Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization - PubMed (original) (raw)
. 2009 May 15;122(Pt 10):1665-79.
doi: 10.1242/jcs.042986. Epub 2009 Apr 28.
Affiliations
- PMID: 19401336
- DOI: 10.1242/jcs.042986
Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization
Julien Colombelli et al. J Cell Sci. 2009.
Erratum in
- J Cell Sci. 2009 Jun 1;122(Pt 11):1928
Abstract
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.
Similar articles
- Dynamics of Actin Stress Fibers and Focal Adhesions during Slow Migration in Swiss 3T3 Fibroblasts: Intracellular Mechanism of Cell Turning.
Sugawara M, Miyoshi H, Miura T, Tanaka H, Tsubota KI, Liu H. Sugawara M, et al. Biomed Res Int. 2016;2016:5749749. doi: 10.1155/2016/5749749. Epub 2016 Dec 29. Biomed Res Int. 2016. PMID: 28119928 Free PMC article. - Intracellular stress transmission through actin stress fiber network in adherent vascular cells.
Deguchi S, Ohashi T, Sato M. Deguchi S, et al. Mol Cell Biomech. 2005 Dec;2(4):205-16. Mol Cell Biomech. 2005. PMID: 16705866 - Rho-kinase dependent organization of stress fibers and focal adhesions in cultured fibroblasts.
Katoh K, Kano Y, Ookawara S. Katoh K, et al. Genes Cells. 2007 May;12(5):623-38. doi: 10.1111/j.1365-2443.2007.01073.x. Genes Cells. 2007. PMID: 17535253 - Zyxin: a mechanotransductor to regulate gene expression.
Wang YX, Wang DY, Guo YC, Guo J. Wang YX, et al. Eur Rev Med Pharmacol Sci. 2019 Jan;23(1):413-425. doi: 10.26355/eurrev_201901_16790. Eur Rev Med Pharmacol Sci. 2019. PMID: 30657586 Review. - LIM proteins in actin cytoskeleton mechanoresponse.
Smith MA, Hoffman LM, Beckerle MC. Smith MA, et al. Trends Cell Biol. 2014 Oct;24(10):575-83. doi: 10.1016/j.tcb.2014.04.009. Epub 2014 Jun 2. Trends Cell Biol. 2014. PMID: 24933506 Free PMC article. Review.
Cited by
- Model-based traction force microscopy reveals differential tension in cellular actin bundles.
Soiné JR, Brand CA, Stricker J, Oakes PW, Gardel ML, Schwarz US. Soiné JR, et al. PLoS Comput Biol. 2015 Mar 6;11(3):e1004076. doi: 10.1371/journal.pcbi.1004076. eCollection 2015 Mar. PLoS Comput Biol. 2015. PMID: 25748431 Free PMC article. - Striated acto-myosin fibers can reorganize and register in response to elastic interactions with the matrix.
Friedrich BM, Buxboim A, Discher DE, Safran SA. Friedrich BM, et al. Biophys J. 2011 Jun 8;100(11):2706-15. doi: 10.1016/j.bpj.2011.04.050. Biophys J. 2011. PMID: 21641316 Free PMC article. - Organization and function of tension-dependent complexes at adherens junctions.
Rauskolb C, Cervantes E, Madere F, Irvine KD. Rauskolb C, et al. J Cell Sci. 2019 Apr 3;132(7):jcs224063. doi: 10.1242/jcs.224063. J Cell Sci. 2019. PMID: 30837288 Free PMC article. - Mechanochemical Effects on Extracellular Signal-Regulated Kinase Dynamics in Stem Cell Differentiation.
Dharmarajan A, Floren M, Cox L, Ding Y, Johnson R, Tan W. Dharmarajan A, et al. Tissue Eng Part A. 2018 Aug;24(15-16):1179-1189. doi: 10.1089/ten.tea.2017.0365. Epub 2018 Jul 3. Tissue Eng Part A. 2018. PMID: 29969368 Free PMC article. - A mechanical-biochemical feedback loop regulates remodeling in the actin cytoskeleton.
Stachowiak MR, Smith MA, Blankman E, Chapin LM, Balcioglu HE, Wang S, Beckerle MC, O'Shaughnessy B. Stachowiak MR, et al. Proc Natl Acad Sci U S A. 2014 Dec 9;111(49):17528-33. doi: 10.1073/pnas.1417686111. Epub 2014 Nov 24. Proc Natl Acad Sci U S A. 2014. PMID: 25422436 Free PMC article.
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases