Trypanosoma brucei modifies the tsetse salivary composition, altering the fly feeding behavior that favors parasite transmission

J Van Den Abbeele, G Caljon, K De Ridder, P De Baetselier, M Coosemans

    Research output: Contribution to journalA1: Web of Science-article

    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
    Original languageEnglish
    JournalPLoS Pathogens
    Volume6
    Issue number6
    Pages (from-to)e1000926
    Number of pages9
    ISSN1553-7366
    DOIs
    Publication statusPublished - 2010

    Keywords

    • B780-tropical-medicine
    • Protozoal diseases
    • Trypanosomiasis-African
    • Sleeping sickness
    • Trypanosoma brucei
    • Vectors
    • Tsetse flies
    • Glossina
    • Infection
    • Saliva
    • Composition
    • Salivary glands
    • Transmission dynamics
    • Feeding behavior
    • Bloodmeal
    • Platelet aggregation
    • Vector-host interactions

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