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Title: MD/DPD Multiscale Framework for Predicting Morphology and Stresses of Red Blood Cells in Health and Disease

Abstract

Healthy red blood cells (RBCs) have remarkable deformability, squeezing through narrow capillaries as small as 3 microns in diameter without any damage. However, in many hematological disorders the spectrin network and lipid bilayer of diseased RBCs may be significantly altered, leading to impaired functionality including loss of deformability. We employ a two-component whole-cell multiscale model to quantify the biomechanical characteristics of the healthy and diseased RBCs, including Plasmodium falciparum-infected RBCs (Pf-RBCs) and defective RBCs in hereditary disorders, such as spherocytosis and elliptocytosis. In particular, we develop a two-step multiscale framework based on coarse-grained molecular dynamics (CGMD) and dissipative particle dynamics (DPD) to predict the static and dynamic responses of RBCs subject to tensile forcing, using experimental information only on the structural defects in the lipid bilayer, cytoskeleton, and their interaction. We first employ CGMD on a small RBC patch to compute the shear modulus, bending stiffness, and network parameters, which are subsequently used as input to a whole-cell DPD model to predict the RBC shape and corresponding stress field. For Pf-RBCs at trophozoite and schizont stages, the presence of cytoadherent knobs elevates the shear response in the lipid bilayer and stiffens the RBC membrane. For RBCs in spherocytosis and elliptocytosis,more » the bilayer-cytoskeleton interaction is weakened, resulting in substantial increase of the tensile stress in the lipid bilayer. Furthermore, we investigate the transient behavior of stretching deformation and shape relaxation of the normal and defective RBCs. Different from the normal RBCs possessing high elasticity, our simulations reveal that the defective RBCs respond irreversibly, i.e., they lose their ability to recover the normal biconcave shape in successive loading cycles of stretching and relaxation. Our findings provide fundamental insights into the microstructure and biomechanics of RBCs, and demonstrate that the two-step multiscale framework presented here can be used effectively for in silico studies of hematological disorders based on first principles and patient-specific experimental input at the protein level.« less

Authors:
 [1];  [1];  [1];  [1];
  1. Brown Univ., Providence, RI (United States). Div. of Applied Mathematics
Publication Date:
Research Org.:
Argonne National Lab (ANL), Lemont, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Innovative and Novel Computational Impact on Theory and Experiment (INCITE)
OSTI Identifier:
1627248
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Computational Biology (Online)
Additional Journal Information:
Journal Name: PLoS Computational Biology (Online); Journal Volume: 12; Journal Issue: 10; Journal ID: ISSN 1553-7358
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
Biochemistry & Molecular Biology; Mathematical & Computational Biology

Citation Formats

Chang, Hung-Yu, Li, Xuejin, Li, He, Karniadakis, George Em, and McCulloch, Andrew D. MD/DPD Multiscale Framework for Predicting Morphology and Stresses of Red Blood Cells in Health and Disease. United States: N. p., 2016. Web. doi:10.1371/journal.pcbi.1005173.
Chang, Hung-Yu, Li, Xuejin, Li, He, Karniadakis, George Em, & McCulloch, Andrew D. MD/DPD Multiscale Framework for Predicting Morphology and Stresses of Red Blood Cells in Health and Disease. United States. https://doi.org/10.1371/journal.pcbi.1005173
Chang, Hung-Yu, Li, Xuejin, Li, He, Karniadakis, George Em, and McCulloch, Andrew D. Fri . "MD/DPD Multiscale Framework for Predicting Morphology and Stresses of Red Blood Cells in Health and Disease". United States. https://doi.org/10.1371/journal.pcbi.1005173. https://www.osti.gov/servlets/purl/1627248.
@article{osti_1627248,
title = {MD/DPD Multiscale Framework for Predicting Morphology and Stresses of Red Blood Cells in Health and Disease},
author = {Chang, Hung-Yu and Li, Xuejin and Li, He and Karniadakis, George Em and McCulloch, Andrew D.},
abstractNote = {Healthy red blood cells (RBCs) have remarkable deformability, squeezing through narrow capillaries as small as 3 microns in diameter without any damage. However, in many hematological disorders the spectrin network and lipid bilayer of diseased RBCs may be significantly altered, leading to impaired functionality including loss of deformability. We employ a two-component whole-cell multiscale model to quantify the biomechanical characteristics of the healthy and diseased RBCs, including Plasmodium falciparum-infected RBCs (Pf-RBCs) and defective RBCs in hereditary disorders, such as spherocytosis and elliptocytosis. In particular, we develop a two-step multiscale framework based on coarse-grained molecular dynamics (CGMD) and dissipative particle dynamics (DPD) to predict the static and dynamic responses of RBCs subject to tensile forcing, using experimental information only on the structural defects in the lipid bilayer, cytoskeleton, and their interaction. We first employ CGMD on a small RBC patch to compute the shear modulus, bending stiffness, and network parameters, which are subsequently used as input to a whole-cell DPD model to predict the RBC shape and corresponding stress field. For Pf-RBCs at trophozoite and schizont stages, the presence of cytoadherent knobs elevates the shear response in the lipid bilayer and stiffens the RBC membrane. For RBCs in spherocytosis and elliptocytosis, the bilayer-cytoskeleton interaction is weakened, resulting in substantial increase of the tensile stress in the lipid bilayer. Furthermore, we investigate the transient behavior of stretching deformation and shape relaxation of the normal and defective RBCs. Different from the normal RBCs possessing high elasticity, our simulations reveal that the defective RBCs respond irreversibly, i.e., they lose their ability to recover the normal biconcave shape in successive loading cycles of stretching and relaxation. Our findings provide fundamental insights into the microstructure and biomechanics of RBCs, and demonstrate that the two-step multiscale framework presented here can be used effectively for in silico studies of hematological disorders based on first principles and patient-specific experimental input at the protein level.},
doi = {10.1371/journal.pcbi.1005173},
journal = {PLoS Computational Biology (Online)},
number = 10,
volume = 12,
place = {United States},
year = {Fri Oct 28 00:00:00 EDT 2016},
month = {Fri Oct 28 00:00:00 EDT 2016}
}

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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
journal, April 2015

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Configurations of fluid membranes and vesicles
journal, February 1997


Scanning electron microscope-analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum-infected erythrocytes.
journal, September 1983

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Blood–plasma separation in Y-shaped bifurcating microfluidic channels: a dissipative particle dynamics simulation study
journal, April 2012


Patient-specific blood rheology in sickle-cell anaemia
journal, February 2016


Vesiculation of healthy and defective red blood cells
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Accurate Coarse-Grained Modeling of Red Blood Cells
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journal, March 2008


The hereditary elliptocytoses: clinical and linkage data
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Hemoglobins S and C Interfere with Actin Remodeling in Plasmodium falciparum-Infected Erythrocytes
journal, November 2011


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journal, July 2010


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journal, March 1987


Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells
journal, February 2002


Multiscale Modeling of Red Blood Cell Mechanics and Blood Flow in Malaria
journal, December 2011


Life Cycle-Dependent Cytoskeletal Modifications in Plasmodium falciparum Infected Erythrocytes
journal, April 2013


Elastic Properties of Lipid Bilayers: Theory and Possible Experiments
journal, December 1973


Spectrin-Level Modeling of the Cytoskeleton and Optical Tweezers Stretching of the Erythrocyte
journal, May 2005


Integral Protein Linkage and the Bilayer-Skeletal Separation Energy in Red Blood Cells
journal, August 2008


Works referencing / citing this record:

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