A random cell motility gradient downstream of FGF controls elongation of an amniote embryo

Bénazéraf, Bertrand; François, Paul; Baker, Ruth E.; Denans, Nicolas; Little, Charles D.; Pourquié, Olivier

doi:10.1038/nature09151

Cited by 308 publications

(419 citation statements)

References 28 publications

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“…This result is of particular interest as the two mechanisms enhancing synchrony in the simulations represent two completely different biological mechanisms: the coupling strength A represents the effect of biochemical cell-cell signalling while the parameter p represents a mechanical interaction. In zebrafish cell-cell coupling is strongly dependent on the NotchDelta signalling pathway while in chick it has been shown that cell motility is strongly influenced by an Fgf gradient along the AP axis [6]. Fig.…”

Section: Resultsmentioning

confidence: 97%

“…Bénazéraf et al [6] have recently quantified random cell motion in the mouse PSM while, in a theoretical study, Uriu et al [7] have demonstrated that random cell movement enhances synchronisation of neighbouring molecular oscillators. We now investigate the effects of random cell movement on the mitosis-perturbed phase dynamics introduced in Sect.…”

Section: Investigating the Perturbation To Oscillator Synchronisationmentioning

confidence: 99%

“…Cell movement in the mouse PSM has recently been quantified: there is a posteriorly increasing motility gradient along the anterior-posterior (AP) axis [6]. This random cell motion results in cells changing their neighbours, at least in the posterior tip of the PSM which, in turn, could influence the synchronisation of neighbouring cells.…”

Section: Introductionmentioning

confidence: 99%

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Modelling Oscillator Synchronisation During Vertebrate Axis Segmentation

Murray

Maini

Baker

2012

Springer Proceedings in Mathematics

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The somitogenesis clock regulates the periodicity with which somites form in the posterior pre-somitic mesoderm. Whilst cell heterogeneity results in noisy oscillation rates amongst constituent cells, synchrony within the population is maintained as oscillators are entrained via juxtracine signalling mechanisms. Here we consider a population of phase-coupled oscillators and investigate how biologically motivated perturbations to the entrained state can perturb synchrony within the population. We find that the ratio of mitosis length to clock period can influence levels of desynchronisation. Moreover, we observe that random cell movement, and hence change of local neighbourhoods, increases synchronisation.

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Section: Resultsmentioning

confidence: 97%

Section: Investigating the Perturbation To Oscillator Synchronisationmentioning

confidence: 99%

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Modelling Oscillator Synchronisation During Vertebrate Axis Segmentation

Murray

Maini

Baker

2012

Springer Proceedings in Mathematics

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“…Hensen's node tissue, along the embryonic midline, is a cellenriched region of the early avian embryo, [20][21][22] and comprises the source tissue of all midline cells in the avian embryo. 23 Due to the cell-dominant composition of the nodal tissue, we assessed the motility characteristics of the cells within elongating nodal explants.…”

Section: Avian Embryonic Explants Continue Characteristic Morphogenetmentioning

confidence: 99%

Identification of emergent motion compartments in the amniote embryo

Loganathan¹,

Little²,

Joshi³

et al. 2014

Organogenesis

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The tissue scale deformations (1mm) required to form an amniote embryo are poorly understood. Here, we studied »400 mm-sized explant units from gastrulating quail embryos. The explants deformed in a reproducible manner when grown using a novel vitelline membrane-based culture method. Time-lapse recordings of latent embryonic motion patterns were analyzed after disk-shaped tissue explants were excised from three specific regions near the primitive streak: 1) anterolateral epiblast, 2) posterolateral epiblast, and 3) the avian organizer (Hensen's node). The explants were cultured for 8 hours-an interval equivalent to gastrulation. Both the anterolateral and the posterolateral epiblastic explants engaged in concentric radial/centrifugal tissue expansion. In sharp contrast, Hensen's node explants displayed Cartesian-like, elongated, bipolar deformations-a pattern reminiscent of axis elongation. Time-lapse analysis of explant tissue motion patterns indicated that both cellular motility and extracellular matrix fiber (tissue) remodeling take place during the observed morphogenetic deformations. As expected, treatment of tissue explants with a selective Rho-Kinase (p160ROCK) signaling inhibitor, Y27632, completely arrested all morphogenetic movements. Microsurgical experiments revealed that lateral epiblastic tissue was dispensable for the generation of an elongated midline axisprovided that an intact organizer (node) is present. Our computational analyses suggest the possibility of delineating tissue-scale morphogenetic movements at anatomically discrete locations in the embryo. Further, tissue deformation patterns, as well as the mechanical state of the tissue, require normal actomyosin function. We conclude that amniote embryos contain tissue-scale, regionalized morphogenetic motion generators, which can be assessed using our novel computational time-lapse imaging approach. These data and future studies-using explants excised from overlapping anatomical positions-will contribute to understanding the emergent tissue flow that shapes the amniote embryo.

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“…In vertebrates, where segments are produced from mesenchymal cells in the presomitic mesoderm, both segmentation and axial elongation are affected by the roles of an FGF8 gradient as a segmentation wavefront and a mediator of cell motility in the presomitic mesoderm 17 . Elongation and its connection to segmentation are less well-characterized in arthropods, whose segments are initially generated within the embryonic epithelium.…”

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confidence: 99%

Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

Nakamoto

Hester²,

Constantinou

et al. 2015

Nat Commun

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Segmented animals are found in major clades as phylogenetically distant as vertebrates and arthropods. Typically, segments form sequentially in what has been thought to be a regular process, relying on a segmentation clock to pattern budding segments and posterior mitosis to generate axial elongation. Here we show that segmentation in Tribolium has phases of variable periodicity during which segments are added at different rates. Furthermore, elongation during a period of rapid posterior segment addition is driven by high rates of cell rearrangement, demonstrated by differential fates of marked anterior and posterior blastoderm cells. A computational model of this period successfully reproduces elongation through cell rearrangement in the absence of cell division. Unlike current models of steady-state sequential segmentation and elongation from a proliferative growth zone, our results indicate that cell behaviours are dynamic and variable, corresponding to differences in segmentation rate and giving rise to morphologically distinct regions of the embryo.

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A random cell motility gradient downstream of FGF controls elongation of an amniote embryo

Cited by 308 publications

References 28 publications

Modelling Oscillator Synchronisation During Vertebrate Axis Segmentation

Modelling Oscillator Synchronisation During Vertebrate Axis Segmentation

Identification of emergent motion compartments in the amniote embryo

Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

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