Coordination of humoral immune factors dictates compatibility between Schistosoma mansoni and Biomphalaria glabrata

  1. Hongyu Li
  2. Jacob R Hambrook
  3. Emmanuel A Pila
  4. Abdullah A Gharamah
  5. Jing Fang
  6. Xinzhong Wu
  7. Patrick Hanington  Is a corresponding author
  1. Beibu Gulf University, China
  2. University of Alberta, Canada

Abstract

Immune factors in snails of the genus Biomphalaria are critical for combating Schistosoma mansoni, the predominant cause of human intestinal schistosomiasis. Independently, many of these factors play an important role in, but do not fully define, the compatibility between the model snail B. glabrata, and S. mansoni. Here, we demonstrate association between four previously characterized humoral immune molecules; BgFREP3, BgTEP1, BgFREP2 and Biomphalysin. We also identify unique immune determinants in the plasma of S. mansoni-resistant B. glabrata that associate with the incompatible phenotype. These factors coordinate to initiate haemocyte-mediated destruction of S. mansoni sporocysts via production of reactive oxygen species. The inclusion of BgFREP2 in a BgFREP3-initiated complex that also includes BgTEP1 almost completely explains resistance to S. mansoni in this model. Our study unifies many independent lines of investigation to provide a more comprehensive understanding of the snail immune system in the context of infection by this important human parasite.

Data availability

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

Article and author information

Author details

  1. Hongyu Li

    Ocean College, Beibu Gulf University, Qinzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Jacob R Hambrook

    School of Public Health, University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Emmanuel A Pila

    School of Public Health, University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Abdullah A Gharamah

    School of Public Health, University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Jing Fang

    Ocean College, Beibu Gulf University, Qinzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Xinzhong Wu

    Ocean College, Beibu Gulf University, Qinzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Patrick Hanington

    School of Public Health, University of Alberta, Edmonton, Canada
    For correspondence
    pch1@ualberta.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3964-5012

Funding

Natural Sciences and Engineering Research Council of Canada (2018-05209)

  • Patrick Hanington

Natural Sciences and Engineering Research Council of Canada (2018- 522661)

  • Patrick Hanington

National Natural Science Foundation of China (31272682)

  • Xinzhong Wu

Guangxi 16 Natural Science Foundation (2016JJD130059)

  • Xinzhong Wu

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

Reviewing Editor

  1. Bruno Lemaître, École Polytechnique Fédérale de Lausanne, Switzerland

Ethics

Animal experimentation: All animal work observed ethical requirements and was approved by the Canadian Council of Animal Care and Use Committee (Biosciences) for the University of Alberta (AUP00000057).

Version history

  1. Received: September 7, 2019
  2. Accepted: January 7, 2020
  3. Accepted Manuscript published: January 9, 2020 (version 1)
  4. Version of Record published: January 20, 2020 (version 2)

Copyright

© 2020, Li 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. Hongyu Li
  2. Jacob R Hambrook
  3. Emmanuel A Pila
  4. Abdullah A Gharamah
  5. Jing Fang
  6. Xinzhong Wu
  7. Patrick Hanington
(2020)
Coordination of humoral immune factors dictates compatibility between Schistosoma mansoni and Biomphalaria glabrata
eLife 9:e51708.
https://doi.org/10.7554/eLife.51708

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https://doi.org/10.7554/eLife.51708

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