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Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns

Overview
Journal Cell
Publisher Cell Press
Specialty Cell Biology
Date 2016 Feb 13
PMID 26871631
Citations 57
Authors
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Abstract

In vertebrate embryos, somites, the precursor of vertebrae, form from the presomitic mesoderm (PSM), which is composed of cells displaying signaling oscillations. Cellular oscillatory activity leads to periodic wave patterns in the PSM. Here, we address the origin of such complex wave patterns. We employed an in vitro randomization and real-time imaging strategy to probe for the ability of cells to generate order from disorder. We found that, after randomization, PSM cells self-organized into several miniature emergent PSM structures (ePSM). Our results show an ordered macroscopic spatial arrangement of ePSM with evidence of an intrinsic length scale. Furthermore, cells actively synchronize oscillations in a Notch-signaling-dependent manner, re-establishing wave-like patterns of gene activity. We demonstrate that PSM cells self-organize by tuning oscillation dynamics in response to surrounding cells, leading to collective synchronization with an average frequency. These findings reveal emergent properties within an ensemble of coupled genetic oscillators.

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References
1.
Foty R, Steinberg M . The differential adhesion hypothesis: a direct evaluation. Dev Biol. 2005; 278(1):255-63. DOI: 10.1016/j.ydbio.2004.11.012. View

2.
Maroto M, Dale J, Dequeant M, Petit A, Pourquie O . Synchronised cycling gene oscillations in presomitic mesoderm cells require cell-cell contact. Int J Dev Biol. 2005; 49(2-3):309-15. DOI: 10.1387/ijdb.041958mm. View

3.
Zaikin A, Zhabotinsky A . Concentration wave propagation in two-dimensional liquid-phase self-oscillating system. Nature. 1970; 225(5232):535-7. DOI: 10.1038/225535b0. View

4.
Ball P . Forging patterns and making waves from biology to geology: a commentary on Turing (1952) 'The chemical basis of morphogenesis'. Philos Trans R Soc Lond B Biol Sci. 2015; 370(1666). PMC: 4360114. DOI: 10.1098/rstb.2014.0218. View

5.
Oates A, Morelli L, Ares S . Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development. 2012; 139(4):625-39. DOI: 10.1242/dev.063735. View