Membrane tension controls adhesion positioning at the leading edge of cells

Pontes, Bruno; Monzo, Pascale; Gole, Leena; Roux, Anabel‐Lise Le; Kosmalska, Anita Joanna; Tam, Zhi Yang; Luo, Weiwei; Kan, Sophie; Viasnoff, Virgile; Roca‐Cusachs, Pere; Tucker-Kellogg, Lisa; Gauthier, Nils C.

doi:10.1083/jcb.201611117

Cited by 111 publications

(112 citation statements)

References 69 publications

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“…2d, e). This is consistent with previous studies showing that cell spreading is facilitated by decreased membrane tension (11) (12). Therefore, we conclude that cell spreading during exit from naive pluripotency occurs concomitantly with a decrease in plasma membrane tension.…”

supporting

confidence: 93%

Membrane tension mediated mechanotransduction drives fate choice in embryonic stem cells

Belly

Jones

Paluch

et al. 2019

Preprint

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Changes in cell shape and mechanics frequently accompany cell fate transitions. Yet how mechanics affects the regulatory pathways controlling cell fate is poorly understood. To probe the interplay between shape, mechanics and fate, we used embryonic stem (ES) cells, which spread as they undergo early differentiation. We found that this spreading is regulated by a betacatenin mediated decrease in plasma membrane tension. Strikingly, preventing the membrane tension decrease obstructs early differentiation of ES cells. We further find that blocking the decrease in membrane tension inhibits endocytosis of FGF signalling components, which direct the exit from the ES cell state. The early differentiation defects we observed can be rescued by increasing Rab5a-facilitated endocytosis. Thus, we show that a mechanically-triggered increase in endocytosis regulates fate transitions. Our findings are of fundamental importance for understanding how cell mechanics regulates biochemical signaling, and therefore cell fate.

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supporting

confidence: 93%

Membrane tension mediated mechanotransduction drives fate choice in embryonic stem cells

Belly

Jones

Paluch

et al. 2019

Preprint

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“…37 The ruffles extended beyond the main cell body and stratified into denser independent twines ( Figure 2B and Movie M3) presumably due to folding-over and buckling. 38 The twines were found to grow in length at the rate of ~0.1 μm/s, and swing freely (in 3D) similarly to reported angular rotations of filopodia, [39][40][41][42] which allowed for selected ones to engage (attach) to a neighboring fiber. The attachment to neighboring fiber occurred in a matter of seconds ( Figure 2C and Movie M4).…”

Section: Twines Emerge From Actin Ruffles and Engage Neighboring Fibesupporting

confidence: 55%

Force-exerting lateral protrusions in fibroblastic cell contraction

Padhi

Singh

Franco‐Barraza

et al. 2019

Preprint

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Aligned extracellular matrix fibers impart an elongated cell morphology and enable fibroblasts to undergo myofibroblastic activation. Yet the biomechanical intricacies that are associated with this microenvironmental phenomenon are unknown. Here, we identify a new role of lateral protrusions, originating anywhere along elongated fibroblastic cells, which apply fiber-deflecting contractile forces. Using aligned fiber networks that serve as force sensors, we quantitate the role of lateral nano-projections (twines) that mature into "perpendicular lateral protrusions" (PLPs) through the formation of twine-bridges, thus allowing elongated cells to spread laterally and effectively contract. Using quantitative microscopy at high spatiotemporal resolution, we show that twines of varying lengths can originate from stratification of cyclic actin waves traversing along the entire length of the cell. Primary twines swing freely in 3D and engage with neighboring extracellular fibers in interaction times of seconds. Once engaged, an actin lamellum grows along the length of primary twine and re-stratifies to form a secondary twine. Engagement of secondary twine with the neighboring fiber leads to the formation of twine-bridge, a critical step in providing a conduit for actin to advance along and populate the twine-bridge. Through arrangement of fiber networks in varying configurations, we confirm that anisotropic fibrous environments are fertile for PLP dynamics, and importantly force-generating PLPs are oriented perpendicular to the parent cell body. Furthermore, cell spreading onto multiple fibers and myofibroblastic-like contraction occur through PLPs. Our identification of force exertion by PLPs identifies a possible explanation for cancer-associated desmoplastic expansion, at single-cell resolution, thus providing new clinical intervention opportunities.

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“…Indeed, when plasma membrane tension was experimentally increased or decreased in migrating fish keratocytes, more filaments acquired orientations around 0° and ±70°, as compared with two major peaks of ±35° at the steady state (Figure 1b). Since small-scale periodic compression and relaxation of the lamellipodial network also occur without experimental interventions [4**,10], periodic rearrangements between the slingshot and trident network geometry may constantly occur at the leading edge.…”

Section: Actin Cytoskeleton In Protrusionmentioning

confidence: 99%

Ultrastructure of the actin cytoskeleton

Svitkina

2018

Current Opinion in Cell Biology

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The actin cytoskeleton is the primary force-generating machinery in the cell, which can produce pushing (protrusive) forces using energy of actin polymerization and pulling (contractile) forces via sliding of bipolar filaments of myosin II along actin filaments, as well as perform other key functions. These functions are essential for whole cell migration, cell interaction with the environment, mechanical properties of the cell surface and other key aspects of cell physiology. The actin cytoskeleton is a highly complex and dynamic system of actin filaments organized into various superstructures by multiple accessory proteins. High resolution architecture of functionally distinct actin arrays provides key clues for understanding actin cytoskeleton functions. This review summarizes recent advance in our understanding of the actin cytoskeleton ultrastructure.

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Membrane tension controls adhesion positioning at the leading edge of cells

Abstract: Pontes et al. show that plasma membrane mechanics exerts an upstream control during cell motility. Variations in plasma membrane tension orchestrate the behavior of the cell leading edge, with increase–decrease cycles in tension promoting adhesion row positioning.

Cited by 111 publications

References 69 publications

Membrane tension mediated mechanotransduction drives fate choice in embryonic stem cells

Membrane tension mediated mechanotransduction drives fate choice in embryonic stem cells

Force-exerting lateral protrusions in fibroblastic cell contraction

Ultrastructure of the actin cytoskeleton

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