Cell intercalation driven by SMAD3 underlies secondary neural tube formation

Gonzalez-Gobartt, Elena; Blanco-Ameijeiras, José; Usieto, Susana; Allio, Guillaume; Bénazéraf, Bertrand; Martı́, Elisa

doi:10.1101/2020.08.24.261008

Cited by 4 publications

(4 citation statements)

References 71 publications

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“…The first heterogeneity that we have observed is patterned spatially in a gradient along the antero-posteriorly axis (Sox2 high anteriorly, Bra high posteriorly) in the dorsal part of the region. This graded expression has been described in chicken embryo (22)(49) and is coherent with fate maps studies at earlier stages showing that the antero-posterior axis of the epiblast/streak gives rise to progeny along the medio-lateral axis (4,6). For instance, anterior cells expressing high levels of Sox2 can give rise to neural cells and more posterior cells expressing high levels of Bra to PSM (and eventually to lateral mesoderm to cells located even more caudally).…”

Section: Discussionsupporting

confidence: 84%

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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Section: Discussionsupporting

confidence: 84%

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 a role for Sox2 in the control of progenitor cell migration has, to our knowledge, not previously been reported, recent works have demonstrated that a rise of Sox2 expression promotes the transition of posterior progenitors to NT during chick embryo secondary neurulation ( Kawachi et al, 2020 ) and that turning off Sox2 is necessary for NMP to enter the mesoderm in zebrafish embryo ( Kinney et al, 2020 ). In addition, it has also been observed by time-lapse analysis that the dorsal zone between the PZ and the NT does not display excessive cell migration but rather local cell intercalations ( Roszko et al, 2007 ; Gonzalez-Gobartt et al, 2021a ). Taken together, these data confirm the hypothesis that Sox2 High cells could be laid down as the PZ moves posteriorly.…”

Section: Discussionmentioning

confidence: 94%

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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“…Recent studies show that SMAD3 drives cell intercalation underlies secondary neural tube formation in the mouse embryo (Gonzalez-Gobartt et al, 2021). Moreover, it was known that the BMP-Rho-ROCK1 pathway targets MLC to control actin remodeling in fibroblasts (Konstantinidis et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Admp regulates tail bending by controlling ventral epidermal cell polarity via phosphorylated myosin localization

Kogure

Muraoka

Koizumi

et al. 2021

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Chordate tailbud embryos have similar morphological features, including a bending tail. A recent study revealed that the actomyosin of the notochord changes the contractility and drive tail bending of the early Ciona tailbud embryo. Yet, the upstream regulator of tail bending remains unknown. In this study, we find that Admp regulates tail bending of Ciona mid-tailbud embryos. Anti-pSmad antibody signal was detected at the ventral midline tail epidermis. Admp knock-down embryo completely inhibited the ventral tail bending and reduced the number of the triangular-shaped cells, which has the apical accumulation of the myosin phosphorylation and inhibited specifically the cell-cell intercalation of the ventral epidermis. The degree of myosin phosphorylation of the ventral cells and tail bending were correlated. Finally, the laser cutter experiments demonstrated the myosin-phosphorylation-dependent tension of the ventral midline epidermis during tail bending. We conclude that Admp is an upstream regulator of the tail bending by controlling myosin phosphorylation and its localization of ventral epidermal cells. These data reveal a new aspect of the function of the Admp that might be evolutionarily conserved in bilaterian animals.

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Cell intercalation driven by SMAD3 underlies secondary neural tube formation

Cited by 4 publications

References 71 publications

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

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

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

Admp regulates tail bending by controlling ventral epidermal cell polarity via phosphorylated myosin localization

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