Use the force: membrane tension as an organizer of cell shape and motility

Diz-Muñoz, Alba; Fletcher, Daniel A.; Weiner, Orion D.

doi:10.1016/j.tcb.2012.09.006

Cited by 520 publications

(501 citation statements)

References 80 publications

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“…It has been shown that increasing membrane tension results in numerous intracellular signaling events, including the inhibition of Rac activation and actin assembly (20,39). Our results agree with these findings.…”

Section: Membrane Tension As a Signal For Late-stage Phagocytosissupporting

confidence: 92%

“…On a purely physical level, tension acts to restrict protrusions, forcing the cell to remain rounded. However, there is evidence that membrane tension is also involved in signaling intracellular processes via membrane-associated sensors (39). Moreover, membrane tension has been shown to play a role in phagocytosis-related signaling (20,21).…”

Section: Estimation Of Tension At the Onset Of Late-stage Contractionmentioning

confidence: 99%

See 1 more Smart Citation

Frustrated Phagocytic Spreading of J774A-1 Macrophages Ends in Myosin II-Dependent Contraction

Kovari

Wei

Chang

et al. 2016

Biophysical Journal

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Conventional studies of dynamic phagocytic behavior have been limited in terms of spatial and temporal resolution due to the inherent three-dimensionality and small features of phagocytosis. To overcome these issues, we use a series of frustrated phagocytosis assays to quantitatively characterize phagocytic spreading dynamics. Our investigation reveals that frustrated phagocytic spreading occurs in phases and is punctuated by a distinct period of contraction. The spreading duration and peak contact areas are independent of the surface opsonin density, although the opsonin density does affect the likelihood that a cell will spread. This reinforces the idea that phagocytosis dynamics are primarily dictated by cytoskeletal activity. Structured illumination microscopy reveals that F-actin is reorganized during the course of frustrated phagocytosis. F-actin in early stages is consistent with that observed in lamellipodial protrusions. During the contraction phase, it is bundled into fibers that surround the cell and is reminiscent of a contractile belt. Using traction force microscopy, we show that cells exert significant strain on the underlying substrate during the contraction phase but little strain during the spreading phase, demonstrating that phagocytes actively constrict during late-stage phagocytosis. We also find that latestage contraction initiates after the cell surface area increases by 225%, which is consistent with the point at which cortical tension begins to rise. Moreover, reducing tension by exposing cells to hypertonic buffer shifts the onset of contraction to occur in larger contact areas. Together, these findings provide further evidence that tension plays a significant role in signaling late-stage phagocytic activity.

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Section: Membrane Tension As a Signal For Late-stage Phagocytosissupporting

confidence: 92%

Section: Estimation Of Tension At the Onset Of Late-stage Contractionmentioning

confidence: 99%

Frustrated Phagocytic Spreading of J774A-1 Macrophages Ends in Myosin II-Dependent Contraction

Kovari

Wei

Chang

et al. 2016

Biophysical Journal

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“…However, an emerging field of research on ion channel regulation in recent years has been to explore the impact of membrane biophysical properties on the activity of different ion channels (16,17). It has been shown that membrane biophysical properties such as static plasma membrane tension (SPMT) have a significant impact on functions of some ion channels ranging from directly gating (e.g.…”

mentioning

confidence: 99%

Regulation of Piezo2 Mechanotransduction by Static Plasma Membrane Tension in Primary Afferent Neurons

Jia

Ikeda

Ling

et al. 2016

Journal of Biological Chemistry

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The Piezo2 channel is a newly identified mammalian mechanical transducer that confers rapidly adapting mechanically activated (RA-MA) currents in primary afferent neurons. The Piezo2 channels sense rapid membrane displacement, but it is not clear whether they are sensitive to osmotic swelling, which slowly increases static plasma membrane tension (SPMT). Here, we show that SPMT exerts a profound impact on the mechanical sensitivity of RA-MA channels in primary afferent neurons. RA-MA currents are greatly enhanced, and the mechanical threshold was reduced in both primary afferent neurons of rat dorsal root ganglia (DRG) and HEK293 cells heterologously expressing Piezo2 when these cells undergo osmotic swelling to increase SPMT. Osmotic swelling switches the kinetics of RA-MA currents to the slowly adapting type in both cultured DRG neurons and HEK293 cells heterologously expressing Piezo2. The potentiation of RA-MA currents is abolished when cultured DRG neurons are treated with cytochalasin D, an actin filament disruptor that prevents SPMT of cultured DRG neurons from an increase by osmotic swelling. Osmotic swelling significantly increases DRG neuron mechano-excitability such that a subthreshold mechanical stimulus can result in action potential firing. Behaviorally, the mechanical hind paw withdrawal threshold in rats is reduced following the injection of a hypotonic solution, but this osmotic effect is abolished when cytochalasin D or Gd 3؉ is co-administered with the hypoosmotic solution. Taken together, our findings suggest that Piezo2-mediated mechanotransduction is regulated by SPMT in primary afferent neurons. Because SPMT can be changed by multiple biological factors, our findings may have broad implications in mechanical sensitivity under physiological and pathological conditions.

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“…In general, the mechanical phenotype of cells is related to their own vital parameters. 2,3,[6][7][8][9][10][11][12][13] The Atomic Force Microscope 14,15 (AFM) has proved to be a valuable tool for the quantitative characterization of static and frequency-dependent mechanical properties of micro-and nanostructures, including biological specimens, [16][17][18][19][20][21][22] thanks to its ability to sense and apply nanoscale forces, and to capture the three-dimensional topography of samples in different environments, including physiological buffers. Several papers report on the measurement by AFM of modulations in cellular elasticity induced by variations in the environmental conditions, like drugs targeting specific cytoskeletal components, [23][24][25] by changes in the elasticity and surface energy of the substrate, [26][27][28] as well as by the correlation between cells' elasticity and their patho-physiological state, including cancer diseases.…”

Section: Introductionmentioning

confidence: 99%

Nanomechanical and topographical imaging of living cells by atomic force microscopy with colloidal probes

Puricelli

Galluzzi

Schulte

et al. 2015

Review of Scientific Instruments

161

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Atomic Force Microscopy (AFM) has a great potential as a tool to characterize mechanical and morphological properties of living cells; these properties have been shown to correlate with cells' fate and patho-physiological state in view of the development of novel early-diagnostic strategies. Although several reports have described experimental and technical approaches for the characterization of cellular elasticity by means of AFM, a robust and commonly accepted methodology is still lacking.Here we show that micrometric spherical probes (also known as colloidal probes) are well suited for performing a combined topographic and mechanical analysis of living cells, with spatial resolution suitable for a complete and accurate mapping of cell morphological and elastic properties, and superior reliability and accuracy in the mechanical measurements with respect to conventional and widely used sharp AFM tips. We address a number of issues concerning the nanomechanical analysis, including the applicability of contact mechanical models and the impact of a constrained contact geometry on the measured Young's modulus (the finite-thickness effect). We have tested our protocol by imaging living PC12 and MDA-MB-231 cells, in order to demonstrate the importance of the correction of the finite-thickness effect and the change in Young's modulus induced by the action of a cytoskeleton-targeting drug.

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Use the force: membrane tension as an organizer of cell shape and motility

Cited by 520 publications

References 80 publications

Frustrated Phagocytic Spreading of J774A-1 Macrophages Ends in Myosin II-Dependent Contraction

Frustrated Phagocytic Spreading of J774A-1 Macrophages Ends in Myosin II-Dependent Contraction

Regulation of Piezo2 Mechanotransduction by Static Plasma Membrane Tension in Primary Afferent Neurons

Nanomechanical and topographical imaging of living cells by atomic force microscopy with colloidal probes

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