Cargando…

Physical mechanisms of ESCRT-III–driven cell division

Living systems propagate by undergoing rounds of cell growth and division. Cell division is at heart a physical process that requires mechanical forces, usually exerted by assemblies of cytoskeletal polymers. Here we developed a physical model for the ESCRT-III–mediated division of archaeal cells, w...

Descripción completa

Detalles Bibliográficos
Autores principales: Harker-Kirschneck, Lena, Hafner, Anne E., Yao, Tina, Vanhille-Campos, Christian, Jiang, Xiuyun, Pulschen, Andre, Hurtig, Fredrik, Hryniuk, Dawid, Culley, Siân, Henriques, Ricardo, Baum, Buzz, Šarić, Anđela
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740586/
https://www.ncbi.nlm.nih.gov/pubmed/34983838
http://dx.doi.org/10.1073/pnas.2107763119
_version_ 1784629340288319488
author Harker-Kirschneck, Lena
Hafner, Anne E.
Yao, Tina
Vanhille-Campos, Christian
Jiang, Xiuyun
Pulschen, Andre
Hurtig, Fredrik
Hryniuk, Dawid
Culley, Siân
Henriques, Ricardo
Baum, Buzz
Šarić, Anđela
author_facet Harker-Kirschneck, Lena
Hafner, Anne E.
Yao, Tina
Vanhille-Campos, Christian
Jiang, Xiuyun
Pulschen, Andre
Hurtig, Fredrik
Hryniuk, Dawid
Culley, Siân
Henriques, Ricardo
Baum, Buzz
Šarić, Anđela
author_sort Harker-Kirschneck, Lena
collection PubMed
description Living systems propagate by undergoing rounds of cell growth and division. Cell division is at heart a physical process that requires mechanical forces, usually exerted by assemblies of cytoskeletal polymers. Here we developed a physical model for the ESCRT-III–mediated division of archaeal cells, which despite their structural simplicity share machinery and evolutionary origins with eukaryotes. By comparing the dynamics of simulations with data collected from live cell imaging experiments, we propose that this branch of life uses a previously unidentified division mechanism. Active changes in the curvature of elastic cytoskeletal filaments can lead to filament perversions and supercoiling, to drive ring constriction and deform the overlying membrane. Abscission is then completed following filament disassembly. The model was also used to explore how different adenosine triphosphate (ATP)-driven processes that govern the way the structure of the filament is changed likely impact the robustness and symmetry of the resulting division. Comparisons between midcell constriction dynamics in simulations and experiments reveal a good agreement with the process when changes in curvature are implemented at random positions along the filament, supporting this as a possible mechanism of ESCRT-III–dependent division in this system. Beyond archaea, this study pinpoints a general mechanism of cytokinesis based on dynamic coupling between a coiling filament and the membrane.
format Online
Article
Text
id pubmed-8740586
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-87405862022-01-25 Physical mechanisms of ESCRT-III–driven cell division Harker-Kirschneck, Lena Hafner, Anne E. Yao, Tina Vanhille-Campos, Christian Jiang, Xiuyun Pulschen, Andre Hurtig, Fredrik Hryniuk, Dawid Culley, Siân Henriques, Ricardo Baum, Buzz Šarić, Anđela Proc Natl Acad Sci U S A Physical Sciences Living systems propagate by undergoing rounds of cell growth and division. Cell division is at heart a physical process that requires mechanical forces, usually exerted by assemblies of cytoskeletal polymers. Here we developed a physical model for the ESCRT-III–mediated division of archaeal cells, which despite their structural simplicity share machinery and evolutionary origins with eukaryotes. By comparing the dynamics of simulations with data collected from live cell imaging experiments, we propose that this branch of life uses a previously unidentified division mechanism. Active changes in the curvature of elastic cytoskeletal filaments can lead to filament perversions and supercoiling, to drive ring constriction and deform the overlying membrane. Abscission is then completed following filament disassembly. The model was also used to explore how different adenosine triphosphate (ATP)-driven processes that govern the way the structure of the filament is changed likely impact the robustness and symmetry of the resulting division. Comparisons between midcell constriction dynamics in simulations and experiments reveal a good agreement with the process when changes in curvature are implemented at random positions along the filament, supporting this as a possible mechanism of ESCRT-III–dependent division in this system. Beyond archaea, this study pinpoints a general mechanism of cytokinesis based on dynamic coupling between a coiling filament and the membrane. National Academy of Sciences 2022-01-04 2022-01-04 /pmc/articles/PMC8740586/ /pubmed/34983838 http://dx.doi.org/10.1073/pnas.2107763119 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Physical Sciences
Harker-Kirschneck, Lena
Hafner, Anne E.
Yao, Tina
Vanhille-Campos, Christian
Jiang, Xiuyun
Pulschen, Andre
Hurtig, Fredrik
Hryniuk, Dawid
Culley, Siân
Henriques, Ricardo
Baum, Buzz
Šarić, Anđela
Physical mechanisms of ESCRT-III–driven cell division
title Physical mechanisms of ESCRT-III–driven cell division
title_full Physical mechanisms of ESCRT-III–driven cell division
title_fullStr Physical mechanisms of ESCRT-III–driven cell division
title_full_unstemmed Physical mechanisms of ESCRT-III–driven cell division
title_short Physical mechanisms of ESCRT-III–driven cell division
title_sort physical mechanisms of escrt-iii–driven cell division
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740586/
https://www.ncbi.nlm.nih.gov/pubmed/34983838
http://dx.doi.org/10.1073/pnas.2107763119
work_keys_str_mv AT harkerkirschnecklena physicalmechanismsofescrtiiidrivencelldivision
AT hafnerannee physicalmechanismsofescrtiiidrivencelldivision
AT yaotina physicalmechanismsofescrtiiidrivencelldivision
AT vanhillecamposchristian physicalmechanismsofescrtiiidrivencelldivision
AT jiangxiuyun physicalmechanismsofescrtiiidrivencelldivision
AT pulschenandre physicalmechanismsofescrtiiidrivencelldivision
AT hurtigfredrik physicalmechanismsofescrtiiidrivencelldivision
AT hryniukdawid physicalmechanismsofescrtiiidrivencelldivision
AT culleysian physicalmechanismsofescrtiiidrivencelldivision
AT henriquesricardo physicalmechanismsofescrtiiidrivencelldivision
AT baumbuzz physicalmechanismsofescrtiiidrivencelldivision
AT saricanđela physicalmechanismsofescrtiiidrivencelldivision