Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns

Tsiairis, Charisios D.; Aulehla, Alexander

doi:10.1016/j.cell.2016.01.028

Cited by 135 publications

(172 citation statements)

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“…This result suggests that even the anti-phase state between neighboring cells would become in-phase within two or three cycles. In the systems such as the PSM, both senders and receivers are in the same cells, and therefore synchronization could occur even more rapidly in such systems than when senders and receivers are in different cells, which explains well the result of the PSM cell aggregation study (Tsiairis and Aulehla 2016). Thus, our new method described here successfully elucidates the underlying mechanism of Notch signaling-mediated robust and rapid synchronization.…”

Section: A Versatile Platform To Characterize Cell-to-cell Transfer Osupporting

confidence: 53%

“…It was shown that when dissociated PSM cells with mixtures of various phases of oscillations were aggregated, they resumed robust and synchronized oscillations within 5-6 h, which is equivalent to two or three cycles, suggesting that synchronization occurs very rapidly (Tsiairis and Aulehla 2016). We successfully measured the phase response curve and phase transition curve for the relationship between Notch signaling inputs and phase shift of Hes1 oscillation in receiving cells.…”

Section: A Versatile Platform To Characterize Cell-to-cell Transfer Omentioning

confidence: 90%

“…However, when PSM cells were dissociated, both Hes1 and Hes7 oscillations became unstable and noisy, suggesting that cell-to-cell communication plays a role in robust and synchronized oscillations (Maroto et al 2005;Masamizu et al 2006). Indeed, when these dissociated PSM cells were aggregated, they resumed robust and synchronized oscillations within 5-6 h even though they were derived from several embryos (Tsiairis and Aulehla 2016). The exact mechanism for such robust synchronization remains to be determined, but previous analyses using genetic perturbations or inhibitor application revealed that the Notch signaling pathway is required for synchronized oscillation (Jiang et al 2000;Horikawa et al 2006;Riedel-Kruse et al 2007;Delaune et al 2012;Shimojo et al 2016;Tsiairis and Aulehla 2016).…”

mentioning

confidence: 99%

“…Indeed, when these dissociated PSM cells were aggregated, they resumed robust and synchronized oscillations within 5-6 h even though they were derived from several embryos (Tsiairis and Aulehla 2016). The exact mechanism for such robust synchronization remains to be determined, but previous analyses using genetic perturbations or inhibitor application revealed that the Notch signaling pathway is required for synchronized oscillation (Jiang et al 2000;Horikawa et al 2006;Riedel-Kruse et al 2007;Delaune et al 2012;Shimojo et al 2016;Tsiairis and Aulehla 2016). However, it is not known whether and how single-cell genetic oscillators transmit and decode dynamic information through Notch signaling and whether Dll1 oscillation is sufficient to convey such information from cell to cell for synchronization.…”

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confidence: 99%

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Optogenetic perturbation and bioluminescence imaging to analyze cell-to-cell transfer of oscillatory information

et al. 2017

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Cells communicate with each other to coordinate their gene activities at the population level through signaling pathways. It has been shown that many gene activities are oscillatory and that the frequency and phase of oscillatory gene expression encode various types of information. However, whether or how such oscillatory information is transmitted from cell to cell remains unknown. Here, we developed an integrated approach that combines optogenetic perturbations and single-cell bioluminescence imaging to visualize and reconstitute synchronized oscillatory gene expression in signal-sending and signal-receiving processes. We found that intracellular and intercellular periodic inputs of Notch signaling entrain intrinsic oscillations by frequency tuning and phase shifting at the singlecell level. In this way, the oscillation dynamics are transmitted through Notch signaling, thereby synchronizing the population of oscillators. Thus, this approach enabled us to control and monitor dynamic cell-to-cell transfer of oscillatory information to coordinate gene expression patterns at the population level.

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Section: A Versatile Platform To Characterize Cell-to-cell Transfer Osupporting

confidence: 53%

Section: A Versatile Platform To Characterize Cell-to-cell Transfer Omentioning

confidence: 90%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Optogenetic perturbation and bioluminescence imaging to analyze cell-to-cell transfer of oscillatory information

et al. 2017

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“…In higher organisms, morphogen fields are dynamic and their temporal changes appear to be read out to regulate cell fates (10,55). Traveling waves are also prevalent in embryonic development (56,57). It would be interesting to explore whether the same mathematical principle applies in these and other systems.…”

Section: Discussionmentioning

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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Under Diffusion Control: from Structuring Matter to Directional Motion

Cera

Schalley

2018

Advanced Materials

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Self-organization in synthetic chemical systems is quickly developing into a powerful strategy for designing new functional materials. As self-organization requires the system to exist far from thermodynamic equilibrium, chemists have begun to go beyond the classical equilibrium self-assembly that is often applied in bottom-up supramolecular synthesis, and to learn about the surprising and unpredicted emergent properties of chemical systems that are characterized by a higher level of complexity and extended reactivity networks. The present review focuses on self-organization in reaction-diffusion systems. Selected examples show how the emergence of complex morphogenesis is feasible in synthetic systems leading to hierarchically and nanostructured matter. Starting from well-investigated oscillating reactions, recent developments extend diffusion-limited reactivity to supramolecular systems. The concept of dynamic instability is introduced and illustrated as an additional tool for the design of smart materials and actuators, with emphasis on the realization of motion even at the macroscopic scale. The formation of spatio-temporal patterns along diffusive chemical gradients is exploited as the main channel to realize symmetry breaking and therefore anisotropic and directional mechanical transformations. Finally, the interaction between external perturbations and chemical gradients is explored to give mechanistic insights in the design of materials responsive to external stimuli.

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Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns

Cited by 135 publications

References 44 publications

Optogenetic perturbation and bioluminescence imaging to analyze cell-to-cell transfer of oscillatory information

Optogenetic perturbation and bioluminescence imaging to analyze cell-to-cell transfer of oscillatory information

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

Under Diffusion Control: from Structuring Matter to Directional Motion

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