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The contributions of the actin machinery to endocytic membrane bending and vesicle formation

Branched and cross-linked actin networks mediate cellular processes that move and shape membranes. To understand how actin contributes during the different stages of endocytic membrane reshaping, we analyzed deletion mutants of yeast actin network components using a hybrid imaging approach that comb...

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Autores principales: Picco, Andrea, Kukulski, Wanda, Manenschijn, Hetty E., Specht, Tanja, Briggs, John A. G., Kaksonen, Marko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5994895/
https://www.ncbi.nlm.nih.gov/pubmed/29851558
http://dx.doi.org/10.1091/mbc.E17-11-0688
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author Picco, Andrea
Kukulski, Wanda
Manenschijn, Hetty E.
Specht, Tanja
Briggs, John A. G.
Kaksonen, Marko
author_facet Picco, Andrea
Kukulski, Wanda
Manenschijn, Hetty E.
Specht, Tanja
Briggs, John A. G.
Kaksonen, Marko
author_sort Picco, Andrea
collection PubMed
description Branched and cross-linked actin networks mediate cellular processes that move and shape membranes. To understand how actin contributes during the different stages of endocytic membrane reshaping, we analyzed deletion mutants of yeast actin network components using a hybrid imaging approach that combines live imaging with correlative microscopy. We could thus temporally dissect the effects of different actin network perturbations, revealing distinct stages of actin-based membrane reshaping. Our data show that initiation of membrane bending requires the actin network to be physically linked to the plasma membrane and to be optimally cross-linked. Once initiated, the membrane invagination process is driven by nucleation and polymerization of new actin filaments, independent of the degree of cross-linking and unaffected by a surplus of actin network components. A key transition occurs 2 s before scission, when the filament nucleation rate drops. From that time point on, invagination growth and vesicle scission are driven by an expansion of the actin network without a proportional increase of net actin amounts. The expansion is sensitive to the amount of filamentous actin and its cross-linking. Our results suggest that the mechanism by which actin reshapes the membrane changes during the progress of endocytosis, possibly adapting to varying force requirements.
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spelling pubmed-59948952018-08-16 The contributions of the actin machinery to endocytic membrane bending and vesicle formation Picco, Andrea Kukulski, Wanda Manenschijn, Hetty E. Specht, Tanja Briggs, John A. G. Kaksonen, Marko Mol Biol Cell Articles Branched and cross-linked actin networks mediate cellular processes that move and shape membranes. To understand how actin contributes during the different stages of endocytic membrane reshaping, we analyzed deletion mutants of yeast actin network components using a hybrid imaging approach that combines live imaging with correlative microscopy. We could thus temporally dissect the effects of different actin network perturbations, revealing distinct stages of actin-based membrane reshaping. Our data show that initiation of membrane bending requires the actin network to be physically linked to the plasma membrane and to be optimally cross-linked. Once initiated, the membrane invagination process is driven by nucleation and polymerization of new actin filaments, independent of the degree of cross-linking and unaffected by a surplus of actin network components. A key transition occurs 2 s before scission, when the filament nucleation rate drops. From that time point on, invagination growth and vesicle scission are driven by an expansion of the actin network without a proportional increase of net actin amounts. The expansion is sensitive to the amount of filamentous actin and its cross-linking. Our results suggest that the mechanism by which actin reshapes the membrane changes during the progress of endocytosis, possibly adapting to varying force requirements. The American Society for Cell Biology 2018-06-01 /pmc/articles/PMC5994895/ /pubmed/29851558 http://dx.doi.org/10.1091/mbc.E17-11-0688 Text en © 2018 Picco, Kukulski, et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0/ This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Picco, Andrea
Kukulski, Wanda
Manenschijn, Hetty E.
Specht, Tanja
Briggs, John A. G.
Kaksonen, Marko
The contributions of the actin machinery to endocytic membrane bending and vesicle formation
title The contributions of the actin machinery to endocytic membrane bending and vesicle formation
title_full The contributions of the actin machinery to endocytic membrane bending and vesicle formation
title_fullStr The contributions of the actin machinery to endocytic membrane bending and vesicle formation
title_full_unstemmed The contributions of the actin machinery to endocytic membrane bending and vesicle formation
title_short The contributions of the actin machinery to endocytic membrane bending and vesicle formation
title_sort contributions of the actin machinery to endocytic membrane bending and vesicle formation
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5994895/
https://www.ncbi.nlm.nih.gov/pubmed/29851558
http://dx.doi.org/10.1091/mbc.E17-11-0688
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