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Shape remodeling and blebbing of active cytoskeletal vesicles

Morphological transformations of living cells, such as shape adaptation to external stimuli, blebbing, invagination, or tethering, result from an intricate interplay between the plasma membrane and its underlying cytoskeleton, where molecular motors generate forces. Cellular complexity defies a clea...

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Autores principales: Loiseau, Etienne, Schneider, Jochen A. M., Keber, Felix C., Pelzl, Carina, Massiera, Gladys, Salbreux, Guillaume, Bausch, Andreas R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4846454/
https://www.ncbi.nlm.nih.gov/pubmed/27152328
http://dx.doi.org/10.1126/sciadv.1500465
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author Loiseau, Etienne
Schneider, Jochen A. M.
Keber, Felix C.
Pelzl, Carina
Massiera, Gladys
Salbreux, Guillaume
Bausch, Andreas R.
author_facet Loiseau, Etienne
Schneider, Jochen A. M.
Keber, Felix C.
Pelzl, Carina
Massiera, Gladys
Salbreux, Guillaume
Bausch, Andreas R.
author_sort Loiseau, Etienne
collection PubMed
description Morphological transformations of living cells, such as shape adaptation to external stimuli, blebbing, invagination, or tethering, result from an intricate interplay between the plasma membrane and its underlying cytoskeleton, where molecular motors generate forces. Cellular complexity defies a clear identification of the competing processes that lead to such a rich phenomenology. In a synthetic biology approach, designing a cell-like model assembled from a minimal set of purified building blocks would allow the control of all relevant parameters. We reconstruct actomyosin vesicles in which the coupling of the cytoskeleton to the membrane, the topology of the cytoskeletal network, and the contractile activity can all be precisely controlled and tuned. We demonstrate that tension generation of an encapsulated active actomyosin network suffices for global shape transformation of cell-sized lipid vesicles, which are reminiscent of morphological adaptations in living cells. The observed polymorphism of our cell-like model, such as blebbing, tether extrusion, or faceted shapes, can be qualitatively explained by the protein concentration dependencies and a force balance, taking into account the membrane tension, the density of anchoring points between the membrane and the actin network, and the forces exerted by molecular motors in the actin network. The identification of the physical mechanisms for shape transformations of active cytoskeletal vesicles sets a conceptual and quantitative benchmark for the further exploration of the adaptation mechanisms of cells.
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spelling pubmed-48464542016-05-05 Shape remodeling and blebbing of active cytoskeletal vesicles Loiseau, Etienne Schneider, Jochen A. M. Keber, Felix C. Pelzl, Carina Massiera, Gladys Salbreux, Guillaume Bausch, Andreas R. Sci Adv Research Articles Morphological transformations of living cells, such as shape adaptation to external stimuli, blebbing, invagination, or tethering, result from an intricate interplay between the plasma membrane and its underlying cytoskeleton, where molecular motors generate forces. Cellular complexity defies a clear identification of the competing processes that lead to such a rich phenomenology. In a synthetic biology approach, designing a cell-like model assembled from a minimal set of purified building blocks would allow the control of all relevant parameters. We reconstruct actomyosin vesicles in which the coupling of the cytoskeleton to the membrane, the topology of the cytoskeletal network, and the contractile activity can all be precisely controlled and tuned. We demonstrate that tension generation of an encapsulated active actomyosin network suffices for global shape transformation of cell-sized lipid vesicles, which are reminiscent of morphological adaptations in living cells. The observed polymorphism of our cell-like model, such as blebbing, tether extrusion, or faceted shapes, can be qualitatively explained by the protein concentration dependencies and a force balance, taking into account the membrane tension, the density of anchoring points between the membrane and the actin network, and the forces exerted by molecular motors in the actin network. The identification of the physical mechanisms for shape transformations of active cytoskeletal vesicles sets a conceptual and quantitative benchmark for the further exploration of the adaptation mechanisms of cells. American Association for the Advancement of Science 2016-04-15 /pmc/articles/PMC4846454/ /pubmed/27152328 http://dx.doi.org/10.1126/sciadv.1500465 Text en Copyright © 2016, The Authors http://creativecommons.org/licenses/by-nc/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (http://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Research Articles
Loiseau, Etienne
Schneider, Jochen A. M.
Keber, Felix C.
Pelzl, Carina
Massiera, Gladys
Salbreux, Guillaume
Bausch, Andreas R.
Shape remodeling and blebbing of active cytoskeletal vesicles
title Shape remodeling and blebbing of active cytoskeletal vesicles
title_full Shape remodeling and blebbing of active cytoskeletal vesicles
title_fullStr Shape remodeling and blebbing of active cytoskeletal vesicles
title_full_unstemmed Shape remodeling and blebbing of active cytoskeletal vesicles
title_short Shape remodeling and blebbing of active cytoskeletal vesicles
title_sort shape remodeling and blebbing of active cytoskeletal vesicles
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4846454/
https://www.ncbi.nlm.nih.gov/pubmed/27152328
http://dx.doi.org/10.1126/sciadv.1500465
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