An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations

Sawai, Shujiro; Thomason, Peter A.; Cox, Edward C.

doi:10.1038/nature03228

Cited by 164 publications

(199 citation statements)

References 27 publications

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“…In the majority of the papers published, cAMP is proposed to be uniformly emitted by cells in response to a cAMP signal, and the phosphodiesterase activity is either distributed uniformly extracellularly in space and time (Levine and Reynolds, 1991;Levine et al, 1996;Sawai et al, 2005), associated with the plasma membrane, or both (Pate and Odell, 1981;Tang and Othmer, 1995). Although both models are capable of reproducing many features of Dictyostelium aggregation, including the propagation of cAMP waves in characteristic spirals and the formation of stream-like aggregates, they are not perfect.…”

Section: Discussionmentioning

confidence: 99%

The Group Migration of Dictyostelium Cells Is Regulated by Extracellular Chemoattractant Degradation

Garcia

Rericha

Heger

et al. 2009

MBoC

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Starvation of Dictyostelium induces a developmental program in which cells form an aggregate that eventually differentiates into a multicellular structure. The aggregate formation is mediated by directional migration of individual cells that quickly transition to group migration in which cells align in a head-to-tail manner to form streams. Cyclic AMP acts as a chemoattractant and its production, secretion, and degradation are highly regulated. A key protein is the extracellular phosphodiesterase PdsA. In this study we examine the role and localization of PdsA during chemotaxis and streaming. We find that pdsA ؊ cells respond chemotactically to a narrower range of chemoattractant concentrations compared with wild-type (WT) cells. Moreover, unlike WT cells, pdsA ؊ cells do not form streams at low cell densities and form unusual thick and transient streams at high cell densities. We find that the intracellular pool of PdsA is localized to the endoplasmic reticulum, which may provide a compartment for storage and secretion of PdsA. Because we find that cAMP synthesis is normal in cells lacking PdsA, we conclude that signal degradation regulates the external cAMP gradient field generation and that the group migration behavior of these cells is compromised even though their signaling machinery is intact. INTRODUCTIONThe process by which cells sense an attractant molecule and respond by migrating directionally toward it is called chemotaxis. Chemotaxis is essential for a variety of physiological processes in mammals as well as for the survival of lower eukaryotes. The mechanisms that regulate the directed migration of neutrophils and Dictyostelium discoideum have been extensively studied previously (van Haastert and Devreotes, 2004;Bagorda et al., 2006;Friedl and Weigelin, 2008;Stephens et al., 2008). One particular challenge of these fast-moving cells is to maintain the ability to respond sensitively and rapidly to an attractant signal. Because both neutrophils and Dictyostelium cells use signal relay loops to propagate chemoattractant signals, mechanisms must be at play to maintain detectable levels of chemoattractants. Remarkably, signal degradation also seems to play an important role in the developmental processes of multicellular organisms. Migration of primordial germ cells in Drosophila and Zebrafish seems to require degradation of specific lysophospholipids in the former or chemokines in the latter to allow these cells to find their proper developmental environment (Renault and Lehmann, 2006;Minina et al., 2007). Many cell types use receptor-mediated degradation to maintain detectable levels of chemoattractants. In this context, cells internalize the bound receptor and as part of the receptor recycling pathway the ligand is released for degradation (Minina et al., 2007;Boldajipour et al., 2008;Borroni et al., 2008;Scola et al., 2008). Alternatively, extracellular enzymes can specifically degrade the extracellular signaling molecules, allowing the sensing machinery to go back to basal levels and retain high se...

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Section: Discussionmentioning

confidence: 99%

The Group Migration of Dictyostelium Cells Is Regulated by Extracellular Chemoattractant Degradation

Garcia

Rericha

Heger

et al. 2009

MBoC

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“…How the F-actin/PIP3 waves and these mechanical principles work together (39,40) and how they are guided by extracellular cues for directional movement (19,41) are an avenue of future work. The present study adds a revealing example to a repertoire of self-organizing spatiotemporal dynamics (42) underlying critical biological functions such as bacterial cell division (43), cell aggregation (27), and somitogenesis (44). Excitable dynamics are well studied in the Belouzov-Zhabotinsky reaction; however, how patterns are influenced by a finite boundary and its movement is largely unexplored (45,46).…”

Section: Phase-map Analysis Reveals Birth and Death Of Spatial Phasementioning

confidence: 99%

“…2D). At the center of a rotational wave, we identified a spatial phase singularity (26)(27)(28) that represents the core of a self-sustaining spiral wave ( Fig. 2A, Right).…”

Section: Phase-map Analysis Reveals Birth and Death Of Spatial Phasementioning

confidence: 99%

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

Taniguchi¹,

Ishihara

Oonuki³

et al. 2013

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

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In both randomly moving Dictyostelium and mammalian cells, phosphatidylinositol (3,4,5)-trisphosphate and F-actin are known to propagate as waves at the membrane and act to push out the protruding edge. To date, however, the relationship between the wave geometry and the patterns of amoeboid shape change remains elusive. Here, by using phase map analysis, we show that morphology dynamics of randomly moving Dictyostelium discoideum cells can be characterized by the number, topology, and position of spatial phase singularities, i.e., points that represent organizing centers of rotating waves. A single isolated singularity near the cellular edge induced a rotational protrusion, whereas a pair of singularities supported a symmetric extension. These singularities appeared by strong phase resetting due to de novo nucleation at the back of preexisting waves. Analysis of a theoretical model indicated excitability of the system that is governed by positive feedback from phosphatidylinositol (3,4,5)-trisphosphate to PI3-kinase activation, and we showed experimentally that this requires F-actin. Furthermore, by incorporating membrane deformation into the model, we demonstrated that geometries of competing waves explain most of the observed semiperiodic changes in amoeboid morphology.reaction-diffusion | oscillations | excitable media | self-organization | PTEN

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“…Within the last two years cellular automata (CA) have re-emerged in the focus of scientific attention, both with respect to fundamental work [1,2] and with respect to applications, e.g., to biology [3,4,5]. Such CA play an important role as minimal models of complex pattern formation.…”

mentioning

confidence: 99%

Similar impact of topological and dynamic noise on complex patterns

Marr¹,

Hütt²

2006

Physics Letters A

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Shortcuts in a regular architecture affect the information transport through the system due to the severe decrease in average path length. A fundamental new perspective in terms of pattern formation is the destabilizing effect of topological perturbations by processing distant uncorrelated information, similarly to stochastic noise. We study the functional coincidence of rewiring and noisy communication on patterns of binary cellular automata.

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An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations

Cited by 164 publications

References 27 publications

The Group Migration of Dictyostelium Cells Is Regulated by Extracellular Chemoattractant Degradation

The Group Migration of Dictyostelium Cells Is Regulated by Extracellular Chemoattractant Degradation

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

Similar impact of topological and dynamic noise on complex patterns

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