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

Abstract
Data availability
Article and author information
Metrics

Abstract

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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source files with the raw data are provided for all Figures, where quantifications are carried out.

Article and author information

Author details

Kai Weißenbruch

Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany

For correspondence
kai.weissenbruch@kit.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9463-6725
Justin Grewe

University of Heidelberg, Heidelberg, Germany

Competing interests
The authors declare that no competing interests exist.
Marc Hippler

Karlsruhe Institute of, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.
Magdalena Fladung

Zoological Institute - Cell and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4213-2891
Moritz Tremmel

Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8901-9362
Kathrin Stricker

Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.
Ulrich Sebastian Schwarz

Institute for Theoretical Physics, Heidelberg University, Heidelberg, Germany

For correspondence
schwarz@thphys.uni-heidelberg.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1483-640X
Martin Bastmeyer

Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany

For correspondence
bastmeyer@kit.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3471-8400

Funding

Deutsche Forschungsgemeinschaft (EXC 2082/1-390761711)

Ulrich Sebastian Schwarz
Martin Bastmeyer

Deutsche Forschungsgemeinschaft (EXC 2181/1 - 390900948)

Ulrich Sebastian Schwarz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.