Image-based model of the spectrin cytoskeleton for red blood cell simulation
Abstract
We simulate deformable red blood cells in the microcirculation using the immersed boundary method with a cytoskeletal model that incorporates structural details revealed by tomographic images. The elasticity of red blood cells is known to be supplied by both their lipid bilayer membranes, which resist bending and local changes in area, and their cytoskeletons, which resist in-plane shear. The cytoskeleton consists of spectrin tetramers that are tethered to the lipid bilayer by ankyrin and by actin-based junctional complexes. We model the cytoskeleton as a random geometric graph, with nodes corresponding to junctional complexes and with edges corresponding to spectrin tetramers such that the edge lengths are given by the end-to-end distances between nodes. The statistical properties of this graph are based on distributions gathered from three-dimensional tomographic images of the cytoskeleton by a segmentation algorithm. We show that the elastic response of our model cytoskeleton, in which the spectrin polymers are treated as entropic springs, is in good agreement with the experimentally measured shear modulus. By simulating red blood cells in flow with the immersed boundary method, we compare this discrete cytoskeletal model to an existing continuum model and predict the extent to which dynamic spectrin network connectivity can protectmore »
- Authors:
-
[1];
[2];
- Harvard Univ., Cambridge, MA (United States)
- New York Univ. (NYU), NY (United States)
- Univ. of Pennsylvania, Philadelphia, PA (United States)
- Publication Date:
- Research Org.:
- Krell Inst., Ames, Iowa (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1499877
- Grant/Contract Number:
- FG02-97ER25308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Computational Biology (Online)
- Additional Journal Information:
- Journal Name: PLoS Computational Biology (Online); Journal Volume: 13; Journal Issue: 10; Journal ID: ISSN 1553-7358
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Fai, Thomas G., Leo-Macias, Alejandra, Stokes, David L., Peskin, Charles S., and Diamond, Scott L. Image-based model of the spectrin cytoskeleton for red blood cell simulation. United States: N. p., 2017.
Web. doi:10.1371/journal.pcbi.1005790.
Fai, Thomas G., Leo-Macias, Alejandra, Stokes, David L., Peskin, Charles S., & Diamond, Scott L. Image-based model of the spectrin cytoskeleton for red blood cell simulation. United States. https://doi.org/10.1371/journal.pcbi.1005790
Fai, Thomas G., Leo-Macias, Alejandra, Stokes, David L., Peskin, Charles S., and Diamond, Scott L. Mon .
"Image-based model of the spectrin cytoskeleton for red blood cell simulation". United States. https://doi.org/10.1371/journal.pcbi.1005790. https://www.osti.gov/servlets/purl/1499877.
@article{osti_1499877,
title = {Image-based model of the spectrin cytoskeleton for red blood cell simulation},
author = {Fai, Thomas G. and Leo-Macias, Alejandra and Stokes, David L. and Peskin, Charles S. and Diamond, Scott L.},
abstractNote = {We simulate deformable red blood cells in the microcirculation using the immersed boundary method with a cytoskeletal model that incorporates structural details revealed by tomographic images. The elasticity of red blood cells is known to be supplied by both their lipid bilayer membranes, which resist bending and local changes in area, and their cytoskeletons, which resist in-plane shear. The cytoskeleton consists of spectrin tetramers that are tethered to the lipid bilayer by ankyrin and by actin-based junctional complexes. We model the cytoskeleton as a random geometric graph, with nodes corresponding to junctional complexes and with edges corresponding to spectrin tetramers such that the edge lengths are given by the end-to-end distances between nodes. The statistical properties of this graph are based on distributions gathered from three-dimensional tomographic images of the cytoskeleton by a segmentation algorithm. We show that the elastic response of our model cytoskeleton, in which the spectrin polymers are treated as entropic springs, is in good agreement with the experimentally measured shear modulus. By simulating red blood cells in flow with the immersed boundary method, we compare this discrete cytoskeletal model to an existing continuum model and predict the extent to which dynamic spectrin network connectivity can protect against failure in the case of a red cell subjected to an applied strain. As a result, the methods presented here could form the basis of disease- and patient-specific computational studies of hereditary diseases affecting the red cell cytoskeleton.},
doi = {10.1371/journal.pcbi.1005790},
journal = {PLoS Computational Biology (Online)},
number = 10,
volume = 13,
place = {United States},
year = {Mon Oct 09 00:00:00 EDT 2017},
month = {Mon Oct 09 00:00:00 EDT 2017}
}
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Quantifying the biophysical characteristics of Plasmodium-falciparum -parasitized red blood cells in microcirculation
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Lipid bilayer and cytoskeletal interactions in a red blood cell
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Multiple stiffening effects of nanoscale knobs on human red blood cells infected with Plasmodium falciparum malaria parasite
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Actin, Spectrin, and Associated Proteins Form a Periodic Cytoskeletal Structure in Axons
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Molecular maps of red cell deformation: hidden elasticity and in situ connectivity
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Multiscale Modeling of Red Blood Cell Mechanics and Blood Flow in Malaria
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Physically-Induced Cytoskeleton Remodeling of Cells in Three-Dimensional Culture
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Stepwise Unfolding of Ankyrin Repeats in a Single Protein Revealed by Atomic Force Microscopy
journal, February 2006
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Tank-Tread Frequency of the Red Cell Membrane: Dependence on the Viscosity of the Suspending Medium
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- Biophysical Journal, Vol. 93, Issue 7
Investigating dynamical deformations of tumor cells in circulation: predictions from a theoretical model
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Red Blood Cell Cytoskeleton Tomography Data
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