Physical mechanisms of ESCRT-III–driven cell division

Lena Harker-Kirschneck; Anne E. Hafner; Tina Yao; Christian Vanhille-Campos; Xiuyun Jiang; Andre Pulschen; Fredrik Hurtig; Dawid Hryniuk; Siân Culley; Ricardo Henriques; Buzz Baum; Andela Šarić

doi:10.1073/pnas.2107763119

Physical mechanisms of ESCRT-III–driven cell division

Lena Harker-Kirschneck, Anne E. Hafner, Tina Yao, Christian Vanhille-Campos, Xiuyun Jiang, Andre Pulschen, Fredrik Hurtig, Dawid Hryniuk, Siân Culley, Ricardo Henriques, Buzz Baum, Andela Šarić^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

19 Citations (Scopus)

Abstract

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.

Original language	English
Article number	e2107763119
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	1
DOIs	https://doi.org/10.1073/pnas.2107763119
Publication status	Published - 4 Jan 2022

Keywords

Archaea
Cell division
ESCRT-III
Membrane simulations
Soft matter

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Harker-Kirschneck, L., Hafner, A. E., Yao, T., Vanhille-Campos, C., Jiang, X., Pulschen, A., Hurtig, F., Hryniuk, D., Culley, S., Henriques, R., Baum, B., & Šarić, A. (2022). Physical mechanisms of ESCRT-III–driven cell division. Proceedings of the National Academy of Sciences of the United States of America, 119(1), Article e2107763119. https://doi.org/10.1073/pnas.2107763119

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title = "Physical mechanisms of ESCRT-III–driven cell division",

abstract = "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.",

keywords = "Archaea, Cell division, ESCRT-III, Membrane simulations, Soft matter",

author = "Lena Harker-Kirschneck and Hafner, {Anne E.} and Tina Yao and Christian Vanhille-Campos and Xiuyun Jiang and Andre Pulschen and Fredrik Hurtig and Dawid Hryniuk and Si{\^a}n Culley and Ricardo Henriques and Buzz Baum and Andela {\v S}ari{\'c}",

note = "Funding Information: ACKNOWLEDGMENTS. We acknowledge support from the Biotechnology and Biological Sciences Research Council (L.H.-K.), Engineering and Physical Sciences Research Council (A.E.H), University College London Institute for the Physics of Living Systems (T.Y. and D.H.), Wellcome Trust Grant 203276/Z/16/Z (to A.P., S.C., R.H., and B.B.), Volkswagen Foundation Grant Az 96727 (to A.P., B.B., and A.{\v S}.), the Medical Research Council Grant MC_CF1226 (to R.H., B.B., and A.{\v S}.), the Life Science Moore-Simons foundation grant (735929LPI), the European Research Council Grant “NEPA” 802960 (to X.J. and A.{\v S}.), the Royal Society (C.V.-C. and A.{\v S}.), and the UK Materials and Molecular Modelling Hub for computational resources (EP/P020194/1). Publisher Copyright: {\textcopyright} 2022 National Academy of Sciences. All rights reserved.",

year = "2022",

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doi = "10.1073/pnas.2107763119",

language = "English",

volume = "119",

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T1 - Physical mechanisms of ESCRT-III–driven cell division

AU - Harker-Kirschneck, Lena

AU - Hafner, Anne E.

AU - Yao, Tina

AU - Vanhille-Campos, Christian

AU - Jiang, Xiuyun

AU - Pulschen, Andre

AU - Hurtig, Fredrik

AU - Hryniuk, Dawid

AU - Culley, Siân

AU - Henriques, Ricardo

AU - Baum, Buzz

AU - Šarić, Andela

N1 - Funding Information: ACKNOWLEDGMENTS. We acknowledge support from the Biotechnology and Biological Sciences Research Council (L.H.-K.), Engineering and Physical Sciences Research Council (A.E.H), University College London Institute for the Physics of Living Systems (T.Y. and D.H.), Wellcome Trust Grant 203276/Z/16/Z (to A.P., S.C., R.H., and B.B.), Volkswagen Foundation Grant Az 96727 (to A.P., B.B., and A.Š.), the Medical Research Council Grant MC_CF1226 (to R.H., B.B., and A.Š.), the Life Science Moore-Simons foundation grant (735929LPI), the European Research Council Grant “NEPA” 802960 (to X.J. and A.Š.), the Royal Society (C.V.-C. and A.Š.), and the UK Materials and Molecular Modelling Hub for computational resources (EP/P020194/1). Publisher Copyright: © 2022 National Academy of Sciences. All rights reserved.

PY - 2022/1/4

Y1 - 2022/1/4

N2 - 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.

AB - 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.

KW - Archaea

KW - Cell division

KW - ESCRT-III

KW - Membrane simulations

KW - Soft matter

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DO - 10.1073/pnas.2107763119

M3 - Article

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AN - SCOPUS:85122703242

SN - 0027-8424

VL - 119

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 1

M1 - e2107763119

ER -

Physical mechanisms of ESCRT-III–driven cell division

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