Reversal of contractility as a signature of self-organization in cytoskeletal bundles

Bundles of cytoskeletal filaments and molecular motors generate motion in living cells, and have internal structures ranging from very organized to apparently disordered. The mechanisms powering the disordered structures are debated, and existing models predominantly predict that they are contractil...

Full description

Bibliographic Details
Main Author: Martin Lenz
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/51751
_version_ 1828165768444903424
author Martin Lenz
author_facet Martin Lenz
author_sort Martin Lenz
collection DOAJ
description Bundles of cytoskeletal filaments and molecular motors generate motion in living cells, and have internal structures ranging from very organized to apparently disordered. The mechanisms powering the disordered structures are debated, and existing models predominantly predict that they are contractile. We reexamine this prediction through a theoretical treatment of the interplay between three well-characterized internal dynamical processes in cytoskeletal bundles: filament assembly and disassembly, the attachement-detachment dynamics of motors and that of crosslinking proteins. The resulting self-organization is easily understood in terms of motor and crosslink localization, and allows for an extensive control of the active bundle mechanics, including reversals of the filaments’ apparent velocities and the possibility of generating extension instead of contraction. This reversal mirrors some recent experimental observations, and provides a robust criterion to experimentally elucidate the underpinnings of both actomyosin activity and the dynamics of microtubule/motor assemblies in vitro as well as in diverse intracellular structures ranging from contractile bundles to the mitotic spindle.
first_indexed 2024-04-12T01:49:20Z
format Article
id doaj.art-5c8ff2b266a14a3ca0e0b552e888e641
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T01:49:20Z
publishDate 2020-03-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-5c8ff2b266a14a3ca0e0b552e888e6412022-12-22T03:52:58ZengeLife Sciences Publications LtdeLife2050-084X2020-03-01910.7554/eLife.51751Reversal of contractility as a signature of self-organization in cytoskeletal bundlesMartin Lenz0https://orcid.org/0000-0002-2307-1106Université Paris-Saclay, CNRS, LPTMS, Orsay, France; PMMH, CNRS, ESPCI Paris, PSL University, Sorbonne Université, Université de Paris, Paris, FranceBundles of cytoskeletal filaments and molecular motors generate motion in living cells, and have internal structures ranging from very organized to apparently disordered. The mechanisms powering the disordered structures are debated, and existing models predominantly predict that they are contractile. We reexamine this prediction through a theoretical treatment of the interplay between three well-characterized internal dynamical processes in cytoskeletal bundles: filament assembly and disassembly, the attachement-detachment dynamics of motors and that of crosslinking proteins. The resulting self-organization is easily understood in terms of motor and crosslink localization, and allows for an extensive control of the active bundle mechanics, including reversals of the filaments’ apparent velocities and the possibility of generating extension instead of contraction. This reversal mirrors some recent experimental observations, and provides a robust criterion to experimentally elucidate the underpinnings of both actomyosin activity and the dynamics of microtubule/motor assemblies in vitro as well as in diverse intracellular structures ranging from contractile bundles to the mitotic spindle.https://elifesciences.org/articles/51751cytoskeletonmathematical modelingactinmicrotubulesmolecular motors
spellingShingle Martin Lenz
Reversal of contractility as a signature of self-organization in cytoskeletal bundles
eLife
cytoskeleton
mathematical modeling
actin
microtubules
molecular motors
title Reversal of contractility as a signature of self-organization in cytoskeletal bundles
title_full Reversal of contractility as a signature of self-organization in cytoskeletal bundles
title_fullStr Reversal of contractility as a signature of self-organization in cytoskeletal bundles
title_full_unstemmed Reversal of contractility as a signature of self-organization in cytoskeletal bundles
title_short Reversal of contractility as a signature of self-organization in cytoskeletal bundles
title_sort reversal of contractility as a signature of self organization in cytoskeletal bundles
topic cytoskeleton
mathematical modeling
actin
microtubules
molecular motors
url https://elifesciences.org/articles/51751
work_keys_str_mv AT martinlenz reversalofcontractilityasasignatureofselforganizationincytoskeletalbundles