Neural-fated self-renewing cells regulated by Sox2 during secondary neurulation in chicken tail bud

Kawachi, Teruaki; Shimokita, Eisuke; Kudo, Ryo; Tadokoro, Ryosuke; Takahashi, Yoshiko

doi:10.1016/j.ydbio.2020.02.007

Cited by 20 publications

(34 citation statements)

References 44 publications

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“…Thus, while these fate maps indicate that cells of the anterior PS epiblast initially produce descendants either in the neural tube or in the mesoderm, our results indicate that NMPs give rise to both neural tube and mesoderm only later, in more posterior regions of the body. These observations are consistent with recent grafts of the epiblast territory in 6-somite chicken embryos showing that the territory first produces neural and then both mesodermal and neural derivatives (Kawachi et al, 2020). Bipotential cells with a neural and mesodermal fate have so far only been reported in zebrafish where they segregate during gastrulation and contribute to the most posterior part of the axis (Attardi et al, 2018).…”

Section: Discussionsupporting

confidence: 90%

Dynamics of primitive streak regression controls the fate of neuro-mesodermal progenitors in the chicken embryo

Guillot

Michaut

Rabe

et al. 2020

Preprint

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In classical descriptions of vertebrate development, the segregation of the three embryonic germ layers is completed by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage committed progenitors during regression of the Primitive Streak (PS) and tail bud (Pasteels, 1937b; Stern, 2004). Identification of Neuro-Mesodermal Progenitors (NMPs) contributing to both musculo-skeletal precursors (paraxial mesoderm) and spinal cord during axis formation by retrospective clonal analysis challenged these notions (Henrique et al., 2015; Tzouanacou et al., 2009). However, in amniotes such as mouse and chicken, the precise identity and localization of these cells has remained unclear despite a wealth of fate mapping analyses of the PS region. Here, we use lineage tracing in the chicken embryo to show that single cells located in the SOX2/T positive anterior PS region contribute to both neural and mesodermal lineages in the trunk and tail, but only express this bipotential fate with some delay. We demonstrate that posterior to anterior gradients of convergence speed and ingression along the PS gradually lead to exhaustion of all mesodermal precursor territories except for NMPs where limited ingression and increased proliferation maintain and amplify this pool of axial progenitors. As a result, most of the remaining mesodermal precursors from the PS in the tail bud are bipotential NMPs. Together, our results provide a novel understanding of the contribution of the PS and tail bud to the formation of the body of amniote embryos.

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Section: Discussionsupporting

confidence: 90%

Dynamics of primitive streak regression controls the fate of neuro-mesodermal progenitors in the chicken embryo

Guillot

Michaut

Rabe

et al. 2020

Preprint

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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: 85%

“…In particular, mouse cells that have a mutation in the Brachyury gene have lower migration speed than wild-type cells when isolated and cultured, explaining part of the mouse embryonic axis truncation phenotype (34). 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 (35) and that turning off Sox2 is necessary for NMP to enter the mesoderm in zebrafish embryo (36). In addition, it has also been observed by time-lapse analysis that the zone between the PZ and the NT does not display excessive migration or neighbor exchanges (37).…”

Section: Discussionmentioning

confidence: 88%

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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“…These caudal elongations differ from the early phase with respect to the underlying mechanisms that rely less on the convergence extension and ingression of NECs. This second phase of morphogenesis is often defined as secondary neurulation, which includes aggregation, cavitation, and caudal-to-rostral migration of NMP-derived neural progenitors (NPCs) ( Kawachi et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Anteroposterior Wnt-RA Gradient Defines Adhesion and Migration Properties of Neural Progenitors in Developing Spinal Cord

et al. 2020

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Summary Mammalian embryos exhibit a transition from head morphogenesis to trunk elongation to meet the demand of axial elongation. The caudal neural tube (NT) is formed with neural progenitors (NPCs) derived from neuromesodermal progenitors localized at the tail tip. However, the molecular and cellular basis of elongating NT morphogenesis is yet elusive. Here, we provide evidence that caudal NPCs exhibit strong adhesion affinity that is gradually decreased along the anteroposterior (AP) axis in mouse embryonic spinal cord and human cellular models. Strong cell-cell adhesion causes collective migration, allowing AP alignment of NPCs depending on their birthdate. We further validated that this axial adhesion gradient is associated with the extracellular matrix and is under the control of graded Wnt signaling emanating from tail buds and antagonistic retinoic acid (RA) signaling. These results suggest that progressive reduction of NPC adhesion along the AP axis is under the control of Wnt-RA molecular networks, which is essential for a proper elongation of the spinal cord.

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Neural-fated self-renewing cells regulated by Sox2 during secondary neurulation in chicken tail bud

Cited by 20 publications

References 44 publications

Dynamics of primitive streak regression controls the fate of neuro-mesodermal progenitors in the chicken embryo

Dynamics of primitive streak regression controls the fate of neuro-mesodermal progenitors in the chicken embryo

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

Anteroposterior Wnt-RA Gradient Defines Adhesion and Migration Properties of Neural Progenitors in Developing Spinal Cord

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