Sox2 and Canonical Wnt Signaling Interact to Activate a Developmental Checkpoint Coordinating Morphogenesis with Mesoderm Fate Acquisition

Kinney, Brian A.; Anber, Arwa Al; Row, Richard H.; Tseng, Yung Zu; Weidmann, Maxwell D.; Knaut, Holger; Martin, Benjamin L.

doi:10.1016/j.celrep.2020.108311

Cited by 22 publications

(22 citation statements)

References 64 publications

(105 reference statements)

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“…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: 90%

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: Discussionmentioning

confidence: 90%

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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“…At the 21-somite stage, the tbxta and sox2 expression domains overlapped in the TB. The expression pattern of sox2 at the 21-somite stage resembled the pattern characteristic of 12-somite stage (Kinney et al, 2020;Okuda et al, 2006;Row et al, 2016), but was more restricted and shortened further at the subsequent stages. This can be at least partly explained by the differentiation of the neural progenitors (Graham et al, 2003).…”

Section: Discussionmentioning

confidence: 66%

“…Our data on the sox2 and tbxta expression from the 21‐somite to the prim‐6 stages confirm and expand the published data. The tbxta was expressed in the notochord and throughout the TB as described previously (Bisgrove et al, 2017; Esterberg et al, 2008; Kinney et al, 2020; Morrow et al, 2017; Zhao et al, 2005). Its expression domain in the TB became smaller along with the development.…”

Section: Discussionmentioning

confidence: 99%

“…NMPs have the dual potency to generate the spinal cord and paraxial mesoderm of the tail and trunk regions in vertebrates. These cells are defined by the co‐expression of sox2 and T ( Brachyury and ntl , tbxta and tbxtb , ta and tb in zebrafish; Javali et al, 2017; Aires et al, 2019; Kinney et al, 2020; Kawachi et al, 2020). Tbxta is a TB and notochord marker (Bisgrove et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…The sox2-expressing cells are held in the partial epithelial-tomesenchymal transition, which prevents their mesodermal differentiation. Sox2 is involved in maintaining the mesoderm-fated NMPs in an undifferentiated state within the TB through the transcriptional activation of tbxta (Kinney et al, 2020). Harrington et al (2010) defined three stages of the posterior NT formation in zebrafish.…”

Section: Introductionmentioning

confidence: 99%

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Neurulation in the posterior region of zebrafish, Danio rerio embryos

Gladysheva

Evnukova

Kondakova

et al. 2021

Journal of Morphology

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The neural tube of amniotes is formed through different mechanisms that take place in the anterior and posterior regions and involve neural plate folding or mesenchymal condensation followed by its cavitation. Meanwhile, in teleost trunk region, the neural plate forms the neural keel, while the lumen develops later. However, the data on neurulation and other morphogenetic processes in the posterior body region in Teleostei remain fragmentary. We proposed that there could be variations in the morphogenetic processes, such as cell shape changes and cell rearrangements, in the posterior region compared to the anterior one at the different stages. Here, we performed morphological and histochemical analyses of morphogenetic processes with an emphasis on neurulation in the zebrafish tail bud (TB) and posterior region. To analyze the posterior expression of sox2 and tbxta we performed whole mount in situ hybridization. We showed that the TB cells of variable shapes and orientation are tightly packed, and the neural and notochord primordia develop first. The shape of the neural primordium undergoes numerous changes as a result of cell rearrangements leading to the development of the neural rod. At the prim‐6 stage, the cells of the neural primordium directly form the neural rod. The neuroepithelial cells undergo sequential shape changes. At the stage of the neural rod formation, the apical regions of triangular neuroepithelial cells of the floor plate are enriched in F‐actin. The neurocoel development onset is above the apical poles of neuroepithelial cells. The expression domains of sox2 and tbxta become more restricted during the development.

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