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Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting
One enigma in biology is the generation, sensing and maintenance of membrane curvature. Curvature-mediating proteins have been shown to induce specific membrane shapes by direct insertion and nanoscopic scaffolding, while the cytoskeletal motors exert forces indirectly through microtubule and actin...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6656732/ https://www.ncbi.nlm.nih.gov/pubmed/31341165 http://dx.doi.org/10.1038/s41467-019-11268-9 |
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author | Rogez, Benoit Würthner, Laeschkir Petrova, Anastasiia B. Zierhut, Felix B. Saczko-Brack, Dario Huergo, Maria-Ana Batters, Christopher Frey, Erwin Veigel, Claudia |
author_facet | Rogez, Benoit Würthner, Laeschkir Petrova, Anastasiia B. Zierhut, Felix B. Saczko-Brack, Dario Huergo, Maria-Ana Batters, Christopher Frey, Erwin Veigel, Claudia |
author_sort | Rogez, Benoit |
collection | PubMed |
description | One enigma in biology is the generation, sensing and maintenance of membrane curvature. Curvature-mediating proteins have been shown to induce specific membrane shapes by direct insertion and nanoscopic scaffolding, while the cytoskeletal motors exert forces indirectly through microtubule and actin networks. It remains unclear, whether the manifold direct motorprotein–lipid interactions themselves constitute another fundamental route to remodel the membrane shape. Here we show, combining super-resolution-fluorescence microscopy and membrane-reshaping nanoparticles, that curvature-dependent lipid interactions of myosin-VI on its own, remarkably remodel the membrane geometry into dynamic spatial patterns on the nano- to micrometer scale. We propose a quantitative theoretical model that explains this dynamic membrane sculpting mechanism. The emerging route of motorprotein–lipid interactions reshaping membrane morphology by a mechanism of feedback and instability opens up hitherto unexplored avenues of membrane remodelling and links cytoskeletal motors to early events in the sequence of membrane sculpting in eukaryotic cell biology. |
format | Online Article Text |
id | pubmed-6656732 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-66567322019-07-29 Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting Rogez, Benoit Würthner, Laeschkir Petrova, Anastasiia B. Zierhut, Felix B. Saczko-Brack, Dario Huergo, Maria-Ana Batters, Christopher Frey, Erwin Veigel, Claudia Nat Commun Article One enigma in biology is the generation, sensing and maintenance of membrane curvature. Curvature-mediating proteins have been shown to induce specific membrane shapes by direct insertion and nanoscopic scaffolding, while the cytoskeletal motors exert forces indirectly through microtubule and actin networks. It remains unclear, whether the manifold direct motorprotein–lipid interactions themselves constitute another fundamental route to remodel the membrane shape. Here we show, combining super-resolution-fluorescence microscopy and membrane-reshaping nanoparticles, that curvature-dependent lipid interactions of myosin-VI on its own, remarkably remodel the membrane geometry into dynamic spatial patterns on the nano- to micrometer scale. We propose a quantitative theoretical model that explains this dynamic membrane sculpting mechanism. The emerging route of motorprotein–lipid interactions reshaping membrane morphology by a mechanism of feedback and instability opens up hitherto unexplored avenues of membrane remodelling and links cytoskeletal motors to early events in the sequence of membrane sculpting in eukaryotic cell biology. Nature Publishing Group UK 2019-07-24 /pmc/articles/PMC6656732/ /pubmed/31341165 http://dx.doi.org/10.1038/s41467-019-11268-9 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Article Rogez, Benoit Würthner, Laeschkir Petrova, Anastasiia B. Zierhut, Felix B. Saczko-Brack, Dario Huergo, Maria-Ana Batters, Christopher Frey, Erwin Veigel, Claudia Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting |
title | Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting |
title_full | Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting |
title_fullStr | Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting |
title_full_unstemmed | Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting |
title_short | Reconstitution reveals how myosin-VI self-organises to generate a dynamic mechanism of membrane sculpting |
title_sort | reconstitution reveals how myosin-vi self-organises to generate a dynamic mechanism of membrane sculpting |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6656732/ https://www.ncbi.nlm.nih.gov/pubmed/31341165 http://dx.doi.org/10.1038/s41467-019-11268-9 |
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