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Sensing the shape of a cell with reaction diffusion and energy minimization

Some dividing cells sense their shape by becoming polarized along their long axis. Cell polarity is controlled in part by polarity proteins, like Rho GTPases, cycling between active membrane-bound forms and inactive cytosolic forms, modeled as a “wave-pinning” reaction-diffusion process. Does shape...

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Detalles Bibliográficos
Autores principales: Singh, Amit R., Leadbetter, Travis, Camley, Brian A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9351364/
https://www.ncbi.nlm.nih.gov/pubmed/35905323
http://dx.doi.org/10.1073/pnas.2121302119
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author Singh, Amit R.
Leadbetter, Travis
Camley, Brian A.
author_facet Singh, Amit R.
Leadbetter, Travis
Camley, Brian A.
author_sort Singh, Amit R.
collection PubMed
description Some dividing cells sense their shape by becoming polarized along their long axis. Cell polarity is controlled in part by polarity proteins, like Rho GTPases, cycling between active membrane-bound forms and inactive cytosolic forms, modeled as a “wave-pinning” reaction-diffusion process. Does shape sensing emerge from wave pinning? We show that wave pinning senses the cell’s long axis. Simulating wave pinning on a curved surface, we find that high-activity domains migrate to peaks and troughs of the surface. For smooth surfaces, a simple rule of minimizing the domain perimeter while keeping its area fixed predicts the final position of the domain and its shape. However, when we introduce roughness to our surfaces, shape sensing can be disrupted, and high-activity domains can become localized to locations other than the global peaks and valleys of the surface. On rough surfaces, the domains of the wave-pinning model are more robust in finding the peaks and troughs than the minimization rule, although both can become trapped in steady states away from the peaks and valleys. We can control the robustness of shape sensing by altering the Rho GTPase diffusivity and the domain size. We also find that the shape-sensing properties of cell polarity models can explain how domains localize to curved regions of deformed cells. Our results help to understand the factors that allow cells to sense their shape—and the limits that membrane roughness can place on this process.
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spelling pubmed-93513642023-01-29 Sensing the shape of a cell with reaction diffusion and energy minimization Singh, Amit R. Leadbetter, Travis Camley, Brian A. Proc Natl Acad Sci U S A Physical Sciences Some dividing cells sense their shape by becoming polarized along their long axis. Cell polarity is controlled in part by polarity proteins, like Rho GTPases, cycling between active membrane-bound forms and inactive cytosolic forms, modeled as a “wave-pinning” reaction-diffusion process. Does shape sensing emerge from wave pinning? We show that wave pinning senses the cell’s long axis. Simulating wave pinning on a curved surface, we find that high-activity domains migrate to peaks and troughs of the surface. For smooth surfaces, a simple rule of minimizing the domain perimeter while keeping its area fixed predicts the final position of the domain and its shape. However, when we introduce roughness to our surfaces, shape sensing can be disrupted, and high-activity domains can become localized to locations other than the global peaks and valleys of the surface. On rough surfaces, the domains of the wave-pinning model are more robust in finding the peaks and troughs than the minimization rule, although both can become trapped in steady states away from the peaks and valleys. We can control the robustness of shape sensing by altering the Rho GTPase diffusivity and the domain size. We also find that the shape-sensing properties of cell polarity models can explain how domains localize to curved regions of deformed cells. Our results help to understand the factors that allow cells to sense their shape—and the limits that membrane roughness can place on this process. National Academy of Sciences 2022-07-29 2022-08-02 /pmc/articles/PMC9351364/ /pubmed/35905323 http://dx.doi.org/10.1073/pnas.2121302119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Singh, Amit R.
Leadbetter, Travis
Camley, Brian A.
Sensing the shape of a cell with reaction diffusion and energy minimization
title Sensing the shape of a cell with reaction diffusion and energy minimization
title_full Sensing the shape of a cell with reaction diffusion and energy minimization
title_fullStr Sensing the shape of a cell with reaction diffusion and energy minimization
title_full_unstemmed Sensing the shape of a cell with reaction diffusion and energy minimization
title_short Sensing the shape of a cell with reaction diffusion and energy minimization
title_sort sensing the shape of a cell with reaction diffusion and energy minimization
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9351364/
https://www.ncbi.nlm.nih.gov/pubmed/35905323
http://dx.doi.org/10.1073/pnas.2121302119
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