Both contractile axial and lateral traction force dynamics drive amoeboid cell motility

Bastounis, Effie; Meili, Ruedi; Álvarez-González, Begoña; Francois, Joshua; Álamo, Juan C. del; Firtel, Richard A.; Lasheras, Juan C.

doi:10.1083/jcb.201307106

Cited by 60 publications

(79 citation statements)

References 66 publications

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“…The 3D force patterns generated by cells lacking actomyosin contraction were similar to those observed for liquid drops when placed onto soft substrates, which exert upward forces due to surface tension around their edge, and downward forces due to fluid pressure under their center (36). These results are consistent with our previous two-dimensional observations that axial cell-substrate forces mediated by actomyosin contraction are lost in mhcA À and abp120 À cells (8,10,11), and suggest that cortical and membrane tension generate the 3D cell-substrate forces observed in these cell strains.…”

Section: Resultssupporting

confidence: 92%

“…2 A), still exert appreciable traction forces on their substrate (9)(10)(11). To understand the genesis of these forces, we measured the 3D cell-substrate forces in MyoII null cells (mhcA À ) and filamin null cells (abp120 À ), and those of their WT background strains (Ax3 and Ax2).…”

Section: Resultsmentioning

confidence: 99%

“…4, A and B, shows a kymographic representation of the instantaneous tangential and normal cell-substrate forces together with the contour of the cell and the location of its nucleus. In a space-time kymograph, the spatial data are aligned so that the cell axis is parallel to the y direction at each instant of time, and data from different instants of time are stacked together in the x direction (see Materials and Methods and Bastounis et al (11) for details).…”

Section: Cortical Tension Is Balanced By Increased Cytoplasmic Pressumentioning

confidence: 99%

“…However, there is a puzzling lack of correlation between the migration speed of amoeboid cells and the strength of the traction forces, and this strength is much larger than needed to overcome friction from the overlying fluid (8). The molecular and structural origins of the traction forces are also unclear, as migrating cells lacking MyoII or F-actin crosslinkers are still able to exert significant traction forces (8)(9)(10)(11). Our biomechanical understanding of cell movement is complicated further because migrating cells exert significant normal forces (perpendicular to the substrate) in addition to the tangential ones (12)(13)(14)(15).…”

Section: Introductionmentioning

confidence: 95%

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Three-Dimensional Balance of Cortical Tension and Axial Contractility Enables Fast Amoeboid Migration

Álvarez-González

Meili

Bastounis

et al. 2015

Biophysical Journal

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Fast amoeboid migration requires cells to apply mechanical forces on their surroundings via transient adhesions. However, the role these forces play in controlling cell migration speed remains largely unknown. We used three-dimensional force microscopy to measure the three-dimensional forces exerted by chemotaxing Dictyostelium cells, and examined wild-type cells as well as mutants with defects in contractility, internal F-actin crosslinking, and cortical integrity. We showed that cells pull on their substrate adhesions using two distinct, yet interconnected mechanisms: axial actomyosin contractility and cortical tension. We found that the migration speed increases when axial contractility overcomes cortical tension to produce the cell shape changes needed for locomotion. We demonstrated that the three-dimensional pulling forces generated by both mechanisms are internally balanced by an increase in cytoplasmic pressure that allows cells to push on their substrate without adhering to it, and which may be relevant for amoeboid migration in complex three-dimensional environments.

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Section: Resultssupporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Section: Cortical Tension Is Balanced By Increased Cytoplasmic Pressumentioning

confidence: 99%

Section: Introductionmentioning

confidence: 95%

See 2 more Smart Citations

Three-Dimensional Balance of Cortical Tension and Axial Contractility Enables Fast Amoeboid Migration

Álvarez-González

Meili

Bastounis

et al. 2015

Biophysical Journal

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“…Cells also need to coordinate their motion in streams which involves coordination of the cytoskeleton in neighbouring cells resulting in local force coordination [44,[92][93][94][95].…”

Section: Aggregationmentioning

confidence: 99%

Progress and perspectives in signal transduction, actin dynamics, and movement at the cell and tissue level: lessons fromDictyostelium

2016

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Movement of cells and tissues is a basic biological process that is used in development, wound repair, the immune response to bacterial invasion, tumour formation and metastasis, and the search for food and mates. While some cell movement is random, directed movement stimulated by extracellular signals is our focus here. This involves a sequence of steps in which cells first detect extracellular chemical and/or mechanical signals via membrane receptors that activate signal transduction cascades and produce intracellular signals. These intracellular signals control the motile machinery of the cell and thereby determine the spatial localization of the sites of force generation needed to produce directed motion. Understanding how force generation within cells and mechanical interactions with their surroundings, including other cells, are controlled in space and time to produce cell-level movement is a major challenge, and involves many issues that are amenable to mathematical modelling.

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Integration of Extracellular Matrices into Organ‐on‐Chip Systems

Kutluk

Bastounis

Constantinou

2023

Adv Healthcare Materials

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The extracellular matrix (ECM) is a complex, dynamic network present within all tissues and organs that not only acts as a mechanical support and anchorage point but can also direct fundamental cell behavior, function, and characteristics. Although the importance of the ECM is well established, the integration of well‐controlled ECMs into Organ‐on‐Chip (OoC) platforms remains challenging and the methods to modulate and assess ECM properties on OoCs remain underdeveloped. In this review, current state‐of‐the‐art design and assessment of in vitro ECM environments is discussed with a focus on their integration into OoCs. Among other things, synthetic and natural hydrogels, as well as polydimethylsiloxane (PDMS) used as substrates, coatings, or cell culture membranes are reviewed in terms of their ability to mimic the native ECM and their accessibility for characterization. The intricate interplay among materials, OoC architecture, and ECM characterization is critically discussed as it significantly complicates the design of ECM‐related studies, comparability between works, and reproducibility that can be achieved across research laboratories. Improving the biomimetic nature of OoCs by integrating properly considered ECMs would contribute to their further adoption as replacements for animal models, and precisely tailored ECM properties would promote the use of OoCs in mechanobiology.

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Both contractile axial and lateral traction force dynamics drive amoeboid cell motility

Abstract: During chemotactic movement, D. discoideum exhibits step-wise amoeboid motility driven by both contractile axial forces and lateral forces.

Cited by 60 publications

References 66 publications

Three-Dimensional Balance of Cortical Tension and Axial Contractility Enables Fast Amoeboid Migration

Three-Dimensional Balance of Cortical Tension and Axial Contractility Enables Fast Amoeboid Migration

Progress and perspectives in signal transduction, actin dynamics, and movement at the cell and tissue level: lessons fromDictyostelium

Integration of Extracellular Matrices into Organ‐on‐Chip Systems

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