that are important disease vectors given their involvement in the transmission of different pathogenic trypanosome species that cause human sleeping sickness and livestock trypanosomiasis in Africa
Several compounds have been implicated in facilitating blood feeding: a thrombin inhibitor [tsetse thrombin inhibitor (TTI)] [5,6] and salivary apyrases [59nucleotidase related protein, Glossina morsitans morsitans salivary gland protein 3 (Sgp3)] including at least one with fibrinogen receptor (GPIIb/IIIa) antagonistic properties (59Nuc) [7]
We investigated whether T. brucei parasites alter the tsetse fly blood feeding behavior in a way that would favor parasite transmission within the mammalian host population
Summary
Tsetse flies (Diptera: Glossinidae) are obligate blood feeding insects that are important disease vectors given their involvement in the transmission of different pathogenic trypanosome species that cause human sleeping sickness and livestock trypanosomiasis in Africa. Rhodesiense – have to go through a complex developmental cycle in the alimentary tract and salivary glands of the tsetse fly [1]. The salivary gland is the tissue in which T. brucei parasites undergo the final developmental phase, i.e. a continuous cycle of multiplication and cellular differentiation into the metacyclic form that is infective for the mammalian host [2]. Once this trypanosome population has been established in the salivary glands, it is continuously maintained at high density throughout the remaining life span of the tsetse fly.
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