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Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes

Pulsatile RhoA dynamics underlie a wide range of cell and tissue behaviors. The circuits that produce these dynamics in different cells share common architectures based on fast positive and delayed negative feedback through F-actin, but they can produce very different spatiotemporal patterns of RhoA...

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Autores principales: Yao, Baixue, Donoughe, Seth, Michaux, Jonathan, Munro, Edwin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9265151/
https://www.ncbi.nlm.nih.gov/pubmed/35138935
http://dx.doi.org/10.1091/mbc.E21-11-0542
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author Yao, Baixue
Donoughe, Seth
Michaux, Jonathan
Munro, Edwin
author_facet Yao, Baixue
Donoughe, Seth
Michaux, Jonathan
Munro, Edwin
author_sort Yao, Baixue
collection PubMed
description Pulsatile RhoA dynamics underlie a wide range of cell and tissue behaviors. The circuits that produce these dynamics in different cells share common architectures based on fast positive and delayed negative feedback through F-actin, but they can produce very different spatiotemporal patterns of RhoA activity. However, the underlying causes of this variation remain poorly understood. Here we asked how this variation could arise through modulation of actin network dynamics downstream of active RhoA in early Caenorhabditis elegans embryos. We find that perturbing two RhoA effectors—formin and anillin—induce transitions from nonrecurrent focal pulses to either large noisy oscillatory pulses (formin depletion) or noisy oscillatory waves (anillin depletion). In both cases these transitions could be explained by changes in local F-actin levels and depletion dynamics, leading to changes in spatial and temporal patterns of RhoA inhibition. However, the underlying mechanisms for F-actin depletion are distinct, with different dependencies on myosin II activity. Thus, modulating actomyosin network dynamics could shape the spatiotemporal dynamics of RhoA activity for different physiological or morphogenetic functions.
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spelling pubmed-92651512022-07-27 Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes Yao, Baixue Donoughe, Seth Michaux, Jonathan Munro, Edwin Mol Biol Cell Articles Pulsatile RhoA dynamics underlie a wide range of cell and tissue behaviors. The circuits that produce these dynamics in different cells share common architectures based on fast positive and delayed negative feedback through F-actin, but they can produce very different spatiotemporal patterns of RhoA activity. However, the underlying causes of this variation remain poorly understood. Here we asked how this variation could arise through modulation of actin network dynamics downstream of active RhoA in early Caenorhabditis elegans embryos. We find that perturbing two RhoA effectors—formin and anillin—induce transitions from nonrecurrent focal pulses to either large noisy oscillatory pulses (formin depletion) or noisy oscillatory waves (anillin depletion). In both cases these transitions could be explained by changes in local F-actin levels and depletion dynamics, leading to changes in spatial and temporal patterns of RhoA inhibition. However, the underlying mechanisms for F-actin depletion are distinct, with different dependencies on myosin II activity. Thus, modulating actomyosin network dynamics could shape the spatiotemporal dynamics of RhoA activity for different physiological or morphogenetic functions. The American Society for Cell Biology 2022-05-12 /pmc/articles/PMC9265151/ /pubmed/35138935 http://dx.doi.org/10.1091/mbc.E21-11-0542 Text en © 2022 Yao 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. https://creativecommons.org/licenses/by-nc-sa/4.0/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 4.0 International Creative Commons License.
spellingShingle Articles
Yao, Baixue
Donoughe, Seth
Michaux, Jonathan
Munro, Edwin
Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes
title Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes
title_full Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes
title_fullStr Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes
title_full_unstemmed Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes
title_short Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes
title_sort modulating rhoa effectors induces transitions to oscillatory and more wavelike rhoa dynamics in caenorhabditis elegans zygotes
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9265151/
https://www.ncbi.nlm.nih.gov/pubmed/35138935
http://dx.doi.org/10.1091/mbc.E21-11-0542
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