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Ordering of myosin II filaments driven by mechanical forces: experiments and theory

Kinjal Dasbiswas, Shiqiong Hu, Frank Schnorrer, Samuel A. Safran, Alexander D. Bershadsky
Published 9 April 2018.DOI: 10.1098/rstb.2017.0114
Kinjal Dasbiswas
James Franck Institute, University of Chicago, Chicago, IL 60637, USA
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Shiqiong Hu
Mechanobiology Institute, National University of Singapore, Singapore 117411, Republic of SingaporeDepartment of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
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Frank Schnorrer
Aix Marseille University, CNRS, IBDM, 13288 Marseille, France
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  • ORCID record for Frank Schnorrer
  • For correspondence: frank.schnorrer@univ-amu.fr
Samuel A. Safran
Department of Chemical and Biological Physics, Weizmann Institute of Science, Rehovot 76100, Israel
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  • For correspondence: sam.safran@weizmann.ac.il
Alexander D. Bershadsky
Mechanobiology Institute, National University of Singapore, Singapore 117411, Republic of SingaporeDepartment of Molecular Cell Biology, Weizmann Institute of Science, Rehovot 76100, Israel
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Abstract

Myosin II filaments form ordered superstructures in both cross-striated muscle and non-muscle cells. In cross-striated muscle, myosin II (thick) filaments, actin (thin) filaments and elastic titin filaments comprise the stereotypical contractile units of muscles called sarcomeres. Linear chains of sarcomeres, called myofibrils, are aligned laterally in registry to form cross-striated muscle cells. The experimentally observed dependence of the registered organization of myofibrils on extracellular matrix elasticity has been proposed to arise from the interactions of sarcomeric contractile elements (considered as force dipoles) through the matrix. Non-muscle cells form small bipolar filaments built of less than 30 myosin II molecules. These filaments are associated in registry forming superstructures (‘stacks’) orthogonal to actin filament bundles. Formation of myosin II filament stacks requires the myosin II ATPase activity and function of the actin filament crosslinking, polymerizing and depolymerizing proteins. We propose that the myosin II filaments embedded into elastic, intervening actin network (IVN) function as force dipoles that interact attractively through the IVN. This is in analogy with the theoretical picture developed for myofibrils where the elastic medium is now the actin cytoskeleton itself. Myosin stack formation in non-muscle cells provides a novel mechanism for the self-organization of the actin cytoskeleton at the level of the entire cell.

This article is part of the theme issue ‘Self-organization in cell biology’.

Footnotes

  • One contribution of 15 to a theme issue ‘Self-organization in cell biology’.

  • Accepted December 30, 2017.
  • © 2018 The Author(s)
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26 May 2018
Volume 373, issue 1747
Philosophical Transactions of the Royal Society B: Biological Sciences: 373 (1747)
  • Table of Contents
Theme issue ‘Self-organization in cell biology’ compiled and edited by Timo Betz and Roland Wedlich-Söldner

Keywords

striated muscle
sarcomere
stress fibres
force dipoles
super-resolution microscopy
non-muscle myosin filaments
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Ordering of myosin II filaments driven by mechanical forces: experiments and theory
Kinjal Dasbiswas, Shiqiong Hu, Frank Schnorrer, Samuel A. Safran, Alexander D. Bershadsky
Phil. Trans. R. Soc. B 2018 373 20170114; DOI: 10.1098/rstb.2017.0114. Published 9 April 2018
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Review article:

Ordering of myosin II filaments driven by mechanical forces: experiments and theory

Kinjal Dasbiswas, Shiqiong Hu, Frank Schnorrer, Samuel A. Safran, Alexander D. Bershadsky
Phil. Trans. R. Soc. B 2018 373 20170114; DOI: 10.1098/rstb.2017.0114. Published 9 April 2018

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Article reuse

  • Article
    • Abstract
    • 1. Introduction
    • 2. Myosin II filaments and their arrangement in cross-striated muscle
    • 3. Registry of myofibrils in striated muscle in culture and in vivo
    • 4. Is there higher-order organization of myosin II filaments in smooth muscle cells?
    • 5. Ordered arrays of myosin II filaments in non-muscle cells
    • 6. Interactions between myosin II filaments through the intervening actin network: a theoretical model
    • 7. Concluding remarks
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    • Funding
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