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Surface model of the human red blood cell simulating changes in membrane curvature under strain

We present mathematical simulations of shapes of red blood cells (RBCs) and their cytoskeleton when they are subjected to linear strain. The cell surface is described by a previously reported quartic equation in three dimensional (3D) Cartesian space. Using recently available functions in Mathematic...

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Autores principales: Kuchel, Philip W., Cox, Charles D., Daners, Daniel, Shishmarev, Dmitry, Galvosas, Petrik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8249411/
https://www.ncbi.nlm.nih.gov/pubmed/34211012
http://dx.doi.org/10.1038/s41598-021-92699-7
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author Kuchel, Philip W.
Cox, Charles D.
Daners, Daniel
Shishmarev, Dmitry
Galvosas, Petrik
author_facet Kuchel, Philip W.
Cox, Charles D.
Daners, Daniel
Shishmarev, Dmitry
Galvosas, Petrik
author_sort Kuchel, Philip W.
collection PubMed
description We present mathematical simulations of shapes of red blood cells (RBCs) and their cytoskeleton when they are subjected to linear strain. The cell surface is described by a previously reported quartic equation in three dimensional (3D) Cartesian space. Using recently available functions in Mathematica to triangularize the surfaces we computed four types of curvature of the membrane. We also mapped changes in mesh-triangle area and curvatures as the RBCs were distorted. The highly deformable red blood cell (erythrocyte; RBC) responds to mechanically imposed shape changes with enhanced glycolytic flux and cation transport. Such morphological changes are produced experimentally by suspending the cells in a gelatin gel, which is then elongated or compressed in a custom apparatus inside an NMR spectrometer. A key observation is the extent to which the maximum and minimum Principal Curvatures are localized symmetrically in patches at the poles or equators and distributed in rings around the main axis of the strained RBC. Changes on the nanometre to micro-meter scale of curvature, suggest activation of only a subset of the intrinsic mechanosensitive cation channels, Piezo1, during experiments carried out with controlled distortions, which persist for many hours. This finding is relevant to a proposal for non-uniform distribution of Piezo1 molecules around the RBC membrane. However, if the curvature that gates Piezo1 is at a very fine length scale, then membrane tension will determine local curvature; so, curvatures as computed here (in contrast to much finer surface irregularities) may not influence Piezo1 activity. Nevertheless, our analytical methods can be extended address these new mechanistic proposals. The geometrical reorganization of the simulated cytoskeleton informs ideas about the mechanism of concerted metabolic and cation-flux responses of the RBC to mechanically imposed shape changes.
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spelling pubmed-82494112021-07-06 Surface model of the human red blood cell simulating changes in membrane curvature under strain Kuchel, Philip W. Cox, Charles D. Daners, Daniel Shishmarev, Dmitry Galvosas, Petrik Sci Rep Article We present mathematical simulations of shapes of red blood cells (RBCs) and their cytoskeleton when they are subjected to linear strain. The cell surface is described by a previously reported quartic equation in three dimensional (3D) Cartesian space. Using recently available functions in Mathematica to triangularize the surfaces we computed four types of curvature of the membrane. We also mapped changes in mesh-triangle area and curvatures as the RBCs were distorted. The highly deformable red blood cell (erythrocyte; RBC) responds to mechanically imposed shape changes with enhanced glycolytic flux and cation transport. Such morphological changes are produced experimentally by suspending the cells in a gelatin gel, which is then elongated or compressed in a custom apparatus inside an NMR spectrometer. A key observation is the extent to which the maximum and minimum Principal Curvatures are localized symmetrically in patches at the poles or equators and distributed in rings around the main axis of the strained RBC. Changes on the nanometre to micro-meter scale of curvature, suggest activation of only a subset of the intrinsic mechanosensitive cation channels, Piezo1, during experiments carried out with controlled distortions, which persist for many hours. This finding is relevant to a proposal for non-uniform distribution of Piezo1 molecules around the RBC membrane. However, if the curvature that gates Piezo1 is at a very fine length scale, then membrane tension will determine local curvature; so, curvatures as computed here (in contrast to much finer surface irregularities) may not influence Piezo1 activity. Nevertheless, our analytical methods can be extended address these new mechanistic proposals. The geometrical reorganization of the simulated cytoskeleton informs ideas about the mechanism of concerted metabolic and cation-flux responses of the RBC to mechanically imposed shape changes. Nature Publishing Group UK 2021-07-01 /pmc/articles/PMC8249411/ /pubmed/34211012 http://dx.doi.org/10.1038/s41598-021-92699-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Kuchel, Philip W.
Cox, Charles D.
Daners, Daniel
Shishmarev, Dmitry
Galvosas, Petrik
Surface model of the human red blood cell simulating changes in membrane curvature under strain
title Surface model of the human red blood cell simulating changes in membrane curvature under strain
title_full Surface model of the human red blood cell simulating changes in membrane curvature under strain
title_fullStr Surface model of the human red blood cell simulating changes in membrane curvature under strain
title_full_unstemmed Surface model of the human red blood cell simulating changes in membrane curvature under strain
title_short Surface model of the human red blood cell simulating changes in membrane curvature under strain
title_sort surface model of the human red blood cell simulating changes in membrane curvature under strain
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8249411/
https://www.ncbi.nlm.nih.gov/pubmed/34211012
http://dx.doi.org/10.1038/s41598-021-92699-7
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