Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking

Many developmental processes break left–right (LR) symmetry with a consistent handedness. LR asymmetry emerges early in development, and in many species the primary determinant of this asymmetry has been linked to the cytoskeleton. However, the nature of the underlying chirally asymmetric cytoskelet...

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Main Authors: Sundar Ram Naganathan, Sebastian Fürthauer, Masatoshi Nishikawa, Frank Jülicher, Stephan W Grill
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/04165
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spelling doaj-4206e317d1264e3ba0caa7a928a2adc62021-05-04T23:35:11ZengeLife Sciences Publications LtdeLife2050-084X2014-12-01310.7554/eLife.04165Active torque generation by the actomyosin cell cortex drives left–right symmetry breakingSundar Ram Naganathan0Sebastian Fürthauer1Masatoshi Nishikawa2Frank Jülicher3Stephan W Grill4Biotechnology Center, Technical University Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute for the Physics of Complex Systems, Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyBiotechnology Center, Technical University Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute for the Physics of Complex Systems, Dresden, GermanyBiotechnology Center, Technical University Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMany developmental processes break left–right (LR) symmetry with a consistent handedness. LR asymmetry emerges early in development, and in many species the primary determinant of this asymmetry has been linked to the cytoskeleton. However, the nature of the underlying chirally asymmetric cytoskeletal processes has remained elusive. In this study, we combine thin-film active chiral fluid theory with experimental analysis of the C. elegans embryo to show that the actomyosin cortex generates active chiral torques to facilitate chiral symmetry breaking. Active torques drive chiral counter-rotating cortical flow in the zygote, depend on myosin activity, and can be altered through mild changes in Rho signaling. Notably, they also execute the chiral skew event at the 4-cell stage to establish the C. elegans LR body axis. Taken together, our results uncover a novel, large-scale physical activity of the actomyosin cytoskeleton that provides a fundamental mechanism for chiral morphogenesis in development.https://elifesciences.org/articles/04165actomyosin cortexactive torqueL/R symmetry breakinghydrodynamicsWnt signaling
collection DOAJ
language English
format Article
sources DOAJ
author Sundar Ram Naganathan
Sebastian Fürthauer
Masatoshi Nishikawa
Frank Jülicher
Stephan W Grill
spellingShingle Sundar Ram Naganathan
Sebastian Fürthauer
Masatoshi Nishikawa
Frank Jülicher
Stephan W Grill
Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
eLife
actomyosin cortex
active torque
L/R symmetry breaking
hydrodynamics
Wnt signaling
author_facet Sundar Ram Naganathan
Sebastian Fürthauer
Masatoshi Nishikawa
Frank Jülicher
Stephan W Grill
author_sort Sundar Ram Naganathan
title Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
title_short Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
title_full Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
title_fullStr Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
title_full_unstemmed Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
title_sort active torque generation by the actomyosin cell cortex drives left–right symmetry breaking
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2014-12-01
description Many developmental processes break left–right (LR) symmetry with a consistent handedness. LR asymmetry emerges early in development, and in many species the primary determinant of this asymmetry has been linked to the cytoskeleton. However, the nature of the underlying chirally asymmetric cytoskeletal processes has remained elusive. In this study, we combine thin-film active chiral fluid theory with experimental analysis of the C. elegans embryo to show that the actomyosin cortex generates active chiral torques to facilitate chiral symmetry breaking. Active torques drive chiral counter-rotating cortical flow in the zygote, depend on myosin activity, and can be altered through mild changes in Rho signaling. Notably, they also execute the chiral skew event at the 4-cell stage to establish the C. elegans LR body axis. Taken together, our results uncover a novel, large-scale physical activity of the actomyosin cytoskeleton that provides a fundamental mechanism for chiral morphogenesis in development.
topic actomyosin cortex
active torque
L/R symmetry breaking
hydrodynamics
Wnt signaling
url https://elifesciences.org/articles/04165
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