Motility-gradient induced elongation of the vertebrate embryo

Regev, Ido; Guevorkian, Karine; Pourquié, Olivier; Mahadevan, L.

doi:10.1101/187443

Cited by 6 publications

(7 citation statements)

References 25 publications

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“…Interestingly, the posterior global movement of the PZ region seems constant all along those different stages. Several works, performed in bird embryo, have indicated that physical constraints exerted by neighboring tissues, in particular the PSM, promote the posterior movement of the PZ ( Bénazéraf et al, 2017 ; Bénazéraf et al, 2010 ; Xiong et al, 2020 ; Regev et al, 2017 ). It is therefore likely that the posterior movement of PZ cells is the result of both local re-arrangements and external forces acting on the whole region.…”

Section: Discussionmentioning

confidence: 99%

Cell-to-cell heterogeneity in Sox2 and Bra expression guides progenitor motility and destiny

Romanos

Allio

Roussigné

et al. 2021

eLife

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Although cell-to-cell heterogeneity in gene and protein expression within cell populations has been widely documented, we know little about its biological functions. By studying progenitors of the posterior region of bird embryos, we found that expression levels of transcription factors Sox2 and Bra, respectively involved in neural tube (NT) and mesoderm specification, display a high degree of cell-to-cell heterogeneity. By combining forced expression and downregulation approaches with time-lapse imaging, we demonstrate that Sox2-to-Bra ratio guides progenitor’s motility and their ability to stay in or exit the progenitor zone to integrate neural or mesodermal tissues. Indeed, high Bra levels confer high motility that pushes cells to join the paraxial mesoderm, while high levels of Sox2 tend to inhibit cell movement forcing cells to integrate the NT. Mathematical modeling captures the importance of cell motility regulation in this process and further suggests that randomness in Sox2/Bra cell-to-cell distribution favors cell rearrangements and tissue shape conservation.

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Section: Discussionmentioning

confidence: 99%

Cell-to-cell heterogeneity in Sox2 and Bra expression guides progenitor motility and destiny

Romanos

Allio

Roussigné

et al. 2021

eLife

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show abstract

“…Interestingly, the posterior global movement of the PZ region seems constant all along those different stages. Several works, realized in bird embryo, have indicated that physical constrains exerted by neighboring tissues, in particular the PSM, promote the posterior movement of the PZ (24,25,39,40). It is therefore likely that the posterior movement of PZ cells is the result of both local re-arrangements and external forces acting on the whole region.…”

Section: Discussionmentioning

confidence: 99%

Cell-to-cell heterogeneity in Sox2 and Brachyury expression ratios guides progenitor destiny by controlling their motility.

Romanos

Allio

Combres

et al. 2020

Preprint

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Although cell-to-cell heterogeneity in gene and protein expression has been widely documented within a given cell population, little is known about its potential biological functions. We addressed this issue by studying posterior progenitors, an embryonic cell population that is central to vertebrate posterior axis formation. These progenitors are able to maintain themselves within the posterior region of the embryo or to exit this region to participate in the formation of neural tube or paraxial mesoderm tissues. Posterior progenitors are known to co-express transcription factors related to neural and mesodermal lineages, e.g. Sox2 and Brachyury (Bra), respectively. In this study, we find that expression levels of Sox2 and Bra proteins display a high degree of variability among posterior progenitors of the quail embryo, therefore highlighting spatial heterogeneity of this cell population. By over-expression/down-regulation experiments and time-lapse imaging, we show that Sox2 and Bra are both involved in controlling progenitor motility, acting however in an opposite way: while Bra is necessary to progenitor motion, Sox2 tends to inhibit cell movement. Combining mathematical modeling and experimental approaches, we provide evidence that the spatial heterogeneity of posterior progenitors, with regards to their expression levels of Sox2 and Bra and thus to their motile properties, is fundamental to maintain a pool of resident progenitors while others segregate to contribute to tissue formation. As a whole, our work reveals that heterogeneity among a population of progenitor cells is critical to ensure robust multi-tissue morphogenesis.

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“…The average speed of this movement thus serves as an indicator of PSM cell addition rate (Figure 1E). To assess the motility of these cells (Figures S1E), we fit the cell tracks with a diffusion model to separate the directional and non-directional components (Regev et al, 2017). This allows us to assess the local motility or "cell diffusivity" in the PSM.…”

Section: Cellular Dynamics Of Axial and Paraxial Elongationmentioning

confidence: 99%

“…Recent studies have revealed the key role of the posterior PSM in the generation of elongation forces during the posterior body formation in amniotes (Bénazéraf et al, 2010;Regev et al, 2017). The physical mechanism linking the movements of PSM cells and the tissue-level expansion remains to be clarified.…”

Section: Force Generation By Cell Dynamics In the Posterior Psmmentioning

confidence: 99%

Mechanical Coupling Coordinates the Co-elongation of Axial and Paraxial Tissues in Avian Embryos

Xiong

Bénazéraf

et al. 2020

Developmental Cell

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Tissues undergoing morphogenesis impose mechanical effects on one another. How developmental programs adapt to or take advantage of these effects remains poorly explored.Here, using a combination of live imaging, modeling, and microsurgical perturbations, we show that the axial and paraxial tissues in the forming avian embryonic body coordinate their rates of elongation through mechanical interactions. First, a cell motility gradient drives paraxial presomitic mesoderm (PSM) expansion, resulting in compression of the axial neural tube and notochord; second, elongation of axial tissues driven by PSM compression and polarized cell intercalation pushes the caudal progenitor domain posteriorly; finally, the axial push drives progenitors to emigrate into the PSM to maintain tissue growth and cell motility. These interactions form an engine-like positive feedback loop, which ensures the tissue-coupling and self-sustaining characteristics of body elongation. Our results suggest a general role of intertissue forces in the coordination of complex morphogenesis involving distinct tissues..

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Motility-gradient induced elongation of the vertebrate embryo

Cited by 6 publications

References 25 publications

Cell-to-cell heterogeneity in Sox2 and Bra expression guides progenitor motility and destiny

Cell-to-cell heterogeneity in Sox2 and Bra expression guides progenitor motility and destiny

Cell-to-cell heterogeneity in Sox2 and Brachyury expression ratios guides progenitor destiny by controlling their motility.

Mechanical Coupling Coordinates the Co-elongation of Axial and Paraxial Tissues in Avian Embryos

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