The Scf/Kit pathway implements self-organized epithelial patterning

Chuyen, Alexandre; Rulquin, Charlotte; Daian, Fabrice; Thomé, Virginie; Clément, Raphaël; Kodjabachian, Laurent; Pasini, Andrea

doi:10.1016/j.devcel.2021.02.026

Cited by 12 publications

(13 citation statements)

References 68 publications

(95 reference statements)

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“…Impairing filopodia activity leads to radial intercalation defects as MCCs fail to anchor to the vertices. Therefore, we propose that filopodia provide the intercalating MCCs with a parallel guiding mechanism to the recently described Scf/kit biochemical signalling pathway 37 . While Scf/kit controls both the spacing between neighboring MCCs and their overall affinity to the overlying epithelium, filopodia precisely inform the MCCs on the position of the vertices.…”

Section: Discussionmentioning

confidence: 70%

Mechanics of cell integration in vivo

Ventura

Amiri

Thiagarajan

et al. 2021

Preprint

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During embryonic development, regeneration and homeostasis, cells have to physically integrate into their target tissues, where they ultimately execute their function. Despite a significant body of research on how mechanical forces instruct cellular behaviors within the plane of an epithelium, very little is known about the mechanical interplay at the interface between migrating cells and their surrounding tissue, which has its own dynamics, architecture and identity. Here, using quantitative in vivo imaging and molecular perturbations, together with a theoretical model, we reveal that multiciliated cell (MCC) precursors in the Xenopus embryo form dynamic filopodia that pull at the vertices of the overlying epithelial sheet to probe their stiffness and identify the preferred positions for their integration into the tissue. Moreover, we report a novel function for a structural component of vertices, the lipolysis-stimulated lipoprotein receptor (LSR), in filopodia dynamics and show its critical role in cell intercalation. Remarkably, we find that pulling forces equip the MCCs to remodel the epithelial junctions of the neighboring tissue, enabling them to generate a permissive environment for their integration. Our findings reveal the intricate physical crosstalk at the cell-tissue interface and uncover previously unknown functions for mechanical forces in orchestrating cell integration.

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Section: Discussionmentioning

confidence: 70%

Mechanics of cell integration in vivo

Ventura

Amiri

Thiagarajan

et al. 2021

Preprint

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“…Next, we generated a geometric model for the preference of MCCs to insert at each vertex type. Although MCCs are capable of some lateral motion ( Chuyen et al, 2021 ), the initial assumption of this model is that MCCs have a limited number of vertices in their neighborhood that are potential sites of insertion. We define that number as q.…”

Section: Resultsmentioning

confidence: 99%

“…Although these results clearly establish a critical role for MTs during intercalation, the functional mechanism of how MTs promote apical insertion remains poorly understood. Finally, the punctate pattern of MCC intercalation appears to be driven at least in part by S cf /Kit-based repulsion of early pre-insertion motile MCCs that helps establish regular spacing ( Chuyen et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Tubulin acetylation promotes penetrative capacity of cells undergoing radial intercalation

et al. 2021

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SUMMARY Post-translational modification of tubulin provides differential functions to microtubule networks. Here, we address the role of tubulin acetylation on the penetrative capacity of cells undergoing radial intercalation, which is the process by which cells move apically, insert between outer cells, and join an epithelium. There are opposing forces that regulate intercalation, namely, the restrictive forces of the epithelial barrier versus the penetrative forces of the intercalating cell. Positively and negatively modulating tubulin acetylation in intercalating cells alters the developmental timing such that cells with more acetylation penetrate faster. We find that intercalating cells preferentially penetrate higher-order vertices rather than the more prevalent tricellular vertices. Differential timing in the ability of cells to penetrate different vertices reveals that lower-order vertices represent more restrictive sites of insertion. We shift the accessibility of intercalating cells toward more restrictive junctions by increasing tubulin acetylation, and we provide a geometric-based mathematical model that describes our results.

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“…The formation of gaps in epithelial tissues also occurs during cell intercalation events, such as the extravasation of immune cells through the endothelial barrier (Escribano et al, 2019), or radial cell intercalation within the Xenopus embryo epidermis, in which multiciliated cells integrate into the superficial skin through the local loss of homotypic cell-cell junctions (Stubbs et al, 2006; Sedzinski et al, 2016; Chuyen et al, 2021; Collins et al, 2021). In the Xenopus epidermis, the multiciliated cells induce the pre-remodelling of the junctions in the superficial epithelial layer to promote the formation of high order junctions, which prime the epithelium for their further integration (Ventura et al, biorxiv).…”

Section: Discussionmentioning

confidence: 99%

Actomyosin contractility in olfactory placode neurons opens the skin epithelium to form the nostril

Baraban

Bonnet

et al. 2022

Preprint

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Despite their barrier function, epithelial layers can locally lose their integrity to create physiological openings during morphogenesis. The cellular and molecular mechanisms driving the formation of these epithelial breaks are only starting to be investigated. Here, we studied the formation of the zebrafish nostril (the olfactory orifice), which opens in the skin epithelium to expose the olfactory neurons to external odorant cues. Combining live imaging, drug treatments, laser ablation and tissue-specific functional perturbations, we demonstrate that the formation of the orifice is driven by a mechanical interplay between the olfactory placode neurons and the skin: the neurons pull on the overlying skin cells in an actomyosin-dependent manner, thus triggering the opening of the orifice. This work unravels an original mechanism to break an epithelial sheet, in which an adjacent group of cells instructs and mechanically assists the epithelium to induce its local rupture.

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The Scf/Kit pathway implements self-organized epithelial patterning

Cited by 12 publications

References 68 publications

Mechanics of cell integration in vivo

Mechanics of cell integration in vivo

Tubulin acetylation promotes penetrative capacity of cells undergoing radial intercalation

Actomyosin contractility in olfactory placode neurons opens the skin epithelium to form the nostril

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