Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model

Autonomous oscillatory dynamics are ubiquitous at every level in Biology. At the cellular level, one of the most relevant and well characterized examples of periodic behavior is the cyclic assembly and disassembly of actomyosin networks. In Drosophila, these oscillations induce the robust contractio...

Full description

Bibliographic Details
Main Authors: Miguel Hernández-Del-Valle, Andrea Valencia-Expósito, Nicole Gorfinkiel, Maria D. Martín-Bermudo, David G. Míguez
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Physics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphy.2022.881384/full
_version_ 1818204061062660096
author Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Andrea Valencia-Expósito
Nicole Gorfinkiel
Maria D. Martín-Bermudo
David G. Míguez
David G. Míguez
David G. Míguez
David G. Míguez
author_facet Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Andrea Valencia-Expósito
Nicole Gorfinkiel
Maria D. Martín-Bermudo
David G. Míguez
David G. Míguez
David G. Míguez
David G. Míguez
author_sort Miguel Hernández-Del-Valle
collection DOAJ
description Autonomous oscillatory dynamics are ubiquitous at every level in Biology. At the cellular level, one of the most relevant and well characterized examples of periodic behavior is the cyclic assembly and disassembly of actomyosin networks. In Drosophila, these oscillations induce the robust contraction and expansion of individual cells required for correct dorsal closure, while in the follicular epithelium that surrounds the germline, periodic contractions of the basal actomyosin network are required for proper elongation of the egg chamber. While some studies suggest that actomyosin oscillations are driven by upstream signaling or mechanochemical features, we have recently proposed that they arise as a systems property from the competition between two well characterized features of the actomyosin machinery: 1) cooperative assembly of actin networks mediated by Actin crosslinker proteins and 2) tension-induced disassembly of actin networks mediated by myosin motors. Here, we perform experiments in amnioserosa and in the follicle cells of drosophila and simulations using a coarse-grained model of the actomyosin cortex to characterize the properties of the oscillations and how they depend on different features of the system. We also compare model and experiments to study the dynamics of actomyosin flows and the effect of mechanical coupling between cells in the tissue. In conclusion, our model is a powerful tool to study key features of actomyosin oscillations, from the effect of the individual components to network properties and finally supra-cellular organization of the oscillations at the tissue level.
first_indexed 2024-12-12T03:35:15Z
format Article
id doaj.art-fc2471db36684a7a807814d279bf9cce
institution Directory Open Access Journal
issn 2296-424X
language English
last_indexed 2024-12-12T03:35:15Z
publishDate 2022-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Physics
spelling doaj.art-fc2471db36684a7a807814d279bf9cce2022-12-22T00:39:50ZengFrontiers Media S.A.Frontiers in Physics2296-424X2022-05-011010.3389/fphy.2022.881384881384Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained ModelMiguel Hernández-Del-Valle0Miguel Hernández-Del-Valle1Miguel Hernández-Del-Valle2Miguel Hernández-Del-Valle3Andrea Valencia-Expósito4Nicole Gorfinkiel5Maria D. Martín-Bermudo6David G. Míguez7David G. Míguez8David G. Míguez9David G. Míguez10Centro De Biología Molecular Severo Ochoa, Universidad Autónoma De Madrid, Madrid, SpainIFIMAC, Fac. De Ciencias, Universidad Autónoma De Madrid, Madrid, SpainInstituto Nicolás Cabrera, Fac. De Ciencias, Universidad Autónoma De Madrid, Madrid, SpainFisica De La Materia Condensada, Fac. De Ciencias, Universidad Autónoma De Madrid, Madrid, SpainCentro Andaluz De Biología Del Desarrollo, Universidad Pablo De Olavide/CSIC/JA, Sevilla, SpainDepartment of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University of Madrid, Madrid, SpainCentro Andaluz De Biología Del Desarrollo, Universidad Pablo De Olavide/CSIC/JA, Sevilla, SpainCentro De Biología Molecular Severo Ochoa, Universidad Autónoma De Madrid, Madrid, SpainIFIMAC, Fac. De Ciencias, Universidad Autónoma De Madrid, Madrid, SpainInstituto Nicolás Cabrera, Fac. De Ciencias, Universidad Autónoma De Madrid, Madrid, SpainFisica De La Materia Condensada, Fac. De Ciencias, Universidad Autónoma De Madrid, Madrid, SpainAutonomous oscillatory dynamics are ubiquitous at every level in Biology. At the cellular level, one of the most relevant and well characterized examples of periodic behavior is the cyclic assembly and disassembly of actomyosin networks. In Drosophila, these oscillations induce the robust contraction and expansion of individual cells required for correct dorsal closure, while in the follicular epithelium that surrounds the germline, periodic contractions of the basal actomyosin network are required for proper elongation of the egg chamber. While some studies suggest that actomyosin oscillations are driven by upstream signaling or mechanochemical features, we have recently proposed that they arise as a systems property from the competition between two well characterized features of the actomyosin machinery: 1) cooperative assembly of actin networks mediated by Actin crosslinker proteins and 2) tension-induced disassembly of actin networks mediated by myosin motors. Here, we perform experiments in amnioserosa and in the follicle cells of drosophila and simulations using a coarse-grained model of the actomyosin cortex to characterize the properties of the oscillations and how they depend on different features of the system. We also compare model and experiments to study the dynamics of actomyosin flows and the effect of mechanical coupling between cells in the tissue. In conclusion, our model is a powerful tool to study key features of actomyosin oscillations, from the effect of the individual components to network properties and finally supra-cellular organization of the oscillations at the tissue level.https://www.frontiersin.org/articles/10.3389/fphy.2022.881384/fullactomyosincoarse-grainedproteinsoscillationscytoskeletonbiophyiscs
spellingShingle Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Miguel Hernández-Del-Valle
Andrea Valencia-Expósito
Nicole Gorfinkiel
Maria D. Martín-Bermudo
David G. Míguez
David G. Míguez
David G. Míguez
David G. Míguez
Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model
Frontiers in Physics
actomyosin
coarse-grained
proteins
oscillations
cytoskeleton
biophyiscs
title Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model
title_full Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model
title_fullStr Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model
title_full_unstemmed Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model
title_short Analysis of Actomyosin Oscillatory Dynamics Using a Coarse-Grained Model
title_sort analysis of actomyosin oscillatory dynamics using a coarse grained model
topic actomyosin
coarse-grained
proteins
oscillations
cytoskeleton
biophyiscs
url https://www.frontiersin.org/articles/10.3389/fphy.2022.881384/full
work_keys_str_mv AT miguelhernandezdelvalle analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT miguelhernandezdelvalle analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT miguelhernandezdelvalle analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT miguelhernandezdelvalle analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT andreavalenciaexposito analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT nicolegorfinkiel analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT mariadmartinbermudo analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT davidgmiguez analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT davidgmiguez analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT davidgmiguez analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel
AT davidgmiguez analysisofactomyosinoscillatorydynamicsusingacoarsegrainedmodel