A new asymmetric division contributes to the continuous production of infective trypanosomes in the tsetse fly

French National Centre for Scientific Research, Lutetia Parisorum, Île-de-France, France
Development (Impact Factor: 6.46). 04/2012; 139(10):1842-50. DOI: 10.1242/dev.072611
Source: PubMed


African trypanosomes are flagellated protozoan parasites that cause sleeping sickness and are transmitted by the bite of the tsetse fly. To complete their life cycle in the insect, trypanosomes reach the salivary glands and transform into the metacyclic infective form. The latter are expelled with the saliva at each blood meal during the whole life of the insect. Here, we reveal a means by which the continuous production of infective parasites could be ensured. Dividing trypanosomes present in the salivary glands of infected tsetse flies were monitored by live video-microscopy and by quantitative immunofluorescence analysis using molecular markers for the cytoskeleton and for surface antigens. This revealed the existence of two distinct modes of trypanosome proliferation occurring simultaneously in the salivary glands. The first cycle produces two equivalent cells that are not competent for infection and are attached to the epithelium. This mode of proliferation is predominant at the early steps of infection, ensuring a rapid colonization of the glands. The second mode is more frequent at later stages of infection and involves an asymmetric division. It produces a daughter cell that matures into the infective metacyclic form that is released in the saliva, as demonstrated by the expression of specific molecular markers - the calflagins. The levels of these calcium-binding proteins increase exclusively in the new flagellum during the asymmetric division, showing the commitment of the future daughter cell to differentiation. The coordination of these two alternative cell cycles contributes to the continuous production of infective parasites, turning the tsetse fly into an efficient and long-lasting vector for African trypanosomes.


Available from: Philippe Bastin, Jun 04, 2015
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    • "if in epimastigotes K is always more anterior than in PP1-3 RNAi induced cells [23] [24]. One hypothesis could be that PP1-3 would act as a brake to refrain cells from undergoing transformation to the epimastigote stage, similar to the protein tyrosine phosphatase TbPTP1 that arrests bloodstream trypanosomes in a stumpy state [25]. "
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    ABSTRACT: Reversible protein phosphorylation is a key regulator in intracellular functions. In the African trypanosome, Trypanosoma brucei, the serine-threonine phosphatase PP1-3, is localised in the cytoplasm. RNAi mediated knockdown of PP1-3 leads to a coordinated rearrangement of cellular organelles and compartments in the procyclic trypanosome. These parasites display their nucleus at the very posterior end of the cell. The kinetoplast is very close to the nucleus, and often located in a more anterior position. The lysosomal compartment, which in a normal procyclic cell is situated between nucleus and kinetoplast, is now positioned towards the anterior end of the cell. The Flagellum Attachment Zone, essential for cytokinesis, is still constructed, allowing initiation of the cleavage furrow and cell division. These adaptations allow dividing cells to distribute their organelles among the daughter cells and to proliferate normally. PP1-3 is therefore essential in conserving the intracellular organisation of the procyclic trypanosome cell.
    Molecular and Biochemical Parasitology 11/2013; 192(1). DOI:10.1016/j.molbiopara.2013.11.001 · 1.79 Impact Factor
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    • "These SG attached epimastigotes are proliferative and proceed to colonize the SG via cell division (Figure 3V). Later in the infection of the SG, another example of asymmetric division is initiated in the SG epimastigote population, where the epimastigotes undergo epitrypo cell division (Figure 3VI) to give rise to trypomastigotes that are thought to be the progenitors for the metacyclic form in the SG (Rotureau et al., 2012). Once a population of metacyclic parasites is established, the cycle can then begin anew when the infected tsetse feeds on a vertebrate host. "
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    ABSTRACT: T. brucei, the causative parasite for African trypanosomiasis, faces an interesting dilemma in its life cycle. It has to successfully complete its infection cycle in the tsetse vector to be able to infect other vertebrate hosts. T. brucei has to undergo multiple morphological changes as it invades the alimentary canal of the tsetse to finally achieve infectivity in the salivary glands. In this review, we attempt to elucidate how these morphological changes are possible for a parasite that has evolved a highly robust cell structure to survive the chemically and physically diverse environments it finds itself in. To achieve this, we juxtaposed the experimental evidence that has been collected from T. brucei forms that are cultured in vitro with the observations that have been carried out on tsetse-infective forms in vivo. Although the accumulated knowledge on T. brucei biology is by no means trivial, several outstanding questions remain for how the parasite mechanistically changes its morphology as it traverses the tsetse and how those changes are triggered. However, we conclude that with recent breakthroughs allowing for the replication of the tsetse-infection process of T. brucei in vitro, these outstanding questions can finally be addressed.
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    • "Parasite paths in the tsetse digestive tract are schematically presented in the left panel [adapted from (Hoare, 1972)]. Successive parasite stages found in the different organs are presented in a chronological order in the right panel [adapted from (Hoare, 1972; Peacock et al., 2007, 2012; Rotureau et al., 2012)]. * indicate proliferating stages and ? "
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    ABSTRACT: African trypanosomes are unicellular flagellated parasites causing trypanosomiases in Africa, a group of severe diseases also known as sleeping sickness in human and nagana in cattle. These parasites are almost exclusively transmitted by the bite of the tsetse fly. In this review, we describe and compare the three developmental programs of the main trypanosome species impacting human and animal health, with focus on the most recent observations. From here, some reflections are made on research issues concerning trypanosome developmental biology in the tsetse fly that are to be addressed in the future.
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