Formation and three-dimensional architecture of Leishmania adhesion in the sand fly vector

  1. Ryuji Yanase
  2. Flávia Moreira-Leite
  3. Edward Rea
  4. Lauren Wilburn
  5. Jovana Sádlová
  6. Barbora Vojtkova
  7. Katerina Pružinová
  8. Atsushi Taniguchi
  9. Shigenori Nonaka
  10. Petr Volf
  11. Jack D Sunter  Is a corresponding author
  1. Oxford Brookes University, United Kingdom
  2. Charles University, Czech Republic
  3. Hokkaido University, Japan
  4. National Institute for Basic Biology, Japan

Abstract

Attachment to a substrate to maintain position in a specific ecological niche is a common strategy across biology, especially for eukaryotic parasites. During development in the sand fly vector, the eukaryotic parasite Leishmania adheres to the stomodeal valve, as the specialised haptomonad form. Dissection of haptomonad adhesion is a critical step for understanding the complete life cycle of Leishmania. Nevertheless, haptomonad studies are limited, as this is a technically challenging life cycle form to investigate. Here, we have combined three-dimensional electron microscopy approaches, including serial block face scanning electron microscopy (SBFSEM) and serial tomography to dissect the organisation and architecture of haptomonads in the sand fly. We showed that the attachment plaque contains distinct structural elements. Using time-lapse light microscopy of in vitro haptomonad-like cells, we identified five stages of haptomonad-like cell differentiation, and showed that calcium is necessary for Leishmania adhesion to the surface in vitro. This study provides the structural and regulatory foundations of Leishmania adhesion,which are critical for a holistic understanding of the Leishmania life cycle.

Data availability

All data generated or analysed during this study are included in the manuscript.

Article and author information

Author details

  1. Ryuji Yanase

    Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9419-398X
  2. Flávia Moreira-Leite

    Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Edward Rea

    Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Lauren Wilburn

    Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Jovana Sádlová

    Department of Parasitology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. Barbora Vojtkova

    Department of Parasitology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  7. Katerina Pružinová

    Department of Parasitology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  8. Atsushi Taniguchi

    Research Center of Mathematics for Social Creativity, Hokkaido University, Sapporo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Shigenori Nonaka

    Laboratory for Spatiotemporal Regulations, National Institute for Basic Biology, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  10. Petr Volf

    Department of Parasitology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1790-1123
  11. Jack D Sunter

    Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom
    For correspondence
    jsunter@brookes.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2836-9622

Funding

Japan Society for the Promotion of Science

  • Ryuji Yanase

National Institute for Basic Biology (20-515)

  • Ryuji Yanase

Horizon 2020 Framework Programme (Infravec2)

  • Petr Volf

Wellcome Trust (221944/Z20/Z)

  • Jack D Sunter

European Regional Development Fund (CeRaViP)

  • Petr Volf

Czech Science Foundation (GACR 21-15700S)

  • Petr Volf

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Dario S Zamboni, Universidade de Sao Paulo, Brazil

Version history

  1. Received: October 28, 2022
  2. Preprint posted: October 30, 2022 (view preprint)
  3. Accepted: May 4, 2023
  4. Accepted Manuscript published: May 10, 2023 (version 1)
  5. Version of Record published: May 18, 2023 (version 2)

Copyright

© 2023, Yanase et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ryuji Yanase
  2. Flávia Moreira-Leite
  3. Edward Rea
  4. Lauren Wilburn
  5. Jovana Sádlová
  6. Barbora Vojtkova
  7. Katerina Pružinová
  8. Atsushi Taniguchi
  9. Shigenori Nonaka
  10. Petr Volf
  11. Jack D Sunter
(2023)
Formation and three-dimensional architecture of Leishmania adhesion in the sand fly vector
eLife 12:e84552.
https://doi.org/10.7554/eLife.84552

Share this article

https://doi.org/10.7554/eLife.84552

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