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

Author

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  • Christian Reuter

    (Biocenter, Julius-Maximilians-Universitaet of Wuerzburg
    University Hospital Wuerzburg)

  • Laura Hauf

    (Biocenter, Julius-Maximilians-Universitaet of Wuerzburg)

  • Fabian Imdahl

    (Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI)
    Julius-Maximilians-Universitaet of Wuerzburg)

  • Rituparno Sen

    (Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI))

  • Ehsan Vafadarnejad

    (Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI))

  • Philipp Fey

    (Translational Center Regenerative Therapies, Fraunhofer ISC)

  • Tamara Finger

    (Translational Center Regenerative Therapies, Fraunhofer ISC)

  • Nicola G. Jones

    (Biocenter, Julius-Maximilians-Universitaet of Wuerzburg)

  • Heike Walles

    (Translational Center Regenerative Therapies, Fraunhofer ISC
    Otto-von-Guericke University)

  • Lars Barquist

    (Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI))

  • Antoine-Emmanuel Saliba

    (Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI)
    Julius-Maximilians-Universitaet of Wuerzburg)

  • Florian Groeber-Becker

    (University Hospital Wuerzburg
    Translational Center Regenerative Therapies, Fraunhofer ISC)

  • Markus Engstler

    (Biocenter, Julius-Maximilians-Universitaet of Wuerzburg)

Abstract

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. We introduce an advanced human skin equivalent and use tsetse flies to naturally infect the skin with trypanosomes. We detail the chronological order of the parasites’ development in the skin by single-cell RNA sequencing and find a rapid activation of metacyclic trypanosomes and differentiation to proliferative parasites. Here we show that after the establishment of a proliferative population, the parasites enter a reversible quiescent state characterized by slow replication and a strongly reduced metabolism. We term these quiescent trypanosomes skin tissue forms, a parasite population that may play an important role in maintaining the infection over long time periods and in asymptomatic infected individuals.

Suggested Citation

  • Christian Reuter & Laura Hauf & Fabian Imdahl & Rituparno Sen & Ehsan Vafadarnejad & Philipp Fey & Tamara Finger & Nicola G. Jones & Heike Walles & Lars Barquist & Antoine-Emmanuel Saliba & Florian Gr, 2023. "Vector-borne Trypanosoma brucei parasites develop in artificial human skin and persist as skin tissue forms," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43437-2
    DOI: 10.1038/s41467-023-43437-2
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    References listed on IDEAS

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    1. Samuel Dean & Rosa Marchetti & Kiaran Kirk & Keith R. Matthews, 2009. "A surface transporter family conveys the trypanosome differentiation signal," Nature, Nature, vol. 459(7244), pages 213-217, May.
    2. Sandra Trindade & Mariana Niz & Mariana Costa-Sequeira & Tiago Bizarra-Rebelo & Fábio Bento & Mario Dejung & Marta Valido Narciso & Lara López-Escobar & João Ferreira & Falk Butter & Frédéric Bringaud, 2022. "Slow growing behavior in African trypanosomes during adipose tissue colonization," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Shuxiong Wang & Michael L. Drummond & Christian F. Guerrero-Juarez & Eric Tarapore & Adam L. MacLean & Adam R. Stabell & Stephanie C. Wu & Guadalupe Gutierrez & Bao T. That & Claudia A. Benavente & Qi, 2020. "Single cell transcriptomics of human epidermis identifies basal stem cell transition states," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
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