Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics

Nonmuscle myosin II (NM II) is an integral part of essential cellular processes, including adhesion and migration. Mammalian cells express up to three isoforms termed NM IIA, B, and C. We used U2OS cells to create CRISPR/Cas9-based knockouts of all three isoforms and analyzed the phenotypes on homog...

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Main Authors: Kai Weißenbruch, Justin Grewe, Marc Hippler, Magdalena Fladung, Moritz Tremmel, Kathrin Stricker, Ulrich Sebastian Schwarz, Martin Bastmeyer
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/71888
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spelling doaj-d5554f2f242b43029a623cd6224178032021-08-26T14:23:29ZengeLife Sciences Publications LtdeLife2050-084X2021-08-011010.7554/eLife.71888Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamicsKai Weißenbruch0https://orcid.org/0000-0002-9463-6725Justin Grewe1Marc Hippler2Magdalena Fladung3https://orcid.org/0000-0002-4213-2891Moritz Tremmel4https://orcid.org/0000-0001-8901-9362Kathrin Stricker5Ulrich Sebastian Schwarz6https://orcid.org/0000-0003-1483-640XMartin Bastmeyer7https://orcid.org/0000-0003-3471-8400Zoological Institute, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany; Institute of Functional Interfaces (IFG), Karlsruhe Institute of Technology (KIT), Karlsruhe, GermanyInstitute for Theoretical Physics, University of Heidelberg, Heidelberg, Germany; BioQuant-Center for Quantitative Biology, University of Heidelberg, Heidelberg, GermanyZoological Institute, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany; Institute of Applied Physics, Karlsruhe Institute of Technology (KIT), Karlsruhe, GermanyZoological Institute, Karlsruhe Institute of Technology (KIT), Karlsruhe, GermanyZoological Institute, Karlsruhe Institute of Technology (KIT), Karlsruhe, GermanyZoological Institute, Karlsruhe Institute of Technology (KIT), Karlsruhe, GermanyInstitute for Theoretical Physics, University of Heidelberg, Heidelberg, Germany; BioQuant-Center for Quantitative Biology, University of Heidelberg, Heidelberg, GermanyZoological Institute, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany; Institute for Biological and Chemical Systems - Biological Information Processing (IBCS-BIP), Karlsruhe Institute of Technology (KIT), Karlsruhe, GermanyNonmuscle myosin II (NM II) is an integral part of essential cellular processes, including adhesion and migration. Mammalian cells express up to three isoforms termed NM IIA, B, and C. We used U2OS cells to create CRISPR/Cas9-based knockouts of all three isoforms and analyzed the phenotypes on homogenously coated surfaces, in collagen gels, and on micropatterned substrates. In contrast to homogenously coated surfaces, a structured environment supports a cellular phenotype with invaginated actin arcs even in the absence of NM IIA-induced contractility. A quantitative shape analysis of cells on micropatterns combined with a scale-bridging mathematical model reveals that NM IIA is essential to build up cellular tension during initial stages of force generation, while NM IIB is necessary to elastically stabilize NM IIA-generated tension. A dynamic cell stretch/release experiment in a three-dimensional scaffold confirms these conclusions and in addition reveals a novel role for NM IIC, namely the ability to establish tensional homeostasis.https://elifesciences.org/articles/71888actomyosinNM II isoformscontractilitycell shapeintracellular forcesmathematical modeling
collection DOAJ
language English
format Article
sources DOAJ
author Kai Weißenbruch
Justin Grewe
Marc Hippler
Magdalena Fladung
Moritz Tremmel
Kathrin Stricker
Ulrich Sebastian Schwarz
Martin Bastmeyer
spellingShingle Kai Weißenbruch
Justin Grewe
Marc Hippler
Magdalena Fladung
Moritz Tremmel
Kathrin Stricker
Ulrich Sebastian Schwarz
Martin Bastmeyer
Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
eLife
actomyosin
NM II isoforms
contractility
cell shape
intracellular forces
mathematical modeling
author_facet Kai Weißenbruch
Justin Grewe
Marc Hippler
Magdalena Fladung
Moritz Tremmel
Kathrin Stricker
Ulrich Sebastian Schwarz
Martin Bastmeyer
author_sort Kai Weißenbruch
title Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
title_short Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
title_full Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
title_fullStr Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
title_full_unstemmed Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
title_sort distinct roles of nonmuscle myosin ii isoforms for establishing tension and elasticity during cell morphodynamics
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-08-01
description Nonmuscle myosin II (NM II) is an integral part of essential cellular processes, including adhesion and migration. Mammalian cells express up to three isoforms termed NM IIA, B, and C. We used U2OS cells to create CRISPR/Cas9-based knockouts of all three isoforms and analyzed the phenotypes on homogenously coated surfaces, in collagen gels, and on micropatterned substrates. In contrast to homogenously coated surfaces, a structured environment supports a cellular phenotype with invaginated actin arcs even in the absence of NM IIA-induced contractility. A quantitative shape analysis of cells on micropatterns combined with a scale-bridging mathematical model reveals that NM IIA is essential to build up cellular tension during initial stages of force generation, while NM IIB is necessary to elastically stabilize NM IIA-generated tension. A dynamic cell stretch/release experiment in a three-dimensional scaffold confirms these conclusions and in addition reveals a novel role for NM IIC, namely the ability to establish tensional homeostasis.
topic actomyosin
NM II isoforms
contractility
cell shape
intracellular forces
mathematical modeling
url https://elifesciences.org/articles/71888
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