4D Traction Force Microscopy Reveals Asymmetric Cortical Forces in Migrating<i>Dictyostelium</i>Cells

Delanoë-Ayari, Hélène; Rieu, Jean-Paul; Sano, Masaki

doi:10.1103/physrevlett.105.248103

Cited by 122 publications

(126 citation statements)

References 22 publications

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“…Previous studies have reported downward pushing forces into the substrate that suggested a role for nuclear compression (22,25), but we find minimal forces exerted in the nuclear and perinuclear regions. This discrepancy may result from differences in cell type (fibroblasts vs. endothelial cells or Dictyostelium), cell shape (spread vs. round), hydrogel rigidity (∼6.5 kPa in this study vs. 400 Pa, ∼4 kPa for previous studies), or spatial resolution of the different TFM methods.…”

Section: Discussioncontrasting

confidence: 46%

“…Interestingly, recent studies have demonstrated that cells on planar substrata exert significant vertical (normal) tractions, indicating that patterns of cellular force generation are more complex than previously thought (22)(23)(24)(25). However, mapping these multidimensional traction stresses with a high spatiotemporal resolution has been challenging, and there is no clear agreement on the dynamics and the location of the normal stresses.…”

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confidence: 94%

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Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions

Legant

Choi

Miller

et al. 2012

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

251

239

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Recent methods have revealed that cells on planar substrates exert both shear (in-plane) and normal (out-of-plane) tractions against the extracellular matrix (ECM). However, the location and origin of the normal tractions with respect to the adhesive and cytoskeletal elements of cells have not been elucidated. We developed a highspatiotemporal-resolution, multidimensional (2.5D) traction force microscopy to measure and model the full 3D nature of cellular forces on planar 2D surfaces. We show that shear tractions are centered under elongated focal adhesions whereas upward and downward normal tractions are detected on distal (toward the cell edge) and proximal (toward the cell body) ends of adhesions, respectively. Together, these forces produce significant rotational moments about focal adhesions in both protruding and retracting peripheral regions. Temporal 2.5D traction force microscopy analysis of migrating and spreading cells shows that these rotational moments are highly dynamic, propagating outward with the leading edge of the cell. Finally, we developed a finite element model to examine how rotational moments could be generated about focal adhesions in a thin lamella. Our model suggests that rotational moments can be generated largely via shear lag transfer to the underlying ECM from actomyosin contractility applied at the intracellular surface of a rigid adhesion of finite thickness. Together, these data demonstrate and probe the origin of a previously unappreciated multidimensional stress profile associated with adhesions and highlight the importance of new approaches to characterize cellular forces.cell mechanics | mechanotransduction | migration | actin U nderstanding how cells generate and respond to mechanical forces is critical in cell biology. In anchorage-dependent cells, myosin-II cross-links and contracts actin filaments to generate tension, which is transmitted to the extracellular matrix (ECM) via integrin-mediated adhesions (1-4). The traction stresses (force per area) exerted between adhesions and the ECM drive cell spreading and migration in morphogenesis (5, 6), wound healing (7), and tumor metastasis (8, 9). In addition, these stresses induce changes in adhesion signaling, cytoskeletal reorganization, and gene expression (4, 10-13), thereby regulating functions such as proliferation (14, 15) and differentiation (16,17).Measurements of cellular traction stresses have advanced our understanding of mechanotransduction and enabled quantitative modeling of cellular interactions with the ECM (18-20). These measurements reveal that cells exert inwardly oriented tractions at their periphery, where focal adhesions grow centripetally (3,4,21). However, the vast majority of methods (collectively termed traction force microscopy, TFM) have assumed that cells exert only shear forces (parallel to the plane of the substrate). Interestingly, recent studies have demonstrated that cells on planar substrata exert significant vertical (normal) tractions, indicating that patterns of cellular force generation...

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Section: Discussioncontrasting

confidence: 46%

mentioning

confidence: 94%

Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions

Legant

Choi

Miller

et al. 2012

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

251

239

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“…The schematic illustration in Figure 5E shows the suggested mechanism of how cell tension creates a pushing force against the rigid substrate on convex spherical geometries while a pulling force is created on concave ones – with a consequential impact on the nuclear morphology. Such a push‐pull mechanism was already presented by Delanoë‐Ayari and co‐workers for flat surfaces 34. It describes that tensile cytoskeletal (pull) forces pointing from the focal adhesions toward the cell's center create significant downward orientated compressive (push) forces at the nucleus 34, 35.…”

Section: Resultsmentioning

confidence: 87%

“…Such a push‐pull mechanism was already presented by Delanoë‐Ayari and co‐workers for flat surfaces 34. It describes that tensile cytoskeletal (pull) forces pointing from the focal adhesions toward the cell's center create significant downward orientated compressive (push) forces at the nucleus 34, 35. On very soft materials this leads to a deformation of the substrate rather than of the nucleus (see34, 35 for detailed explanation).…”

Section: Resultsmentioning

confidence: 87%

Surface Curvature Differentially Regulates Stem Cell Migration and Differentiation via Altered Attachment Morphology and Nuclear Deformation

et al. 2016

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Signals from the microenvironment around a cell are known to influence cell behavior. Material properties, such as biochemical composition and substrate stiffness, are today accepted as significant regulators of stem cell fate. The knowledge of how cell behavior is influenced by 3D geometric cues is, however, strongly limited despite its potential relevance for the understanding of tissue regenerative processes and the design of biomaterials. Here, the role of surface curvature on the migratory and differentiation behavior of human mesenchymal stem cells (hMSCs) has been investigated on 3D surfaces with well‐defined geometric features produced by stereolithography. Time lapse microscopy reveals a significant increase of cell migration speed on concave spherical compared to convex spherical structures and flat surfaces resulting from an upward‐lift of the cell body due to cytoskeletal forces. On convex surfaces, cytoskeletal forces lead to substantial nuclear deformation, increase lamin‐A levels and promote osteogenic differentiation. The findings of this study demonstrate a so far missing link between 3D surface curvature and hMSC behavior. This will not only help to better understand the role of extracellular matrix architecture in health and disease but also give new insights in how 3D geometries can be used as a cell‐instructive material parameter in the field of biomaterial‐guided tissue regeneration.

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“…This means that actomyosin contractility is triggered by the same molecular signal (probably calcium level [5]) whatever its fine structure (filamentous cortex or fibrils). For amoeboid microplasmodia, one can estimate the cortical tension transmitted to the substrate by simply dividing the peripheral force by the perimeter L, t C ¼ F/L ¼ 5-20 mN m 21 , a value intermediate between the ones previously measured for Dictyostelium at single cell and slug stages, respectively [11,18]. For chain type microplasmodia, assuming that the force per contractile unit (typically about 5 mN) is mostly transmitted all around a ring of about R ¼ 50 mm radius (dotted line in figure 8a), we can estimate a head tension t H ¼ F=2pR ≃ 30 mN m À1 , a value quite similar to t C .…”

Section: Discussionmentioning

confidence: 99%

Periodic traction in migrating large amoeba ofPhysarum polycephalum

Rieu

Delanoë-Ayari

Takagi

et al. 2015

J. R. Soc. Interface.

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The slime mould Physarum polycephalum is a giant multinucleated cell exhibiting well-known Ca 2þ -dependent actomyosin contractions of its vein network driving the so-called cytoplasmic shuttle streaming. Its actomyosin network forms both a filamentous cortical layer and large fibrils. In order to understand the role of each structure in the locomotory activity, we performed birefringence observations and traction force microscopy on excised fragments of Physarum. After several hours, these microplasmodia adopt three main morphologies: flat motile amoeba, chain types with round contractile heads connected by tubes and motile hybrid types. Each type exhibits oscillations with a period of about 1.5 min of cell area, traction forces and fibril activity (retardance) when fibrils are present. The amoeboid types show only peripheral forces while the chain types present a neverreported force pattern with contractile rings far from the cell boundary under the spherical heads. Forces are mostly transmitted where the actomyosin cortical layer anchors to the substratum, but fibrils maintain highly invaginated structures and contribute to forces by increasing the length of the anchorage line. Microplasmodia are motile only when there is an asymmetry in the shape and/or the force distribution.

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4D Traction Force Microscopy Reveals Asymmetric Cortical Forces in MigratingDictyosteliumCells

Cited by 122 publications

References 22 publications

Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions

Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions

Surface Curvature Differentially Regulates Stem Cell Migration and Differentiation via Altered Attachment Morphology and Nuclear Deformation

Periodic traction in migrating large amoeba ofPhysarum polycephalum

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