Abstract
Toxoplasma gondii is a common parasite of humans and animals, which is transmitted via oocysts in cat faeces or tissue cysts in contaminated meat. The robust oocyst and sporocyst walls protect the infective sporozoites from deleterious external attacks including disinfectants. Upon oocyst acquisition, these walls lose their integrity to let the sporozoites excyst and invade host cells following a process that remains poorly understood. Given the resistance of the oocyst wall to digestive enzymes and the ability of oocysts to cause parenteral infections, the present study investigated the possible contribution of macrophages in supporting sporozoite excystation following oocyst internalisation. By using single cell micromanipulations, real-time and time-point imaging techniques, we demonstrated that RAW macrophages could interact rapidly with oocysts and engulfed them by remodelling of their actin cytoskeleton. Internalised oocysts were associated to macrophage acidic compartments and showed evidences of wall disruption. Sporozoites were observed in macrophages containing oocyst remnants or in new macrophages, giving rise to dividing tachyzoites. All together, these results highlight an unexpected role of phagocytic cells in processing T. gondii oocysts, in line with non-classical routes of infection, and open new perspectives to identify chemical factors that lead to oocyst wall disruption under physiological conditions.
Highlights
Level of protection for the sporozoites[3,9,10], though its capacity to resist physical and chemical attacks is relatively unknown
The macrophages could attach to several oocysts in a sequential manner and repeated phagocytosis resulted in macrophages containing multiple oocysts (Supplementary Movie S3)
The present study demonstrates that mouse macrophage-like RAW cells are able to facilitate the excystation of T. gondii sporozoites following internalisation of oocysts
Summary
Level of protection for the sporozoites[3,9,10], though its capacity to resist physical and chemical attacks is relatively unknown. The capacity of naïve macrophages to ingest large particles (10–20 μm in diameter)[23] besides their inability to eliminate the sporozoite and tachyzoite forms of T. gondii[11,13,14,24,25] prompted us to investigate whether the macrophages were able to internalise T. gondii oocysts, open their wall, allowing the sporozoites to excyst prior to their differentiation into tachyzoites To address this question, we investigated the direct interactions between T. gondii oocysts and RAW murine macrophages at different time points by using single cell and parasite micropipette micromanipulations and a combination of real-time and time-point imaging techniques. We present data highlighting an unexpected role for the macrophage in facilitating the excystation and differentiation of T. gondii sporozoites following oocyst internalisation
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