Modelling membrane reshaping by staged polymerization of ESCRT-III filaments

Jiang X, Harker-Kirschneck L, Vanhille-Campos CE, Pfitzner A-K, Lominadze E, Roux A, Baum B, Šarić A. 2022. Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. PLOS Computational Biology. 18(10), e1010586.

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Journal Article | Published | English

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Author
Jiang, Xiuyun; Harker-Kirschneck, Lena; Vanhille-Campos, Christian EduardoISTA; Pfitzner, Anna-Katharina; Lominadze, Elene; Roux, Aurélien; Baum, Buzz; Šarić, AnđelaISTA
Department
Abstract
ESCRT-III filaments are composite cytoskeletal polymers that can constrict and cut cell membranes from the inside of the membrane neck. Membrane-bound ESCRT-III filaments undergo a series of dramatic composition and geometry changes in the presence of an ATP-consuming Vps4 enzyme, which causes stepwise changes in the membrane morphology. We set out to understand the physical mechanisms involved in translating the changes in ESCRT-III polymer composition into membrane deformation. We have built a coarse-grained model in which ESCRT-III polymers of different geometries and mechanical properties are allowed to copolymerise and bind to a deformable membrane. By modelling ATP-driven stepwise depolymerisation of specific polymers, we identify mechanical regimes in which changes in filament composition trigger the associated membrane transition from a flat to a buckled state, and then to a tubule state that eventually undergoes scission to release a small cargo-loaded vesicle. We then characterise how the location and kinetics of polymer loss affects the extent of membrane deformation and the efficiency of membrane neck scission. Our results identify the near-minimal mechanical conditions for the operation of shape-shifting composite polymers that sever membrane necks.
Publishing Year
Date Published
2022-10-17
Journal Title
PLOS Computational Biology
Publisher
Public Library of Science
Acknowledgement
A.S . received an award from European Research Council (https://erc.europa.eu, “NEPA" 802960), and an award from the Royal Society (https://royalsociety.org, UF160266). L. H.-K. received an award from the Biotechnology and Biological Sciences Research Council (https:// www.ukri.org/councils/bbsrc/). E. L. received an award from the University College London (https://www.ucl.ac.uk/biophysics/news/2022/feb/applications-biop-brian-duff-and-ipls-summerundergraduate-studentships-now-open, Brian Duff Undergraduate Summer Research Studentship). B.B. and A.S. received an award from Volkswagen Foundation https://www.volkswagenstiftung.de/en/foundation, Az 96727), and an award from Medical Research Council (https://www.ukri.org/councils/mrc, MC_CF1226). A. R. received an award from the Swiss National Fund for Research (https://www.snf.ch/en, 31003A_130520, 31003A_149975, and 31003A_173087) and an award from the European Research Council Consolidator (https://erc.europa.eu, 311536). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Volume
18
Issue
10
Article Number
e1010586
ISSN
IST-REx-ID

Cite this

Jiang X, Harker-Kirschneck L, Vanhille-Campos CE, et al. Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. PLOS Computational Biology. 2022;18(10). doi:10.1371/journal.pcbi.1010586
Jiang, X., Harker-Kirschneck, L., Vanhille-Campos, C. E., Pfitzner, A.-K., Lominadze, E., Roux, A., … Šarić, A. (2022). Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. PLOS Computational Biology. Public Library of Science. https://doi.org/10.1371/journal.pcbi.1010586
Jiang, Xiuyun, Lena Harker-Kirschneck, Christian Eduardo Vanhille-Campos, Anna-Katharina Pfitzner, Elene Lominadze, Aurélien Roux, Buzz Baum, and Anđela Šarić. “Modelling Membrane Reshaping by Staged Polymerization of ESCRT-III Filaments.” PLOS Computational Biology. Public Library of Science, 2022. https://doi.org/10.1371/journal.pcbi.1010586.
X. Jiang et al., “Modelling membrane reshaping by staged polymerization of ESCRT-III filaments,” PLOS Computational Biology, vol. 18, no. 10. Public Library of Science, 2022.
Jiang X, Harker-Kirschneck L, Vanhille-Campos CE, Pfitzner A-K, Lominadze E, Roux A, Baum B, Šarić A. 2022. Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. PLOS Computational Biology. 18(10), e1010586.
Jiang, Xiuyun, et al. “Modelling Membrane Reshaping by Staged Polymerization of ESCRT-III Filaments.” PLOS Computational Biology, vol. 18, no. 10, e1010586, Public Library of Science, 2022, doi:10.1371/journal.pcbi.1010586.
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2023-01-24
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