Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure

Many cell division processes have been conserved throughout evolution and are being revealed by studies on model organisms such as bacteria, yeasts, and protozoa. Cellular membrane constriction is one of these processes, observed almost universally during cell division. It happens similarly in all o...

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Main Authors: Elena Beltrán-Heredia, Víctor G. Almendro-Vedia, Francisco Monroy, Francisco J. Cao
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-05-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fphys.2017.00312/full
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spelling doaj-c464ae984e304fe389ec8ce48484b5082020-11-25T00:20:57ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2017-05-01810.3389/fphys.2017.00312252567Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic PressureElena Beltrán-Heredia0Elena Beltrán-Heredia1Víctor G. Almendro-Vedia2Víctor G. Almendro-Vedia3Francisco Monroy4Francisco Monroy5Francisco J. Cao6Departamento de Física Atómica, Molecular y Nuclear, Universidad Complutense de MadridMadrid, SpainDepartamento de Química Física I, Universidad Complutense de MadridMadrid, SpainDepartamento de Física Atómica, Molecular y Nuclear, Universidad Complutense de MadridMadrid, SpainDepartamento de Química Física I, Universidad Complutense de MadridMadrid, SpainDepartamento de Química Física I, Universidad Complutense de MadridMadrid, SpainTranslational Biophysics, Instituto de Investigación Sanitaria Hospital 12 de Octubre (imas12)Madrid, SpainDepartamento de Física Atómica, Molecular y Nuclear, Universidad Complutense de MadridMadrid, SpainMany cell division processes have been conserved throughout evolution and are being revealed by studies on model organisms such as bacteria, yeasts, and protozoa. Cellular membrane constriction is one of these processes, observed almost universally during cell division. It happens similarly in all organisms through a mechanical pathway synchronized with the sequence of cytokinetic events in the cell interior. Arguably, such a mechanical process is mastered by the coordinated action of a constriction machinery fueled by biochemical energy in conjunction with the passive mechanics of the cellular membrane. Independently of the details of the constriction engine, the membrane component responds against deformation by minimizing the elastic energy at every constriction state following a pathway still unknown. In this paper, we address a theoretical study of the mechanics of membrane constriction in a simplified model that describes a homogeneous membrane vesicle in the regime where mechanical work due to osmotic pressure, surface tension, and bending energy are comparable. We develop a general method to find approximate analytical expressions for the main descriptors of a symmetrically constricted vesicle. Analytical solutions are obtained by combining a perturbative expansion for small deformations with a variational approach that was previously demonstrated valid at the reference state of an initially spherical vesicle at isotonic conditions. The analytic approximate results are compared with the exact solution obtained from numerical computations, getting a good agreement for all the computed quantities (energy, area, volume, constriction force). We analyze the effects of the spontaneous curvature, the surface tension and the osmotic pressure in these quantities, focusing especially on the constriction force. The more favorable conditions for vesicle constriction are determined, obtaining that smaller constriction forces are required for positive spontaneous curvatures, low or negative membrane tension and hypertonic media. Conditions for spontaneous constriction at a given constriction force are also determined. The implications of these results for biological cell division are discussed. This work contributes to a better quantitative understanding of the mechanical pathway of cellular division, and could assist the design of artificial divisomes in vesicle-based self-actuated microsystems obtained from synthetic biology approaches.http://journal.frontiersin.org/article/10.3389/fphys.2017.00312/fullcell divisionmembrane constrictionbending energyspontaneous curvaturesurface tensionosmotic pressure
collection DOAJ
language English
format Article
sources DOAJ
author Elena Beltrán-Heredia
Elena Beltrán-Heredia
Víctor G. Almendro-Vedia
Víctor G. Almendro-Vedia
Francisco Monroy
Francisco Monroy
Francisco J. Cao
spellingShingle Elena Beltrán-Heredia
Elena Beltrán-Heredia
Víctor G. Almendro-Vedia
Víctor G. Almendro-Vedia
Francisco Monroy
Francisco Monroy
Francisco J. Cao
Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure
Frontiers in Physiology
cell division
membrane constriction
bending energy
spontaneous curvature
surface tension
osmotic pressure
author_facet Elena Beltrán-Heredia
Elena Beltrán-Heredia
Víctor G. Almendro-Vedia
Víctor G. Almendro-Vedia
Francisco Monroy
Francisco Monroy
Francisco J. Cao
author_sort Elena Beltrán-Heredia
title Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure
title_short Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure
title_full Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure
title_fullStr Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure
title_full_unstemmed Modeling the Mechanics of Cell Division: Influence of Spontaneous Membrane Curvature, Surface Tension, and Osmotic Pressure
title_sort modeling the mechanics of cell division: influence of spontaneous membrane curvature, surface tension, and osmotic pressure
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2017-05-01
description Many cell division processes have been conserved throughout evolution and are being revealed by studies on model organisms such as bacteria, yeasts, and protozoa. Cellular membrane constriction is one of these processes, observed almost universally during cell division. It happens similarly in all organisms through a mechanical pathway synchronized with the sequence of cytokinetic events in the cell interior. Arguably, such a mechanical process is mastered by the coordinated action of a constriction machinery fueled by biochemical energy in conjunction with the passive mechanics of the cellular membrane. Independently of the details of the constriction engine, the membrane component responds against deformation by minimizing the elastic energy at every constriction state following a pathway still unknown. In this paper, we address a theoretical study of the mechanics of membrane constriction in a simplified model that describes a homogeneous membrane vesicle in the regime where mechanical work due to osmotic pressure, surface tension, and bending energy are comparable. We develop a general method to find approximate analytical expressions for the main descriptors of a symmetrically constricted vesicle. Analytical solutions are obtained by combining a perturbative expansion for small deformations with a variational approach that was previously demonstrated valid at the reference state of an initially spherical vesicle at isotonic conditions. The analytic approximate results are compared with the exact solution obtained from numerical computations, getting a good agreement for all the computed quantities (energy, area, volume, constriction force). We analyze the effects of the spontaneous curvature, the surface tension and the osmotic pressure in these quantities, focusing especially on the constriction force. The more favorable conditions for vesicle constriction are determined, obtaining that smaller constriction forces are required for positive spontaneous curvatures, low or negative membrane tension and hypertonic media. Conditions for spontaneous constriction at a given constriction force are also determined. The implications of these results for biological cell division are discussed. This work contributes to a better quantitative understanding of the mechanical pathway of cellular division, and could assist the design of artificial divisomes in vesicle-based self-actuated microsystems obtained from synthetic biology approaches.
topic cell division
membrane constriction
bending energy
spontaneous curvature
surface tension
osmotic pressure
url http://journal.frontiersin.org/article/10.3389/fphys.2017.00312/full
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