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Vector-borne Trypanosoma brucei parasites develop in artificial human skin and persist as skin tissue forms

Christian Reuter, Fabian Imdahl, Laura Hauf, Ehsan Vafadarnejad, Philipp Fey, Tamara Finger, Heike Walles, Antoine-Emmanuel Saliba, Florian Groeber-Becker, View ORCID ProfileMarkus Engstler
doi: https://doi.org/10.1101/2021.05.13.443986
Christian Reuter
1Department of Cell and Developmental Biology, Julius-Maximilians University, Würzburg, Germany
2Department of Tissue Engineering and Regenerative Medicine (TERM), University Hospital Würzburg, Würzburg, Germany
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Fabian Imdahl
5Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI), Würzburg, Germany
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Laura Hauf
1Department of Cell and Developmental Biology, Julius-Maximilians University, Würzburg, Germany
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Ehsan Vafadarnejad
5Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI), Würzburg, Germany
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Philipp Fey
3Translational Center Regenerative Medicine, Fraunhofer ISC, Würzburg, Germany
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Tamara Finger
3Translational Center Regenerative Medicine, Fraunhofer ISC, Würzburg, Germany
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Heike Walles
4Core Facility Tissue Engineering, Otto-von-Guericke University, Magdeburg, Germany
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Antoine-Emmanuel Saliba
5Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI), Würzburg, Germany
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Florian Groeber-Becker
3Translational Center Regenerative Medicine, Fraunhofer ISC, Würzburg, Germany
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Markus Engstler
1Department of Cell and Developmental Biology, Julius-Maximilians University, Würzburg, Germany
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  • ORCID record for Markus Engstler
  • For correspondence: markus.engstler@biozentrum.uni-wuerzburg.de
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Summary

Transmission of Trypanosoma brucei by tsetse flies involves the deposition of the cell cycle-arrested metacyclic life cycle stage into mammalian skin at the site of the fly’s bite. In the skin, the metacyclic parasites reactivate and differentiate into proliferative trypanosomes before colonizing the host’s blood and tissues. We generated an advanced human skin equivalent and used tsetse flies to naturally infect the artificial skin with trypanosomes. We detailed the chronological order of the parasites’ development in the skin, and found a rapid activation of metacyclic trypanosomes and differentiation to proliferative parasites. Single-cell parasite transcriptomics were used to document the biological events during differentiation and host invasion at five different timepoints. After the establishment of a proliferative trypanosome population in the skin, the parasites entered a reversible quiescent state characterized by slow replication and a strongly reduced metabolism. We termed these quiescent trypanosomes skin tissue forms (STF), a parasite population that may play an important role in maintaining the infection over long time periods and in asymptomatic infected individuals.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 13, 2021.
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Vector-borne Trypanosoma brucei parasites develop in artificial human skin and persist as skin tissue forms
Christian Reuter, Fabian Imdahl, Laura Hauf, Ehsan Vafadarnejad, Philipp Fey, Tamara Finger, Heike Walles, Antoine-Emmanuel Saliba, Florian Groeber-Becker, Markus Engstler
bioRxiv 2021.05.13.443986; doi: https://doi.org/10.1101/2021.05.13.443986
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Vector-borne Trypanosoma brucei parasites develop in artificial human skin and persist as skin tissue forms
Christian Reuter, Fabian Imdahl, Laura Hauf, Ehsan Vafadarnejad, Philipp Fey, Tamara Finger, Heike Walles, Antoine-Emmanuel Saliba, Florian Groeber-Becker, Markus Engstler
bioRxiv 2021.05.13.443986; doi: https://doi.org/10.1101/2021.05.13.443986

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