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

Labouesse, Céline; Gabella, Chiara; Meister, Jean-Jacques; Vianay, Benoît; Verkhovsky, Alexander B.

doi:10.1038/srep23722

Cited by 17 publications

(12 citation statements)

References 26 publications

(56 reference statements)

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“…The ability of this technology to arbitrarily standardize cell geometry has dramatically improved the field's understanding of how cell shape controls traction force, cytoskeletal architecture, proliferation/apoptosis, and stem cell fate (8,19,20). Micropatterning has also been used to prescribe the geometry of peripheral SFs (21)(22)(23). We reasoned that we could productively exploit micropatterning approaches to control cell and SF geometry in combination with SLA and thereby gain new insights into SF mechanics.…”

Section: Resultsmentioning

confidence: 99%

Geometry and network connectivity govern the mechanics of stress fibers

Kassianidou

Brand

Schwarz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Actomyosin stress fibers (SFs) play key roles in driving polarized motility and generating traction forces, yet little is known about how tension borne by an individual SF is governed by SF geometry and its connectivity to other cytoskeletal elements. We now address this question by combining single-cell micropatterning with subcellular laser ablation to probe the mechanics of single, geometrically defined SFs. The retraction length of geometrically isolated SFs after cutting depends strongly on SF length, demonstrating that longer SFs dissipate more energy upon incision. Furthermore, when cell geometry and adhesive spacing are fixed, cell-to-cell heterogeneities in SF dissipated elastic energy can be predicted from varying degrees of physical integration with the surrounding network. We apply genetic, pharmacological, and computational approaches to demonstrate a causal and quantitative relationship between SF connectivity and mechanics for patterned cells and show that similar relationships hold for nonpatterned cells allowed to form cell-cell contacts in monolayer culture. Remarkably, dissipation of a single SF within a monolayer induces cytoskeletal rearrangements in cells long distances away. Finally, stimulation of cell migration leads to characteristic changes in network connectivity that promote SF bundling at the cell rear. Our findings demonstrate that SFs influence and are influenced by the networks in which they reside. Such higher order network interactions contribute in unexpected ways to cell mechanics and motility.cytoskeleton | active cable model | actin | myosin | cell migration

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Section: Resultsmentioning

confidence: 99%

Geometry and network connectivity govern the mechanics of stress fibers

Kassianidou

Brand

Schwarz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…, 2001; Labouesse et al. , 2015, 2016). Of interest, some mechanical tension across a cell remains after treatment with such an inhibitor, potentially reflecting filament cross-linking in the actomyosin bundles (Labouesse et al.…”

Section: Modulation Of Force Generation In Actomyosin Bundlesmentioning

confidence: 99%

Dissipation of contractile forces: the missing piece in cell mechanics

Kurzawa

Vianay

Senger

et al. 2017

MBoC

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Mechanical forces are key regulators of cell and tissue physiology. The basic molecular mechanism of fiber contraction by the sliding of actin filament upon myosin leading to conformational change has been known for decades. The regulation of force generation at the level of the cell, however, is still far from elucidated. Indeed, the magnitude of cell traction forces on the underlying extracellular matrix in culture is almost impossible to predict or experimentally control. The considerable variability in measurements of cell-traction forces indicates that they may not be the optimal readout to properly characterize cell contractile state and that a significant part of the contractile energy is not transferred to cell anchorage but instead is involved in actin network dynamics. Here we discuss the experimental, numerical, and biological parameters that may be responsible for the variability in traction force production. We argue that limiting these sources of variability and investigating the dissipation of mechanical work that occurs with structural rearrangements and the disengagement of force transmission is key for further understanding of cell mechanics.

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“…http://dx.doi.org/10.1101/167270 doi: bioRxiv preprint first posted online sparsely distributed as a result of cell volume increase because their total amount per cell was unchanged. At this time, individual actin fibers may be stretched out, as they have an extensibility as high as 200% (Labouesse et al, 2016). These events may be involved in pressure-induced cell growth retardation.…”

Section: Discussionmentioning

confidence: 99%

Modest static pressure suppresses columnar epithelial cell proliferation in association with cell shape and cytoskeletal modifications

Hagiyama

Yabuta

Okuzaki

et al. 2017

Preprint

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Intraluminal pressure elevation can cause degenerative disorders, such as ileus and hydronephrosis, and the threshold is fairly low and constant, 20-30 cm H 2 O. We previously devised a novel two-chamber culture system subjecting cells cultured on a semipermeable membrane to increased culture medium height (water pressure up to 60 cm H 2 O). Here, we cultured several different cell lines using the low static pressure-loadable two-chamber system, and examined cell growth, cell cycle, and cell

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

Cited by 17 publications

References 26 publications

Geometry and network connectivity govern the mechanics of stress fibers

Geometry and network connectivity govern the mechanics of stress fibers

Dissipation of contractile forces: the missing piece in cell mechanics

Modest static pressure suppresses columnar epithelial cell proliferation in association with cell shape and cytoskeletal modifications

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