Literature DB >> 25992722

Cell shape dynamics reveal balance of elasticity and contractility in peripheral arcs.

Céline Labouesse1, Alexander B Verkhovsky2, Jean-Jacques Meister2, Chiara Gabella2, Benoît Vianay2.   

Abstract

The mechanical interaction between adherent cells and their substrate relies on the formation of adhesion sites and on the stabilization of contractile acto-myosin bundles, or stress fibers. The shape of the cell and the orientation of these fibers can be controlled by adhesive patterning. On nonadhesive gaps, fibroblasts develop thick peripheral stress fibers, with a concave curvature. The radius of curvature of these arcs results from the balance of the line tension in the arc and of the surface tension in the cell bulk. However, the nature of these forces, and in particular the contribution of myosin-dependent contractility, is not clear. To get insight into the force balance, we inhibit myosin activity and simultaneously monitor the dynamics of peripheral arc radii and traction forces. We use these measurements to estimate line and surface tension. We found that myosin inhibition led to a decrease in the traction forces and an increase in arc radius, indicating that both line tension and surface tension dropped, but the line tension decreased to a lesser extent than surface tension. These results suggest that myosin-independent force contributes to tension in the peripheral arcs. We propose a simple physical model in which the peripheral arc line tension is due to the combination of myosin II contractility and a passive elastic component, while surface tension is largely due to active contractility. Numerical solutions of this model reproduce well the experimental data and allow estimation of the contributions of elasticity and contractility to the arc line tension.
Copyright © 2015 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2015        PMID: 25992722      PMCID: PMC4457271          DOI: 10.1016/j.bpj.2015.04.005

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  44 in total

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Journal:  Mol Biol Cell       Date:  2003-09-05       Impact factor: 4.138

2.  Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells.

Authors:  Shinji Deguchi; Toshiro Ohashi; Masaaki Sato
Journal:  J Biomech       Date:  2005-10-10       Impact factor: 2.712

3.  Focal adhesions as mechanosensors: the two-spring model.

Authors:  Ulrich S Schwarz; Thorsten Erdmann; Ilka B Bischofs
Journal:  Biosystems       Date:  2005-10-19       Impact factor: 1.973

4.  Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics.

Authors:  Sanjay Kumar; Iva Z Maxwell; Alexander Heisterkamp; Thomas R Polte; Tanmay P Lele; Matthew Salanga; Eric Mazur; Donald E Ingber
Journal:  Biophys J       Date:  2006-02-24       Impact factor: 4.033

5.  Cell distribution of stress fibres in response to the geometry of the adhesive environment.

Authors:  Manuel Théry; Anne Pépin; Emilie Dressaire; Yong Chen; Michel Bornens
Journal:  Cell Motil Cytoskeleton       Date:  2006-06

Review 6.  Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis.

Authors:  Thomas Lecuit; Pierre-François Lenne
Journal:  Nat Rev Mol Cell Biol       Date:  2007-08       Impact factor: 94.444

7.  Geometry regulates traction stresses in adherent cells.

Authors:  Patrick W Oakes; Shiladitya Banerjee; M Cristina Marchetti; Margaret L Gardel
Journal:  Biophys J       Date:  2014-08-19       Impact factor: 4.033

8.  Emergence of large-scale cell morphology and movement from local actin filament growth dynamics.

Authors:  Catherine I Lacayo; Zachary Pincus; Martijn M VanDuijn; Cyrus A Wilson; Daniel A Fletcher; Frank B Gertler; Alex Mogilner; Julie A Theriot
Journal:  PLoS Biol       Date:  2007-09       Impact factor: 8.029

9.  Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility.

Authors:  Patricia T Yam; Cyrus A Wilson; Lin Ji; Benedict Hebert; Erin L Barnhart; Natalie A Dye; Paul W Wiseman; Gaudenz Danuser; Julie A Theriot
Journal:  J Cell Biol       Date:  2007-09-24       Impact factor: 10.539

10.  Stress fibers are generated by two distinct actin assembly mechanisms in motile cells.

Authors:  Pirta Hotulainen; Pekka Lappalainen
Journal:  J Cell Biol       Date:  2006-05-01       Impact factor: 10.539

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  11 in total

Review 1.  The assembly and function of perinuclear actin cap in migrating cells.

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Journal:  Protoplasma       Date:  2017-01-18       Impact factor: 3.356

2.  Geometry and network connectivity govern the mechanics of stress fibers.

Authors:  Elena Kassianidou; Christoph A Brand; Ulrich S Schwarz; Sanjay Kumar
Journal:  Proc Natl Acad Sci U S A       Date:  2017-02-17       Impact factor: 11.205

3.  Prediction of traction forces of motile cells.

Authors:  Clément Roux; Alain Duperray; Valérie M Laurent; Richard Michel; Valentina Peschetola; Claude Verdier; Jocelyn Étienne
Journal:  Interface Focus       Date:  2016-10-06       Impact factor: 3.906

4.  Deconstructing the role of myosin contractility in force fluctuations within focal adhesions.

Authors:  Debsuvra Ghosh; Subhadip Ghosh; Abhishek Chaudhuri
Journal:  Biophys J       Date:  2022-03-26       Impact factor: 3.699

Review 5.  Balancing forces in migration.

Authors:  Patrick W Oakes
Journal:  Curr Opin Cell Biol       Date:  2018-05-23       Impact factor: 8.382

6.  Dynamics of Cell Ensembles on Adhesive Micropatterns: Bridging the Gap between Single Cell Spreading and Collective Cell Migration.

Authors:  Philipp J Albert; Ulrich S Schwarz
Journal:  PLoS Comput Biol       Date:  2016-04-07       Impact factor: 4.475

7.  Dissipation of contractile forces: the missing piece in cell mechanics.

Authors:  Laetitia Kurzawa; Benoit Vianay; Fabrice Senger; Timothée Vignaud; Laurent Blanchoin; Manuel Théry
Journal:  Mol Biol Cell       Date:  2017-07-07       Impact factor: 4.138

8.  Microsurgery-aided in-situ force probing reveals extensibility and viscoelastic properties of individual stress fibers.

Authors:  Céline Labouesse; Chiara Gabella; Jean-Jacques Meister; Benoît Vianay; Alexander B Verkhovsky
Journal:  Sci Rep       Date:  2016-03-30       Impact factor: 4.379

9.  Modeling cell shape and dynamics on micropatterns.

Authors:  Philipp J Albert; Ulrich S Schwarz
Journal:  Cell Adh Migr       Date:  2016-02-02       Impact factor: 3.405

10.  Profiling cellular morphodynamics by spatiotemporal spectrum decomposition.

Authors:  Xiao Ma; Onur Dagliyan; Klaus M Hahn; Gaudenz Danuser
Journal:  PLoS Comput Biol       Date:  2018-08-02       Impact factor: 4.475

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