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A surface transporter family conveys the trypanosome differentiation signal

Author

Listed:
  • Samuel Dean

    (Centre for Immunity, Infection and Evolution, Institute for Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK)

  • Rosa Marchetti

    (School of Biochemistry & Molecular Biology, Australian National University, Canberra, ACT 0200, Australia)

  • Kiaran Kirk

    (School of Biochemistry & Molecular Biology, Australian National University, Canberra, ACT 0200, Australia)

  • Keith R. Matthews

    (Centre for Immunity, Infection and Evolution, Institute for Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK)

Abstract

Microbial pathogens use environmental cues to trigger the developmental events needed to infect mammalian hosts or transmit to disease vectors. The parasites causing African sleeping sickness respond to citrate or cis-aconitate (CCA) to initiate life-cycle development when transmitted to their tsetse fly vector. This requires hypersensitization of the parasites to CCA by exposure to low temperature, conditions encountered after tsetse fly feeding at dusk or dawn. Here we identify a carboxylate-transporter family, PAD (proteins associated with differentiation), required for perception of this differentiation signal. Consistent with predictions for the response of trypanosomes to CCA, PAD proteins are expressed on the surface of the transmission-competent ‘stumpy-form’ parasites in the bloodstream, and at least one member is thermoregulated, showing elevated expression and surface access at low temperature. Moreover, RNA-interference-mediated ablation of PAD expression diminishes CCA-induced differentiation and eliminates CCA hypersensitivity under cold-shock conditions. As well as being molecular transducers of the differentiation signal in these parasites, PAD proteins provide the first example of a surface marker able to discriminate the transmission stage of trypanosomes in their mammalian host.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:459:y:2009:i:7244:d:10.1038_nature07997
    DOI: 10.1038/nature07997
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    Citations

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    Cited by:

    1. Mabel Deladem Tettey & Federico Rojas & Keith R. Matthews, 2022. "Extracellular release of two peptidases dominates generation of the trypanosome quorum-sensing signal," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Mathieu Cayla & Christos Spanos & Kirsty McWilliam & Eliza Waskett & Juri Rappsilber & Keith R. Matthews, 2024. "Differentiation granules, a dynamic regulator of T. brucei development," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Juan F. Quintana & Praveena Chandrasegaran & Matthew C. Sinton & Emma M. Briggs & Thomas D. Otto & Rhiannon Heslop & Calum Bentley-Abbot & Colin Loney & Luis de Lecea & Neil A. Mabbott & Annette MacLe, 2022. "Single cell and spatial transcriptomic analyses reveal microglia-plasma cell crosstalk in the brain during Trypanosoma brucei infection," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. 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.

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