BMP signalling controls the construction of vertebrate mucociliary epithelia

Cibois, Marie; Luxardi, Guillaume; Chevalier, B.; Thomé, Virginie; Mercey, Olivier; Zaragosi, Laure‐Emmanuelle; Barbry, Pascal; Pasini, Andrea; Marcet, Brice; Kodjabachian, Laurent

doi:10.1242/dev.118679

Cited by 44 publications

(51 citation statements)

References 53 publications

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“…During differentiation, cells migrate from the mesenchyme outwards to the epidermis, and ultimately integrate into the mature epidermis, a single-layered epithelial sheet (Tu et al, 2015). This is in contrast to other established models used for studying the generation of epithelial cell type diversity (Cibois et al, 2015; Dubaissi and Papalopulu, 2011; Quigley et al, 2011), such as the Xenopus embryonic epidermis, in which epithelial progenitors migrate from an inner monolayer to an outer monolayer. In this case, progenitors can rely on physical cell-cell communication to determine cell fates (Cibois et al, 2015; Dubaissi and Papalopulu, 2011; Quigley et al, 2011).…”

Section: Introductionmentioning

confidence: 79%

“…This is in contrast to other established models used for studying the generation of epithelial cell type diversity (Cibois et al, 2015; Dubaissi and Papalopulu, 2011; Quigley et al, 2011), such as the Xenopus embryonic epidermis, in which epithelial progenitors migrate from an inner monolayer to an outer monolayer. In this case, progenitors can rely on physical cell-cell communication to determine cell fates (Cibois et al, 2015; Dubaissi and Papalopulu, 2011; Quigley et al, 2011). In planarians, mesenchymal progenitors are hypothesized to rely on secreted positional cues (Reddien, 2011), creating different challenges for the generation of cell-type diversity.…”

Section: Introductionmentioning

confidence: 79%

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Planarian Epidermal Stem Cells Respond to Positional Cues to Promote Cell-Type Diversity

2017

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Summary Successful regeneration requires that progenitors of different lineages form the appropriate missing cell types. However, simply generating lineages is not enough. Cells produced by a particular lineage often have distinct functions depending on their position within the organism. How this occurs in regeneration is largely unexplored. In planarian regeneration, new cells arise from a proliferative cell population (neoblasts). We used the planarian epidermal lineage to study how the location of adult progenitor cells results in their acquisition of distinct functional identities. Single-cell RNA sequencing of epidermal progenitors revealed the emergence of distinct spatial identities as early in the lineage as the epidermal neoblasts, with further pre-patterning occurring in their post-mitotic migratory progeny. Establishment of dorsal-ventral epidermal identities and functions, in response to BMP signaling, required neoblasts. Our work identified positional signals that activate regionalized transcriptional programs in the stem cell population and subsequently promote cell type diversity in the epidermis.

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Section: Introductionmentioning

confidence: 79%

Section: Introductionmentioning

confidence: 79%

Planarian Epidermal Stem Cells Respond to Positional Cues to Promote Cell-Type Diversity

2017

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“…FLDX was detected by incubation with alkaline phosphatase conjugated anti-fluorescein antibody (dilution 1/10,000; Roche). Sections were prepared and immune staining was performed as previously described (Cibois et al, 2015; Castillo-Briceno and Kodjabachian, 2014). Primary antibodies were as follows: anti-Myc (9E10; Santa Cruz Biotech, dilution 1/300 RRID:AB_627268), anti-GFP (GFP-1020; 2BScientific; dilution 1/1000 RRID:AB_10000240), anti-γ-Tubulin (ab16504; Abcam; dilution 1/1000 RRID:AB_443396), anti-phospho-MEK1 (9121; Cell Signaling Technology; dilution 1/400 RRID:AB_331648).…”

Section: Methodsmentioning

confidence: 99%

Lineage commitment of embryonic cells involves MEK1-dependent clearance of pluripotency regulator Ventx2

Scerbo

Marchal

Kodjabachian

2017

eLife

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During early embryogenesis, cells must exit pluripotency and commit to multiple lineages in all germ-layers. How this transition is operated in vivo is poorly understood. Here, we report that MEK1 and the Nanog-related transcription factor Ventx2 coordinate this transition. MEK1 was required to make Xenopus pluripotent cells competent to respond to all cell fate inducers tested. Importantly, MEK1 activity was necessary to clear the pluripotency protein Ventx2 at the onset of gastrulation. Thus, concomitant MEK1 and Ventx2 knockdown restored the competence of embryonic cells to differentiate. Strikingly, MEK1 appeared to control the asymmetric inheritance of Ventx2 protein following cell division. Consistently, when Ventx2 lacked a functional PEST-destruction motif, it was stabilized, displayed symmetric distribution during cell division and could efficiently maintain pluripotency gene expression over time. We suggest that asymmetric clearance of pluripotency regulators may represent an important mechanism to ensure the progressive assembly of primitive embryonic tissues.DOI: http://dx.doi.org/10.7554/eLife.21526.001

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“…Notch inhibition also drives MCC specification in mouse oviducts and brain ventricles (Kessler et al 2015;Kyrousi et al 2015). Recently, bone morphogenetic protein (BMP) signaling has been shown to interact with the Notch pathway to control mucociliary differentiation of vertebrate epithelia (Cibois et al 2015).…”

Section: Multiciliated Epithelia Across Animalsmentioning

confidence: 99%

Multiciliated Cells in Animals

Meunier¹,

Azimzadeh²

2016

Cold Spring Harb Perspect Biol

102

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Many animal cells assemble single cilia involved in motile and/or sensory functions. In contrast, multiciliated cells (MCCs) assemble up to 300 motile cilia that beat in a coordinate fashion to generate a directional fluid flow. In the human airways, the brain, and the oviduct, MCCs allow mucus clearance, cerebrospinal fluid circulation, and egg transportation, respectively. Impairment of MCC function leads to chronic respiratory infections and increased risks of hydrocephalus and female infertility. MCC differentiation during development or repair involves the activation of a regulatory cascade triggered by the inhibition of Notch activity in MCC progenitors. The downstream events include the simultaneous assembly of a large number of basal bodies (BBs)-from which cilia are nucleated-in the cytoplasm of the differentiating MCCs, their migration and docking at the plasma membrane associated to an important remodeling of the actin cytoskeleton, and the assembly and polarization of motile cilia. The direction of ciliary beating is coordinated both within cells and at the tissue level by a combination of planar polarity cues affecting BB position and hydrodynamic forces that are both generated and sensed by the cilia. Herein, we review the mechanisms controlling the specification and differentiation of MCCs and BB assembly and organization at the apical surface, as well as ciliary assembly and coordination in MCCs.

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BMP signalling controls the construction of vertebrate mucociliary epithelia

Cited by 44 publications

References 53 publications

Planarian Epidermal Stem Cells Respond to Positional Cues to Promote Cell-Type Diversity

Planarian Epidermal Stem Cells Respond to Positional Cues to Promote Cell-Type Diversity

Lineage commitment of embryonic cells involves MEK1-dependent clearance of pluripotency regulator Ventx2

Multiciliated Cells in Animals

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