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Differentiation granules, a dynamic regulator of T. brucei development

Author

Listed:
  • Mathieu Cayla

    (University of Edinburgh
    University of York)

  • Christos Spanos

    (University of Edinburgh)

  • Kirsty McWilliam

    (University of Edinburgh)

  • Eliza Waskett

    (University of Edinburgh)

  • Juri Rappsilber

    (University of Edinburgh)

  • Keith R. Matthews

    (University of Edinburgh)

Abstract

Adaptation to a change of environment is an essential process for survival, in particular for parasitic organisms exposed to a wide range of hosts. Such adaptations include rapid control of gene expression through the formation of membraneless organelles composed of poly-A RNA and proteins. The African trypanosome Trypanosoma brucei is exquisitely sensitive to well-defined environmental stimuli that trigger cellular adaptations through differentiation events that characterise its complex life cycle. The parasite has been shown to form stress granules in vitro, and it has been proposed that such a stress response could have been repurposed to enable differentiation and facilitate parasite transmission. Therefore, we explored the composition and positional dynamics of membraneless granules formed in response to starvation stress and during differentiation in the mammalian host between the replicative slender and transmission-adapted stumpy forms. We find that T. brucei differentiation does not reflect the default response to environmental stress. Instead, the developmental response of the parasites involves a specific and programmed hierarchy of membraneless granule assembly, with distinct components and regulation by protein kinases such as TbDYRK, that are required for the parasite to successfully progress through its life cycle development and prepare for transmission.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47309-1
    DOI: 10.1038/s41467-024-47309-1
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    References listed on IDEAS

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    1. Binny M. Mony & Paula MacGregor & Alasdair Ivens & Federico Rojas & Andrew Cowton & Julie Young & David Horn & Keith Matthews, 2014. "Genome-wide dissection of the quorum sensing signalling pathway in Trypanosoma brucei," Nature, Nature, vol. 505(7485), pages 681-685, January.
    2. 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.
    3. Arpan Kumar Rai & Jia-Xuan Chen & Matthias Selbach & Lucas Pelkmans, 2018. "Kinase-controlled phase transition of membraneless organelles in mitosis," Nature, Nature, vol. 559(7713), pages 211-216, July.
    4. Emma M. Briggs & Federico Rojas & Richard McCulloch & Keith R. Matthews & Thomas D. Otto, 2021. "Single-cell transcriptomic analysis of bloodstream Trypanosoma brucei reconstructs cell cycle progression and developmental quorum sensing," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    5. Nicola M. Moloney & Konstantin Barylyuk & Eelco Tromer & Oliver M. Crook & Lisa M. Breckels & Kathryn S. Lilley & Ross F. Waller & Paula MacGregor, 2023. "Mapping diversity in African trypanosomes using high resolution spatial proteomics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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