Phase geometries of two-dimensional excitable waves govern self-organized morphodynamics of amoeboid cells

Taniguchi, Daisuke; Ishihara, Shuji; Oonuki, Takehiko; Honda‐Kitahara, Mai; Kaneko, Kunihiko; Sawai, Shujiro

doi:10.1073/pnas.1218025110

Cited by 135 publications

(209 citation statements)

References 46 publications

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“…4) (8,27). Perturbation of other networks, by disrupting G proteins or actin cytoskeleton, also affected the apparent excitability of the signal transduction network (8,9,28). Even if a stimulus entered at one point, for example through actin cytoskeleton, the activation of the signal transduction network could be required to amplify the signal.…”

Section: Discussionmentioning

confidence: 99%

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Artemenko

Axiotakis

Borleis

et al. 2016

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

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Signal transduction pathways activated by chemoattractants have been extensively studied, but little is known about the events mediating responses to mechanical stimuli. We discovered that acute mechanical perturbation of cells triggered transient activation of all tested components of the chemotactic signal transduction network, as well as actin polymerization. Similarly to chemoattractants, the shear flow-induced signal transduction events displayed features of excitability, including the ability to mount a full response irrespective of the length of the stimulation and a refractory period that is shared with that generated by chemoattractants. Loss of G protein subunits, inhibition of multiple signal transduction events, or disruption of calcium signaling attenuated the response to acute mechanical stimulation. Unlike the response to chemoattractants, an intact actin cytoskeleton was essential for reacting to mechanical perturbation. These results taken together suggest that chemotactic and mechanical stimuli trigger activation of a common signal transduction network that integrates external cues to regulate cytoskeletal activity and drive cell migration.biochemical excitability | shear stress | motility | biomechanics | inflammation

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Section: Discussionmentioning

confidence: 99%

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Artemenko

Axiotakis

Borleis

et al. 2016

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

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“…Note that for amoebae, recently time-resolved traction forces could be related to alternating protrusion, contraction, retraction and relaxation cycles. 60,61 Although amoebae move differently (by pseudopods) and have a different adhesion mechanism (devoid of integrins), extensions of our modeling approach could be of value for this system as well.…”

Section: Complex Modes Of Movementmentioning

confidence: 99%

Modeling crawling cell movement on soft engineered substrates

2014

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Self-propelled motion, emerging spontaneously or in response to external cues, is a hallmark of living organisms. Systems of self-propelled synthetic particles are also relevant for multiple applications, from targeted drug delivery to the design of self-healing materials. Self-propulsion relies on the force transfer to the surrounding. While self-propelled swimming in the bulk of liquids is fairly well characterized, many open questions remain in our understanding of self-propelled motion along substrates, such as in the case of crawling cells or related biomimetic objects. How is the force transfer organized and how does it interplay with the deformability of the moving object and the substrate? How do the spatially dependent traction distribution and adhesion dynamics give rise to complex cell behavior? How can we engineer a specific cell response on synthetic compliant substrates? Here we generalize our recently developed model for a crawling cell by incorporating locally resolved traction forces and substrate deformations.The model captures the generic structure of the traction force distribution and faithfully reproduces experimental observations, like the response of a cell on a gradient in substrate elasticity (durotaxis). It also exhibits complex modes of cell movement such as "bipedal" motion. Our work may guide experiments on cell traction force microscopy and substrate-based cell sorting and can be helpful for the design of biomimetic "crawlers" and active and reconfigurable self-healing materials.

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“…Dictyostelium discoideum AX4 cells expressing Epac1camps (Epac1camps/AX4) (24), PH domain of CRAC fused to monomeric red fluorescent protein (mRFP) (PH CRAC -RFP/AX4) (43), and both PH CRAC -RFP and Epac1camps (Epac1camps PH CRAC -RFP/AX4) were used. For coexpression, Epac1camps/AX4 cells were transformed with PH CRAC -RFP expression vector by electroporation.…”

Section: Methodsmentioning

confidence: 99%

Fold-change detection and scale invariance of cell–cell signaling in social amoeba

Kamino

Kondo

Nakajima

et al. 2017

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

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Cell-cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively give rise to oscillations and waves of cyclic adenosine 3′,5′-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change-dependent response at the singlecell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism.fold-change detection | oscillations | collective behavior | Dictyostelium | robustness C ell-cell signaling lies at the basis of development and maintenance of multicellular forms of life. Extracellular signals are often subject to greater fluctuations in the size of extracellular space and the number of cells (Fig. 1A), not to mention nonspecific binding to other molecules, degradation, and dilution. These factors introduce an uncertainty to the detectable number of extracellular ligand molecules, thus posing a threat to the fidelity of cell-cell communication. One of the means by which cells could cope with such uncertainties is to base their behavioral decisions on temporal changes in the extracellular signals. Persistent stimuli are often ignored while their changes in time elicit transient responses-a property collectively called adaptation (1-3). Recent studies have highlighted cellular response whose magnitude appears to be dictated by the fold change in the input stimuli-a property referred to as "fold-change detection" (FCD) (4, 5). In bacterial chemotaxis, cells respond adaptively to a fold change in chemoattractant concentration (6) so that their search patterns depend only on the spatial profiles of the chemoattractant irrespective of its absolute level. Fold-change dependence is also implied in eukaryotic chemotactic response (7, 8) as well as cell fate control and gene regulation in Xenopus embryo (9), Drosophila imaginal disk (10), and mammalian cells (11). These studies have shed light on the role of FCD for a simple unidirectional signal transduction from an extracellular ligand-receptor interaction (input) to a cellular response (output). However, cell-cell signaling and multicellular systems as a whole often use secretion and sensing of the same molecules (12), whereby the output is fed back to the responding cell itself in addition to the neighboring cells, thus forming a complex bidirectional signal transduction system. Th...

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Phase geometries of two-dimensional excitable waves govern self-organized morphodynamics of amoeboid cells

Cited by 135 publications

References 46 publications

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Modeling crawling cell movement on soft engineered substrates

Fold-change detection and scale invariance of cell–cell signaling in social amoeba

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