Insight from the maximal activation of the signal transduction excitable network in
            <i>Dictyostelium discoideum</i>

Edwards, Marc; Cai, Huaqing; Abubaker‐Sharif, Bedri; Lan, Yu; Lampert, Thomas J.; Devreotes, Peter N.

doi:10.1073/pnas.1710480115

Cited by 22 publications

(37 citation statements)

References 41 publications

(59 reference statements)

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“…The present framework of data analysis potentially provides means to test and improve specific models of migrating cells. Distinctions between various excitable (14,41,61) and cell polarity models (38,62,63) will become more relevant as we proceed further to analyze detailed geometries and dynamics associated with specific cells and conditions. For example, our ideal cell model gave more frequent rise to pseudopods from the tail region compared to the real cell data.…”

Section: Discussionmentioning

confidence: 99%

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Comparative mapping of crawling-cell morphodynamics in deep learning-based feature space

Imoto

Saito

Nakajima

et al. 2020

Preprint

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Navigation of fast migrating cells such as amoeba Dictyostelium and immune cells are tightly associated with their morphologies that range from steady polarized forms that support high directionality to those more complex and variable when making frequent turns. Model simulations are essential for quantitative understanding of these features and their origins, however systematic comparisons with real data are underdeveloped. Here, by employing deep-learning-based feature extraction combined with phase-field modeling framework, we show that a low dimensional feature space for 2D migrating cell morphologies obtained from the shape stereotype of keratocytes, Dictyostelium and neutrophils can be fully mapped by interlinked signaling network of cell-polarization and protrusion dynamics. Our analysis links the data-driven shape analysis to the underlying causalities by identifying key parameters critical for migratory morphologies both normal and aberrant under genetic and pharmacological perturbations. The results underscore the importance of deciphering self-organizing states and their interplay when characterizing morphological phenotypes.

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Section: Discussionmentioning

confidence: 99%

“…S3b,c) and non-bifurcating polarized cells (fig.S3f,g), we shall exclude these parameter regimes from the following analysis. Related oscillatory and fan-like morphologies have been addressed earlier(39)(40)(41).…”

mentioning

confidence: 89%

Comparative mapping of crawling-cell morphodynamics in deep learning-based feature space

Imoto

Saito

Nakajima

et al. 2020

Preprint

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“…While the presence of a threshold for activation in this cascade has been well documented in studies of chemotaxis of amoeboid cells [ 5 , 20 , 24 , 25 ], it is only recently that it has been appreciated that this threshold arises from the existence of an excitable network [ 9 , 10 , 26 – 32 ]. Recent advances in cell biology have allowed acute genetic perturbations of the signaling network that lower this threshold, leading to greater signaling activity, increased actin polymerization along the cell cortex, and faster moving cells [ 17 , 33 ].…”

Section: Discussionmentioning

confidence: 99%

The threshold of an excitable system serves as a control mechanism for noise filtering during chemotaxis

Bhattacharya

Iglesias

2018

PLoS ONE

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Chemotaxis, the migration of cells in the direction of a chemical gradient, is of utmost importance in various biological processes. In recent years, research has demonstrated that the underlying mechanism that controls cell migration is an excitable network. One of the properties that characterizes excitability is the presence of a threshold for activation. Here, we show that excitable systems possess noise filtering capabilities that enable faster and more efficient directed migration compared to other systems that also include a threshold, such as ultrasensitive switches. We demonstrate that this filtering ability is a consequence of the varying responses of excitable systems to step and pulse stimuli. Whereas the response to step inputs is determined solely by the magnitude of the stimulus, for pulse stimuli, the response depends on both the magnitude and duration of the stimulus. We then show that these two forms of threshold behavior can be decoupled from one another, allowing finer control in chemotaxis. Finally, we use a simple model of chemotaxis to demonstrate that cells that rely on an excitable system display faster and more effective directed migration that a hypothetical cell guided by an ultra-sensitive switch.

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“…The dynamics of chemotaxis and its regulatory pathways have continued to be the subject of intense studies in Dictyostelium, in particular for understanding how the different signalling networks are wired together, and for generating models of random and oriented cell motility in 2-and 3-D, often anticipating results and insights that have promoted research in neutrophils and other organisms (Stuelten et al, 2018;van Haastert et al, 2018;Liu et al, 2018;Li et al, 2018;Nichols et al, 2015;Edwards et al, 2018).…”

Section: Past and Present Of A Model Organismmentioning

confidence: 99%

“…Most recent reviews or relevant papers Cytoskeleton, motility and chemotaxis Gräf et al 2015;Rivero and Xiong, 2016;Stuelten et al 2018;Liu et al 2018;van Haastert et al 2018;Edwards et al 2018;Kriebel et al 2018;Nichols et al 2019;Miyanaga et al, 2018 Phagocytosis, macropinocytosis and endo-lysosomal traffic Williams and Kay, 2018;Williams et al 2019;Pan et al 2018;Meena and Kimmel, 2017;Buckley et al, 20192019;Dunn et al 2018;Dinh et al 2018;Marinović et al, 2019 Cytokinesis Srivastava et al, 2016 Cell adhesion Fujimori et al 2019;Lampert et al 2017 Autophagy Mesquita et al 2017;Fischer et al 2019 Development, pattern formation Yamada and Schaap, 2019 Social evolution Ostrowski, 2019 Dictyostelium as model organism 325…”

Section: Biological Processmentioning

confidence: 99%

The past, present and future of Dictyostelium as a model system

Bozzaro¹

2019

Int. J. Dev. Biol.

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The social amoeba Dictyostelium discoideum has been a preferred model organism during the last 50 years, particularly for the study of cell motility and chemotaxis, phagocytosis and macropinocytosis, intercellular adhesion, pattern formation, caspase-independent cell death and more recently autophagy and social evolution. Being a soil amoeba and professional phagocyte, thus exposed to a variety of potential pathogens, D. discoideum has also proven to be a powerful genetic and cellular model for investigating host-pathogen interactions and microbial infections. The finding that the Dictyostelium genome harbours several homologs of human genes responsible for a variety of diseases has stimulated their analysis, providing new insights into the mechanism of action of the encoded proteins and in some cases into the defect underlying the disease. Recent technological developments have covered the genetic gap between mammals and non-mammalian model organisms, challenging the modelling role of the latter. Is there a future for Dictyostelium discoideum as a model organism? Peculiarities and advantages of Dictyostelium discoideum as model organismAmong the non-mammalian model organisms, Dictyostelium discoideum (in the following Dictyostelium) is unique, due to cell division and development being totally uncoupled, and because of the transition from a unicellular to a multicellular stage during the life cycle. Growing cells proliferate by binary fission but do not differentiate, whereas starving cells undergo multicellular development and differentiation without dividing and without any need for external nutrients. Thus growth and development can be studied separately, and several non-lethal mutants can be isolated

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Insight from the maximal activation of the signal transduction excitable network in Dictyostelium discoideum

Cited by 22 publications

References 41 publications

Comparative mapping of crawling-cell morphodynamics in deep learning-based feature space

Comparative mapping of crawling-cell morphodynamics in deep learning-based feature space

The threshold of an excitable system serves as a control mechanism for noise filtering during chemotaxis

The past, present and future of Dictyostelium as a model system

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