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A modification to the life cycle of the parasite Trypanosoma brucei

Sarah Schuster, Ines Subota, Jaime Lisack, Henriette Zimmermann, Christian Reuter, View ORCID ProfileBrooke Morriswood, View ORCID ProfileMarkus Engstler
doi: https://doi.org/10.1101/717975
Sarah Schuster
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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Ines Subota
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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Jaime Lisack
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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Henriette Zimmermann
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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Christian Reuter
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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Brooke Morriswood
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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Markus Engstler
Department of Cell and Developmental Biology, Biocentre, University of Wuerzburg
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  • For correspondence: markus.engstler@biozentrum.uni-wuerzburg.de
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Abstract

African trypanosomes cause sleeping sickness in humans and nagana in cattle. These unicellular parasites are transmitted by the blood-sucking tsetse fly1. In the mammalian host’s circulation, tissues, and interstitium, at least two main life cycle stages exist: slender and stumpy bloodstream forms2,3,4,5,6. Proliferating slender forms differentiate into cell cycle-arrested stumpy forms at high levels of parasitaemia. This developmental stage transition occurs in response to the quorum sensing factor SIF (stumpy induction factor)7, and is thought to fulfil two main functions. First, it auto-regulates the parasite load in the host. Second, the stumpy stage is regarded as pre-adapted for tsetse fly infection and the only form capable of successful vector transmission8. Differentiation to the stumpy form is accompanied by fundamental morphological and metabolic changes, including expression of the stumpy marker, protein associated with differentiation 1 (PAD1)9. Here, we show that proliferating slender stage trypanosomes are equally able to infect the tsetse fly, and that a single parasite is sufficient. The slender parasites complete the complex life cycle in the fly with comparable overall success rates and kinetics as stumpy forms. We further show that in the tsetse midgut, the slender parasites activate the canonical PAD1 pathway, without undergoing either cell cycle arrest or a morphological transition to the stumpy form. Instead, with the onset of PAD1 expression, the parasites directly differentiate into the procyclic (insect) stage. Our findings not only propose a revision to the traditional view of the trypanosome life cycle, but also suggest a solution to a long-acknowledged paradox in the transmission event: parasitaemia in chronic infections is typically quite low, and so the probability of a tsetse ingesting a stumpy cell during a bloodmeal is also low10,11,12,13.

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Posted July 29, 2019.
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A modification to the life cycle of the parasite Trypanosoma brucei
Sarah Schuster, Ines Subota, Jaime Lisack, Henriette Zimmermann, Christian Reuter, Brooke Morriswood, Markus Engstler
bioRxiv 717975; doi: https://doi.org/10.1101/717975
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A modification to the life cycle of the parasite Trypanosoma brucei
Sarah Schuster, Ines Subota, Jaime Lisack, Henriette Zimmermann, Christian Reuter, Brooke Morriswood, Markus Engstler
bioRxiv 717975; doi: https://doi.org/10.1101/717975

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