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Scaling of cytoskeletal organization with cell size in Drosophila

Spatially organized macromolecular complexes are essential for cell and tissue function, but the mechanisms that organize micron-scale structures within cells are not well understood. Microtubule-based structures such as mitotic spindles scale with cell size, but less is known about the scaling of a...

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Autores principales: Spencer, Alison K., Schaumberg, Andrew J., Zallen, Jennifer A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5449150/
https://www.ncbi.nlm.nih.gov/pubmed/28404752
http://dx.doi.org/10.1091/mbc.E16-10-0691
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author Spencer, Alison K.
Schaumberg, Andrew J.
Zallen, Jennifer A.
author_facet Spencer, Alison K.
Schaumberg, Andrew J.
Zallen, Jennifer A.
author_sort Spencer, Alison K.
collection PubMed
description Spatially organized macromolecular complexes are essential for cell and tissue function, but the mechanisms that organize micron-scale structures within cells are not well understood. Microtubule-based structures such as mitotic spindles scale with cell size, but less is known about the scaling of actin structures within cells. Actin-rich denticle precursors cover the ventral surface of the Drosophila embryo and larva and provide templates for cuticular structures involved in larval locomotion. Using quantitative imaging and statistical modeling, we demonstrate that denticle number and spacing scale with cell length over a wide range of cell sizes in embryos and larvae. Denticle number and spacing are reduced under space-limited conditions, and both features robustly scale over a 10-fold increase in cell length during larval growth. We show that the relationship between cell length and denticle spacing can be recapitulated by specific mathematical equations in embryos and larvae and that accurate denticle spacing requires an intact microtubule network and the microtubule minus end–binding protein, Patronin. These results identify a novel mechanism of micro­tubule-dependent actin scaling that maintains precise patterns of actin organization during tissue growth.
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spelling pubmed-54491502017-08-16 Scaling of cytoskeletal organization with cell size in Drosophila Spencer, Alison K. Schaumberg, Andrew J. Zallen, Jennifer A. Mol Biol Cell Articles Spatially organized macromolecular complexes are essential for cell and tissue function, but the mechanisms that organize micron-scale structures within cells are not well understood. Microtubule-based structures such as mitotic spindles scale with cell size, but less is known about the scaling of actin structures within cells. Actin-rich denticle precursors cover the ventral surface of the Drosophila embryo and larva and provide templates for cuticular structures involved in larval locomotion. Using quantitative imaging and statistical modeling, we demonstrate that denticle number and spacing scale with cell length over a wide range of cell sizes in embryos and larvae. Denticle number and spacing are reduced under space-limited conditions, and both features robustly scale over a 10-fold increase in cell length during larval growth. We show that the relationship between cell length and denticle spacing can be recapitulated by specific mathematical equations in embryos and larvae and that accurate denticle spacing requires an intact microtubule network and the microtubule minus end–binding protein, Patronin. These results identify a novel mechanism of micro­tubule-dependent actin scaling that maintains precise patterns of actin organization during tissue growth. The American Society for Cell Biology 2017-06-01 /pmc/articles/PMC5449150/ /pubmed/28404752 http://dx.doi.org/10.1091/mbc.E16-10-0691 Text en © 2017 Spencer et al. 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 (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Spencer, Alison K.
Schaumberg, Andrew J.
Zallen, Jennifer A.
Scaling of cytoskeletal organization with cell size in Drosophila
title Scaling of cytoskeletal organization with cell size in Drosophila
title_full Scaling of cytoskeletal organization with cell size in Drosophila
title_fullStr Scaling of cytoskeletal organization with cell size in Drosophila
title_full_unstemmed Scaling of cytoskeletal organization with cell size in Drosophila
title_short Scaling of cytoskeletal organization with cell size in Drosophila
title_sort scaling of cytoskeletal organization with cell size in drosophila
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5449150/
https://www.ncbi.nlm.nih.gov/pubmed/28404752
http://dx.doi.org/10.1091/mbc.E16-10-0691
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