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Balance of microtubule stiffness and cortical tension determines the size of blood cells with marginal band across species

View ORCID ProfileSerge Dmitrieff, Adolfo Alsina, Aastha Mathur, François Nedéléc
doi: https://doi.org/10.1101/086728
Serge Dmitrieff
aCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
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  • ORCID record for Serge Dmitrieff
Adolfo Alsina
aCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
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Aastha Mathur
aCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
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François Nedéléc
aCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
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  • For correspondence: nedelec@embl.de
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Abstract

The fast blood stream of animals is associated with large shear stresses. Consequently, blood cells have evolved a special morphology and a specific internal architecture allowing them to maintain their integrity over several weeks. For instance, non-mammalian red blood cells, mammalian erythroblasts and platelets have a peripheral ring of microtubules, called the marginal band, that flattens the overall cell morphology by pushing on the cell cortex. In this article, we model how the shape of these cells stems from the balance between marginal band elasticity and cortical tension. We predict that the diameter of the cell scales with the total microtubule polymer, and verify the predicted law across a wide range of species. Our analysis also shows that the combination of the marginal band rigidity and cortical tension increases the ability of the cell to withstand forces without deformation. Finally, we model the marginal band coiling that occurs during the disc-to-sphere transition observed for instance at the onset of blood platelet activation. We show that when cortical tension increases faster than crosslinkers can unbind, the marginal band will coil, whereas if the tension increases slower, the marginal band may shorten as microtubules slide relative to each other.

Significance Statement Many blood cells have a discoidal shape, which is essential for them to function properly within the organism. For some cells, such as blood platelets, this shape is due to the interplay between the elasticity of the marginal band, which is a closed ring of stiff filaments called microtubules, and the tension of the cell cortex, a polymer scaffold associated with the plasma membrane. Dmitrieff et al. examined how cell size is determined by the mechanical balance between these two components. Remarkably, the theory is confirmed over nearly three orders of magnitudes, by data collected from 25 species. The theory also shows how the composite structure is adapted to resist transient mechanical challenges, as encountered in the blood stream.

Footnotes

  • Conceived and designed the work: FN SD. Performed the theory: SD AA. Performed the experiments: AM. Analyzed data: SD AA AM. Wrote the paper: FN SD AM.

  • The authors declare no conflict of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 09, 2016.
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Balance of microtubule stiffness and cortical tension determines the size of blood cells with marginal band across species
Serge Dmitrieff, Adolfo Alsina, Aastha Mathur, François Nedéléc
bioRxiv 086728; doi: https://doi.org/10.1101/086728
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Balance of microtubule stiffness and cortical tension determines the size of blood cells with marginal band across species
Serge Dmitrieff, Adolfo Alsina, Aastha Mathur, François Nedéléc
bioRxiv 086728; doi: https://doi.org/10.1101/086728

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