1. Physics of Living Systems

Stochastic bond dynamics facilitates alignment of malaria parasite at erythrocyte membrane upon invasion

  1. Sebastian Hillringhaus
  2. Anil K Dasanna
  3. Gerhard Gompper  Is a corresponding author
  4. Dmitry A Fedosov  Is a corresponding author
  1. Forschungszentrum Juelich, Germany
  2. Forschungszentrum Jülich, Germany
https://doi.org/10.7554/eLife.56500
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  1. Sebastian Hillringhaus
  2. Anil K Dasanna
  3. Gerhard Gompper
  4. Dmitry A Fedosov
(2020)
Stochastic bond dynamics facilitates alignment of malaria parasite at erythrocyte membrane upon invasion
eLife 9:e56500.
https://doi.org/10.7554/eLife.56500
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Abstract

Malaria parasites invade healthy red blood cells (RBCs) during the blood stage of the disease. Even though parasites initially adhere to RBCs with a random orientation, they need to align their apex toward the membrane in order to start the invasion process. Using hydrodynamic simulations of a RBC and parasite, where both interact through discrete stochastic bonds, we show that parasite alignment is governed by the combination of RBC membrane deformability and dynamics of adhesion bonds. The stochastic nature of bond-based interactions facilitates a diffusive-like re-orientation of the parasite at the RBC membrane, while RBC deformation aids in the establishment of apex-membrane contact through partial parasite wrapping by the membrane. This bond-based model for parasite adhesion quantitatively captures alignment times measured experimentally and demonstrates that alignment times increase drastically with increasing rigidity of the RBC membrane. Our results suggest that the alignment process is mediated simply by passive parasite adhesion.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2-8, including all figure supplements. Figure 1 is a model schematic, which does not contain any data.

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Author details

  1. Sebastian Hillringhaus

    Institute of Biological Information Processing, Forschungszentrum Juelich, Juelich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0100-9368

  2. Anil K Dasanna

    Institute of Biological Information Processing, Forschungszentrum Juelich, Juelich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5960-4579

  3. Gerhard Gompper

    Theoretical Soft Matter and Biophysics, Institute of Complex Systems and Institute for Advanced Simulation, Forschungszentrum Jülich, Jülich, Germany
    For correspondence
    g.gompper@fz-juelich.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8904-0986

  4. Dmitry A Fedosov

    Institute of Biological Information Processing, Forschungszentrum Juelich, Juelich, Germany
    For correspondence
    d.fedosov@fz-juelich.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7469-9844

Funding

The authors declare that there was no funding for this work.

Copyright

© 2020, Hillringhaus 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. Sebastian Hillringhaus
  2. Anil K Dasanna
  3. Gerhard Gompper
  4. Dmitry A Fedosov
(2020)
Stochastic bond dynamics facilitates alignment of malaria parasite at erythrocyte membrane upon invasion
eLife 9:e56500.
https://doi.org/10.7554/eLife.56500

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https://doi.org/10.7554/eLife.56500

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    1. Physics of Living Systems

    Effect of malaria parasite shape on its alignment at erythrocyte membrane

    Anil K Dasanna, Sebastian Hillringhaus ... Dmitry A Fedosov
    Research Advance Updated

    During the blood stage of malaria pathogenesis, parasites invade healthy red blood cells (RBC) to multiply inside the host and evade the immune response. When attached to RBC, the parasite first has to align its apex with the membrane for a successful invasion. Since the parasite’s apex sits at the pointed end of an oval (egg-like) shape with a large local curvature, apical alignment is in general an energetically unfavorable process. Previously, using coarse-grained mesoscopic simulations, we have shown that optimal alignment time is achieved due to RBC membrane deformation and the stochastic nature of bond-based interactions between the parasite and RBC membrane (Hillringhaus et al., 2020). Here, we demonstrate that the parasite’s shape has a prominent effect on the alignment process. The alignment times of spherical parasites for intermediate and large bond off-rates (or weak membrane-parasite interactions) are found to be close to those of an egg-like shape. However, for small bond off-rates (or strong adhesion and large membrane deformations), the alignment time for a spherical shape increases drastically. Parasite shapes with large aspect ratios such as oblate and long prolate ellipsoids are found to exhibit very long alignment times in comparison to the egg-like shape. At a stiffened RBC, a spherical parasite aligns faster than any other investigated shape. This study shows that the original egg-like shape performs not worse for parasite alignment than other considered shapes but is more robust with respect to different adhesion interactions and RBC membrane rigidities.