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First published online 28 April 2009
doi: 10.1242/jcs.042986

This Article Figures Only Full Text Full Text (PDF) Supplementary Material An erratum has been published All Versions of this Article: jcs.042986v1 jcs.042986v2 122/10/1665    most recent Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Colombelli, J. Articles by Stelzer, E. H. K. Search for Related Content PubMed PubMed Citation Articles by Colombelli, J. Articles by Stelzer, E. H. K. Social Bookmarking                         What's this?

Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization

Julien Colombelli^1,*,, Achim Besser², Holger Kress^1,3, Emmanuel G. Reynaud¹, Philippe Girard¹, Emmanuel Caussinus⁴, Uta Haselmann¹, John V. Small⁵, Ulrich S. Schwarz² and Ernst H. K. Stelzer¹

¹ Cell Biology and Biophysics, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, D-69117 Heidelberg, Germany
² University of Heidelberg, Bioquant, BQ0013 BIOMS Schwarz, Im Neuenheimer Feld 267, D-69120 Heidelberg, Germany
³ Department of Mechanical Engineering, Yale University, New Haven, CT 06511, USA
⁴ Biozentrum, Klingelbergstrasse 50/70, CH-4056 Basel, Switzerland
⁵ Institute of Molecular Biotechnology Austrian Academy of Sciences (IMBA), Dr Bohrgasse 7, A-1030, Vienna, Austria

Author for correspondence (e-mail: julien.colombelli{at}irbbarcelona.org)

Accepted 6 January 2009

The mechanics of the actin cytoskeleton have a central role in the regulation of cells and tissues, but the details of how molecular sensors recognize deformations and forces are elusive. By performing cytoskeleton laser nanosurgery in cultured epithelial cells and fibroblasts, we show that the retraction of stress fibers (SFs) is restricted to the proximity of the cut and that new adhesions form at the retracting end. This suggests that SFs are attached to the substrate. A new computational model for SFs confirms this hypothesis and predicts the distribution and propagation of contractile forces along the SF. We then analyzed the dynamics of zyxin, a focal adhesion protein present in SFs. Fluorescent redistribution after laser nanosurgery and drug treatment shows a high correlation between the experimentally measured localization of zyxin and the computed localization of forces along SFs. Correlative electron microscopy reveals that zyxin is recruited very fast to intermediate substrate anchor points that are highly tensed upon SF release. A similar acute localization response is found if SFs are mechanically perturbed with the cantilever of an atomic force microscope. If actin bundles are cut by nanosurgery in living Drosophila egg chambers, we also find that zyxin redistribution dynamics correlate to force propagation and that zyxin relocates at tensed SF anchor points, demonstrating that these processes also occur in living organisms. In summary, our quantitative analysis shows that force and protein localization are closely correlated in stress fibers, suggesting a very direct force-sensing mechanism along actin bundles.

Key words: Mechanosensing, Stress fibers, Zyxin, -actinin, Actomyosin contractility, Laser nanosurgery, Correlative microscopy, Viscoelasticity

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