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Robust organizational principles of protrusive biopolymer networks in migrating living cells

  • Cell migration is associated with the dynamic protrusion of a thin actin-based cytoskeletal extension at the cell front, which has been shown to consist of two different substructures, the leading lamellipodium and the subsequent lamellum. While the formation of the lamellipodium is increasingly well understood, organizational principles underlying the emergence of the lamellum are just beginning to be unraveled. We report here on a 1D mathematical model which describes the reaction-diffusion processes of a polarized actin network in steady state, and reproduces essential characteristics of the lamellipodium-lamellum system. We observe a steep gradient in filament lengths at the protruding edge, a local depolymerization maximum a few microns behind the edge, as well as a differential dominance of the network destabilizer ADF/cofilin and the stabilizer tropomyosin. We identify simple and robust organizational principles giving rise to the derived network characteristics, uncoupled fromCell migration is associated with the dynamic protrusion of a thin actin-based cytoskeletal extension at the cell front, which has been shown to consist of two different substructures, the leading lamellipodium and the subsequent lamellum. While the formation of the lamellipodium is increasingly well understood, organizational principles underlying the emergence of the lamellum are just beginning to be unraveled. We report here on a 1D mathematical model which describes the reaction-diffusion processes of a polarized actin network in steady state, and reproduces essential characteristics of the lamellipodium-lamellum system. We observe a steep gradient in filament lengths at the protruding edge, a local depolymerization maximum a few microns behind the edge, as well as a differential dominance of the network destabilizer ADF/cofilin and the stabilizer tropomyosin. We identify simple and robust organizational principles giving rise to the derived network characteristics, uncoupled from the specifics of any molecular implementation, and thus plausibly valid across cell types. An analysis of network length dependence on physico-chemical system parameters implies that to limit array treadmilling to cellular dimensions, network growth has to be truncated by mechanisms other than aging-induced depolymerization, e.g., by myosin-associated network dissociation at the transition to the cell body. Our work contributes to the analytical understanding of the cytoskeletal extension's bisection into lamellipodium and lamellum and sheds light on how cells organize their molecular machinery to achieve motility.show moreshow less

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    2011 Stuhrmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Metadaten
Author:Björn Stuhrmann, Florian HuberORCiD, Josef Käs
open access (DINI-Set):open_access
Qualitätssicherung:peer reviewed
Fachbereich/Einrichtung:Hochschule Düsseldorf / Fachbereich - Medien
Document Type:Article
Year of Completion:2011
Language of Publication:English
Publisher:Public Library of Science (PLoS)
Parent Title (English):Plos One
Volume:6
Issue:1
Article Number:e14471
URN:urn:nbn:de:hbz:due62-opus-34901
DOI:https://doi.org/10.1371/journal.pone.0014471
ISSN:1932-6203
Tag:DOAJ
Dewey Decimal Classification:0 Informatik, Informationswissenschaft, allgemeine Werke / 00 Informatik, Wissen, Systeme / 004 Datenverarbeitung; Informatik
Licence (German):Creative Commons - CC BY - Namensnennung 4.0 International
Release Date:2021/11/22
Note:
Funding: This work has been supported by the Leipzig Graduate College ‘‘GK 1097 InterNeuro - Interdisciplinary Approaches in Cellular Neuroscience’’ (http://
www.uni-leipzig.de/˜ineuro/) and the Graduate School ‘‘Leipzig School of Natural Sciences - Building with Molecules and Nano-objects (BuildMoNa)’’ (http://www.
buildmona.de/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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