Control of Directed Cell Migration In Vivo by Membrane-to-Cortex Attachment

Diz-Muñoz, Alba; Krieg, Michael; Bergert, Martin; Ibarlucea-Benitez, Itziar; Müller, Daniel J.; Paluch, Ewa K.; Heisenberg, Carl‐Philipp

doi:10.1371/journal.pbio.1000544

Cited by 253 publications

(301 citation statements)

References 52 publications

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“…The asymmetric distribution of this small density of talin links seems to be enough to drive directed motion in amoebae (28). Similar observations are reported for zebrafish cells (31). For completeness, assuming a ligand length d~1 nm, we find…”

Section: Discussion Of Micropipette Experimentssupporting

confidence: 86%

“…Whenever the equilibrium stress exceeds the critical value s*, we expect the cell membrane to detach spontaneously. Micropipette aspiration (12,16,(27)(28)(29), among other techniques (11,30,31), allows us to apply pressure perturbations of controlled intensity and area. Pressure perturbations can be supplemented with perturbations on relevant cell parameters such as myosin activity and link or cortex density, by genetics (27)(28)(29) or direct drug treatment (10,11,31).…”

Section: Biophysical Journal 108(8) 1878-1886mentioning

confidence: 99%

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Model for Probing Membrane-Cortex Adhesion by Micropipette Aspiration and Fluctuation Spectroscopy

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Casademunt

Brugués

et al. 2015

Biophysical Journal

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We propose a model for membrane-cortex adhesion that couples membrane deformations, hydrodynamics, and kinetics of membrane-cortex ligands. In its simplest form, the model gives explicit predictions for the critical pressure for membrane detachment and for the value of adhesion energy. We show that these quantities exhibit a significant dependence on the active acto-myosin stresses. The model provides a simple framework to access quantitative information on cortical activity by means of micropipette experiments. We also extend the model to incorporate fluctuations and show that detailed information on the stability of membrane-cortex coupling can be obtained by a combination of micropipette aspiration and fluctuation spectroscopy measurements.

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Section: Discussion Of Micropipette Experimentssupporting

confidence: 86%

Section: Biophysical Journal 108(8) 1878-1886mentioning

confidence: 99%

Model for Probing Membrane-Cortex Adhesion by Micropipette Aspiration and Fluctuation Spectroscopy

Alert

Casademunt

Brugués

et al. 2015

Biophysical Journal

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show abstract

“…There is evidence that this membrane tension is important for driving cell migration both in vitro and in vivo (46,47,65). Chemically reducing membrane tension may accelerate cell spreading and lamellipodial extension (19), whereas increasing membrane tension by hypotonic treatment may cause lamellipodial and filopodial retraction (66).…”

Section: Discussionmentioning

confidence: 99%

Myosin Light Chain Kinase (MLCK) Regulates Cell Migration in a Myosin Regulatory Light Chain Phosphorylation-independent Mechanism

Chen

Tao

Wen

et al. 2014

Journal of Biological Chemistry

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Background: MLCK in cell migration remains controversial. Results: MLCK deletion causes enhanced cell protrusion along with a reduction of membrane tension and is rescued by kinase-dead MLCK or five-DFRXXL motif. Conclusion: MLCK regulates cell migration not by myosin regulatory light chain phosphorylation but possibly through a membrane tension-based mechanism. Significance: Our results shed light on a novel regulatory mechanism of protrusion during cell migration.

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“…There are several proposals for bleb site selection, including by local contraction of the cortex (8) or local weakening of it (16,17) and by local weakening of the attachment between cortex and membrane (18,19). In cells of the parasite E. histolytica, where blebs expand rapidly, there are, however, no visible signs of a weakening of the actin cortex before a bleb forms (10) and likewise blebs in Dictyostelium form without detectable weakening of the cortex.…”

mentioning

confidence: 99%

How blebs and pseudopods cooperate during chemotaxis

Tyson

Zatulovskiy

Kay

et al. 2014

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

113

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Two motors can drive extension of the leading edge of motile cells: actin polymerization and myosin-driven contraction of the cortex, producing fluid pressure and the formation of blebs. Dictyostelium cells can move with both blebs and actin-driven pseudopods at the same time, and blebs, like pseudopods, can be orientated by chemotactic gradients. Here we ask how bleb sites are selected and how the two forms of projection cooperate. We show that membrane curvature is an important, yet overlooked, factor. Dictyostelium cells were observed moving under agarose, which efficiently induces blebbing, and the dynamics of membrane deformations were analyzed. Blebs preferentially originate from negatively curved regions, generated on the flanks of either extending pseudopods or blebs themselves. This is true of cells at different developmental stages, chemotaxing to either folate or cyclic AMP and moving with both blebs and pseudopods or with blebs only. A physical model of blebbing suggests that detachment of the cell membrane is facilitated in concave areas of the cell, where membrane tension produces an outward directed force, as opposed to pulling inward in convex regions. Our findings assign a role to membrane tension in spatially coupling blebs and pseudopods, thus contributing to clustering protrusions to the cell front.C rawling cells must restrict protrusions to a limited part of their periphery if they are to move efficiently, and when these cells chemotax, the location of projections must be further controlled by the chemotactic gradient (1-3). Cellular protrusions are of two main types: those driven by actin polymerization, such as pseudopods or lamellipods, and those driven by fluid pressure, which are usually called blebs. Blebs form when the cell membrane locally detaches from the underlying cortex and is driven outward by hydrostatic pressure, created by myosin-IIdriven contraction of the cortex (4, 5). When blebs form, the cortex is left behind as an "F-actin scar," which depolymerizes, while a new actin cortex forms at the freshly exposed membrane.Blebbing is important in cells migrating in three-dimensional environments, such as during tumor invasion (6, 7), zebrafish primordial germ cell migration (8, 9), or migration of the pathogen Entamoeba histolytica in the liver (10). Dictyostelium amoebae can also move with blebs (11). In standard conditions on a 2D surface under buffer, they move mainly with F-actin-driven pseudopods, but switch progressively to bleb-driven motility when faced with mechanical resistance to their movement (12). This can be conveniently applied by inducing the cells to migrate under an elastic overlay, such as agarose, which they must deform to progress (13). Blebbing is stimulated by acute treatment with the chemoattractant cyclic AMP (14), and blebs can be chemotactically orientated by cyclic-AMP gradients (11,12).Actin-driven pseudopods are preferentially formed up-gradient by chemotaxing cells, and they can be induced on the flanks of cells by applying a steep gradient of ch...

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Control of Directed Cell Migration In Vivo by Membrane-to-Cortex Attachment

Abstract: Analysis of cell migration in vivo combined with biophysical measurements reveals how membrane-to-cortex attachment fine-tunes the type of protrusions formed by cells and, as a consequence, controls directed migration during zebrafish gastrulation.

Cited by 253 publications

References 52 publications

Model for Probing Membrane-Cortex Adhesion by Micropipette Aspiration and Fluctuation Spectroscopy

Model for Probing Membrane-Cortex Adhesion by Micropipette Aspiration and Fluctuation Spectroscopy

Myosin Light Chain Kinase (MLCK) Regulates Cell Migration in a Myosin Regulatory Light Chain Phosphorylation-independent Mechanism

How blebs and pseudopods cooperate during chemotaxis

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