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Curvature sensing as an emergent property of multiscale assembly of septins

The ability of cells to sense and communicate their shape is central to many of their functions. Much is known about how cells generate complex shapes, yet how they sense and respond to geometric cues remains poorly understood. Septins are GTP-binding proteins that localize to sites of micrometer-sc...

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Autores principales: Shi, Wenzheng, Cannon, Kevin S., Curtis, Brandy N., Edelmaier, Christopher, Gladfelter, Amy S., Nazockdast, Ehssan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9963131/
https://www.ncbi.nlm.nih.gov/pubmed/36716363
http://dx.doi.org/10.1073/pnas.2208253120
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author Shi, Wenzheng
Cannon, Kevin S.
Curtis, Brandy N.
Edelmaier, Christopher
Gladfelter, Amy S.
Nazockdast, Ehssan
author_facet Shi, Wenzheng
Cannon, Kevin S.
Curtis, Brandy N.
Edelmaier, Christopher
Gladfelter, Amy S.
Nazockdast, Ehssan
author_sort Shi, Wenzheng
collection PubMed
description The ability of cells to sense and communicate their shape is central to many of their functions. Much is known about how cells generate complex shapes, yet how they sense and respond to geometric cues remains poorly understood. Septins are GTP-binding proteins that localize to sites of micrometer-scale membrane curvature. Assembly of septins is a multistep and multiscale process, but it is unknown how these discrete steps lead to curvature sensing. Here, we experimentally examine the time-dependent binding of septins at different curvatures and septin bulk concentrations. These experiments unexpectedly indicated that septins’ curvature preference is not absolute but rather is sensitive to the combinations of membrane curvatures present in a reaction, suggesting that there is competition between different curvatures for septin binding. To understand the physical underpinning of this result, we developed a kinetic model that connects septins’ self-assembly and curvature-sensing properties. Our experimental and modeling results are consistent with curvature-sensitive assembly being driven by cooperative associations of septin oligomers in solution with the bound septins. When combined, the work indicates that septin curvature sensing is an emergent property of the multistep, multiscale assembly of membrane-bound septins. As a result, curvature preference is not absolute and can be modulated by changing the physicochemical and geometric parameters involved in septin assembly, including bulk concentration, and the available membrane curvatures. While much geometry-sensitive assembly in biology is thought to be guided by intrinsic material properties of molecules, this is an important example of how curvature sensing can arise from multiscale assembly of polymers.
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spelling pubmed-99631312023-07-30 Curvature sensing as an emergent property of multiscale assembly of septins Shi, Wenzheng Cannon, Kevin S. Curtis, Brandy N. Edelmaier, Christopher Gladfelter, Amy S. Nazockdast, Ehssan Proc Natl Acad Sci U S A Physical Sciences The ability of cells to sense and communicate their shape is central to many of their functions. Much is known about how cells generate complex shapes, yet how they sense and respond to geometric cues remains poorly understood. Septins are GTP-binding proteins that localize to sites of micrometer-scale membrane curvature. Assembly of septins is a multistep and multiscale process, but it is unknown how these discrete steps lead to curvature sensing. Here, we experimentally examine the time-dependent binding of septins at different curvatures and septin bulk concentrations. These experiments unexpectedly indicated that septins’ curvature preference is not absolute but rather is sensitive to the combinations of membrane curvatures present in a reaction, suggesting that there is competition between different curvatures for septin binding. To understand the physical underpinning of this result, we developed a kinetic model that connects septins’ self-assembly and curvature-sensing properties. Our experimental and modeling results are consistent with curvature-sensitive assembly being driven by cooperative associations of septin oligomers in solution with the bound septins. When combined, the work indicates that septin curvature sensing is an emergent property of the multistep, multiscale assembly of membrane-bound septins. As a result, curvature preference is not absolute and can be modulated by changing the physicochemical and geometric parameters involved in septin assembly, including bulk concentration, and the available membrane curvatures. While much geometry-sensitive assembly in biology is thought to be guided by intrinsic material properties of molecules, this is an important example of how curvature sensing can arise from multiscale assembly of polymers. National Academy of Sciences 2023-01-30 2023-02-07 /pmc/articles/PMC9963131/ /pubmed/36716363 http://dx.doi.org/10.1073/pnas.2208253120 Text en Copyright © 2023 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
Shi, Wenzheng
Cannon, Kevin S.
Curtis, Brandy N.
Edelmaier, Christopher
Gladfelter, Amy S.
Nazockdast, Ehssan
Curvature sensing as an emergent property of multiscale assembly of septins
title Curvature sensing as an emergent property of multiscale assembly of septins
title_full Curvature sensing as an emergent property of multiscale assembly of septins
title_fullStr Curvature sensing as an emergent property of multiscale assembly of septins
title_full_unstemmed Curvature sensing as an emergent property of multiscale assembly of septins
title_short Curvature sensing as an emergent property of multiscale assembly of septins
title_sort curvature sensing as an emergent property of multiscale assembly of septins
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9963131/
https://www.ncbi.nlm.nih.gov/pubmed/36716363
http://dx.doi.org/10.1073/pnas.2208253120
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