Modelling membrane reshaping by staged polymerization of ESCRT-III filaments.
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 stepw...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2022-10-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://doi.org/10.1371/journal.pcbi.1010586 |
| _version_ | 1798044789520728064 |
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| author | Xiuyun Jiang Lena Harker-Kirschneck Christian Vanhille-Campos Anna-Katharina Pfitzner Elene Lominadze Aurélien Roux Buzz Baum Anđela Šarić |
| author_facet | Xiuyun Jiang Lena Harker-Kirschneck Christian Vanhille-Campos Anna-Katharina Pfitzner Elene Lominadze Aurélien Roux Buzz Baum Anđela Šarić |
| author_sort | Xiuyun Jiang |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T23:09:58Z |
| format | Article |
| id | doaj.art-922a294992104e3dae30951e44653f6d |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-04-11T23:09:58Z |
| publishDate | 2022-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-922a294992104e3dae30951e44653f6d2022-12-22T03:57:53ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-10-011810e101058610.1371/journal.pcbi.1010586Modelling membrane reshaping by staged polymerization of ESCRT-III filaments.Xiuyun JiangLena Harker-KirschneckChristian Vanhille-CamposAnna-Katharina PfitznerElene LominadzeAurélien RouxBuzz BaumAnđela ŠarićESCRT-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.https://doi.org/10.1371/journal.pcbi.1010586 |
| spellingShingle | Xiuyun Jiang Lena Harker-Kirschneck Christian Vanhille-Campos Anna-Katharina Pfitzner Elene Lominadze Aurélien Roux Buzz Baum Anđela Šarić Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. PLoS Computational Biology |
| title | Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. |
| title_full | Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. |
| title_fullStr | Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. |
| title_full_unstemmed | Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. |
| title_short | Modelling membrane reshaping by staged polymerization of ESCRT-III filaments. |
| title_sort | modelling membrane reshaping by staged polymerization of escrt iii filaments |
| url | https://doi.org/10.1371/journal.pcbi.1010586 |
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