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BAR scaffolds drive membrane fission by crowding disordered domains

Cellular membranes are continuously remodeled. The crescent-shaped bin-amphiphysin-rvs (BAR) domains remodel membranes in multiple cellular pathways. Based on studies of isolated BAR domains in vitro, the current paradigm is that BAR domain–containing proteins polymerize into cylindrical scaffolds t...

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Autores principales: Snead, Wilton T., Zeno, Wade F., Kago, Grace, Perkins, Ryan W., Richter, J Blair, Zhao, Chi, Lafer, Eileen M., Stachowiak, Jeanne C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6363457/
https://www.ncbi.nlm.nih.gov/pubmed/30504247
http://dx.doi.org/10.1083/jcb.201807119
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author Snead, Wilton T.
Zeno, Wade F.
Kago, Grace
Perkins, Ryan W.
Richter, J Blair
Zhao, Chi
Lafer, Eileen M.
Stachowiak, Jeanne C.
author_facet Snead, Wilton T.
Zeno, Wade F.
Kago, Grace
Perkins, Ryan W.
Richter, J Blair
Zhao, Chi
Lafer, Eileen M.
Stachowiak, Jeanne C.
author_sort Snead, Wilton T.
collection PubMed
description Cellular membranes are continuously remodeled. The crescent-shaped bin-amphiphysin-rvs (BAR) domains remodel membranes in multiple cellular pathways. Based on studies of isolated BAR domains in vitro, the current paradigm is that BAR domain–containing proteins polymerize into cylindrical scaffolds that stabilize lipid tubules. But in nature, proteins that contain BAR domains often also contain large intrinsically disordered regions. Using in vitro and live cell assays, here we show that full-length BAR domain–containing proteins, rather than stabilizing membrane tubules, are instead surprisingly potent drivers of membrane fission. Specifically, when BAR scaffolds assemble at membrane surfaces, their bulky disordered domains become crowded, generating steric pressure that destabilizes lipid tubules. More broadly, we observe this behavior with BAR domains that have a range of curvatures. These data suggest that the ability to concentrate disordered domains is a key driver of membrane remodeling and fission by BAR domain–containing proteins.
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spelling pubmed-63634572019-08-04 BAR scaffolds drive membrane fission by crowding disordered domains Snead, Wilton T. Zeno, Wade F. Kago, Grace Perkins, Ryan W. Richter, J Blair Zhao, Chi Lafer, Eileen M. Stachowiak, Jeanne C. J Cell Biol Research Articles Cellular membranes are continuously remodeled. The crescent-shaped bin-amphiphysin-rvs (BAR) domains remodel membranes in multiple cellular pathways. Based on studies of isolated BAR domains in vitro, the current paradigm is that BAR domain–containing proteins polymerize into cylindrical scaffolds that stabilize lipid tubules. But in nature, proteins that contain BAR domains often also contain large intrinsically disordered regions. Using in vitro and live cell assays, here we show that full-length BAR domain–containing proteins, rather than stabilizing membrane tubules, are instead surprisingly potent drivers of membrane fission. Specifically, when BAR scaffolds assemble at membrane surfaces, their bulky disordered domains become crowded, generating steric pressure that destabilizes lipid tubules. More broadly, we observe this behavior with BAR domains that have a range of curvatures. These data suggest that the ability to concentrate disordered domains is a key driver of membrane remodeling and fission by BAR domain–containing proteins. Rockefeller University Press 2019-02-04 /pmc/articles/PMC6363457/ /pubmed/30504247 http://dx.doi.org/10.1083/jcb.201807119 Text en © 2019 Snead et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Research Articles
Snead, Wilton T.
Zeno, Wade F.
Kago, Grace
Perkins, Ryan W.
Richter, J Blair
Zhao, Chi
Lafer, Eileen M.
Stachowiak, Jeanne C.
BAR scaffolds drive membrane fission by crowding disordered domains
title BAR scaffolds drive membrane fission by crowding disordered domains
title_full BAR scaffolds drive membrane fission by crowding disordered domains
title_fullStr BAR scaffolds drive membrane fission by crowding disordered domains
title_full_unstemmed BAR scaffolds drive membrane fission by crowding disordered domains
title_short BAR scaffolds drive membrane fission by crowding disordered domains
title_sort bar scaffolds drive membrane fission by crowding disordered domains
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6363457/
https://www.ncbi.nlm.nih.gov/pubmed/30504247
http://dx.doi.org/10.1083/jcb.201807119
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