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Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex

Filamentous actin (F-actin) and non-muscle myosin II motors drive cell motility and cell shape changes that guide large scale tissue movements during embryonic morphogenesis. To gain a better understanding of the role of actomyosin in vivo, we have developed a two-dimensional (2D) computational mode...

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Autores principales: Miller, Callie J., Harris, Demetrius, Weaver, Robert, Ermentrout, G. Bard, Davidson, Lance A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6171965/
https://www.ncbi.nlm.nih.gov/pubmed/30222728
http://dx.doi.org/10.1371/journal.pcbi.1006344
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author Miller, Callie J.
Harris, Demetrius
Weaver, Robert
Ermentrout, G. Bard
Davidson, Lance A.
author_facet Miller, Callie J.
Harris, Demetrius
Weaver, Robert
Ermentrout, G. Bard
Davidson, Lance A.
author_sort Miller, Callie J.
collection PubMed
description Filamentous actin (F-actin) and non-muscle myosin II motors drive cell motility and cell shape changes that guide large scale tissue movements during embryonic morphogenesis. To gain a better understanding of the role of actomyosin in vivo, we have developed a two-dimensional (2D) computational model to study emergent phenomena of dynamic unbranched actomyosin arrays in the cell cortex. These phenomena include actomyosin punctuated contractions, or "actin asters" that form within quiescent F-actin networks. Punctuated contractions involve both formation of high intensity aster-like structures and disassembly of those same structures. Our 2D model allows us to explore the kinematics of filament polarity sorting, segregation of motors, and morphology of F-actin arrays that emerge as the model structure and biophysical properties are varied. Our model demonstrates the complex, emergent feedback between filament reorganization and motor transport that generate as well as disassemble actin asters. Since intracellular actomyosin dynamics are thought to be controlled by localization of scaffold proteins that bind F-actin or their myosin motors we also apply our 2D model to recapitulate in vitro studies that have revealed complex patterns of actomyosin that assemble from patterning filaments and motor complexes with microcontact printing. Although we use a minimal representation of filament, motor, and cross-linker biophysics, our model establishes a framework for investigating the role of other actin binding proteins, how they might alter actomyosin dynamics, and makes predictions that can be tested experimentally within live cells as well as within in vitro models.
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spelling pubmed-61719652018-10-19 Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex Miller, Callie J. Harris, Demetrius Weaver, Robert Ermentrout, G. Bard Davidson, Lance A. PLoS Comput Biol Research Article Filamentous actin (F-actin) and non-muscle myosin II motors drive cell motility and cell shape changes that guide large scale tissue movements during embryonic morphogenesis. To gain a better understanding of the role of actomyosin in vivo, we have developed a two-dimensional (2D) computational model to study emergent phenomena of dynamic unbranched actomyosin arrays in the cell cortex. These phenomena include actomyosin punctuated contractions, or "actin asters" that form within quiescent F-actin networks. Punctuated contractions involve both formation of high intensity aster-like structures and disassembly of those same structures. Our 2D model allows us to explore the kinematics of filament polarity sorting, segregation of motors, and morphology of F-actin arrays that emerge as the model structure and biophysical properties are varied. Our model demonstrates the complex, emergent feedback between filament reorganization and motor transport that generate as well as disassemble actin asters. Since intracellular actomyosin dynamics are thought to be controlled by localization of scaffold proteins that bind F-actin or their myosin motors we also apply our 2D model to recapitulate in vitro studies that have revealed complex patterns of actomyosin that assemble from patterning filaments and motor complexes with microcontact printing. Although we use a minimal representation of filament, motor, and cross-linker biophysics, our model establishes a framework for investigating the role of other actin binding proteins, how they might alter actomyosin dynamics, and makes predictions that can be tested experimentally within live cells as well as within in vitro models. Public Library of Science 2018-09-17 /pmc/articles/PMC6171965/ /pubmed/30222728 http://dx.doi.org/10.1371/journal.pcbi.1006344 Text en © 2018 Miller et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Miller, Callie J.
Harris, Demetrius
Weaver, Robert
Ermentrout, G. Bard
Davidson, Lance A.
Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
title Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
title_full Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
title_fullStr Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
title_full_unstemmed Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
title_short Emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
title_sort emergent mechanics of actomyosin drive punctuated contractions and shape network morphology in the cell cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6171965/
https://www.ncbi.nlm.nih.gov/pubmed/30222728
http://dx.doi.org/10.1371/journal.pcbi.1006344
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