Geometric constraints alter cell arrangements within curved epithelial tissues

Rupprecht, Jean-François; Ong, Kok Haur; Yin, Jianguo; Huang, Anqi; Dinh, Huy-Hong-Quan; Singh, Annette; Zhang, Shaobo; Yu, Weimiao; Saunders, Timothy E.

doi:10.1091/mbc.e17-01-0060

Cited by 44 publications

(56 citation statements)

References 66 publications

(76 reference statements)

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“…However, there is evidence that epithelial cells are able to contact different neighbouring cells at different depths along the apico-basal axis of the cell (contrary to the prism/frustum paradigm). The appearance of these intercalations along the apical-basal axis has been observed in the columnar epithelium of Drosophila imaginal discs 39 or during Drosophila germ-band extension 40 , 41 and has been also modelled computationally in the context of a planar tissue 42 .…”

Section: Introductionmentioning

confidence: 99%

Scutoids are a geometrical solution to three-dimensional packing of epithelia

et al. 2018

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As animals develop, tissue bending contributes to shape the organs into complex three-dimensional structures. However, the architecture and packing of curved epithelia remains largely unknown. Here we show by means of mathematical modelling that cells in bent epithelia can undergo intercalations along the apico-basal axis. This phenomenon forces cells to have different neighbours in their basal and apical surfaces. As a consequence, epithelial cells adopt a novel shape that we term “scutoid”. The detailed analysis of diverse tissues confirms that generation of apico-basal intercalations between cells is a common feature during morphogenesis. Using biophysical arguments, we propose that scutoids make possible the minimization of the tissue energy and stabilize three-dimensional packing. Hence, we conclude that scutoids are one of nature's solutions to achieve epithelial bending. Our findings pave the way to understand the three-dimensional organization of epithelial organs.

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Section: Introductionmentioning

confidence: 99%

Scutoids are a geometrical solution to three-dimensional packing of epithelia

et al. 2018

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“…Consistent with the key role of cortical F-actin density in mechanically regulating convergence and extension (Shawky et al, 2018), we observed increased intensity of actin during the convergence of adaxial cells at the PSM. We have previously identified apical-to-basal neighbor exchanges in the highly curved anterior of the early Drosophila embryo (Rupprecht et al, 2017). Such apicalto-basal neighbor exchanges release high tension due to dense cell packing in regions of high curvature.…”

Section: Discussionmentioning

confidence: 96%

Shh induces symmetry breaking in the presomitic mesoderm by inducing tissue shear and orientated cell rearrangements

Yin

Saunders

2019

Preprint

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Future boundaries of skeletal muscle segments are determined in the presomitic mesoderm (PSM). Within the PSM, future somitic cells undergo significant changes in both morphology and position. How such large-scale cellular changes are coordinated and the effect on the future border formation is unknown. We find that cellular rearrangements differ between cell populations within the PSM. In contrast to lateral somitic cells, which display less organized rearrangement, the adaxial cell layer undergoes significant tissue shearing with dorsal and ventral cells sliding posteriorly.This shear is generated by orientated intercalations of dorsally and ventrally located adaxial cells, which induces a chevron-like pattern. We find Shh signaling is required for the tissue shear and morphogenesis of adaxial cells. In particular, we observe Shhdependent polarized recruitment of non-muscle myosin IIA drives apical constrictions, and thus the intercalations and shear. This reveals a novel role for Shh in regulating cell mechanics in the PSM.

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“…Quantitative image analysis revealed the presence of scutoidshaped cells within the curved epithelia of the Drosophila salivary gland, egg chamber, and developing embryo, all of which showed evidence of apical-basal transitions. Cells with different neighbors at their apical and basal domains had been observed previously in the Drosophila leg imaginal disc [15] and the anterior pole of the embryo [16], although it is unclear whether these cells were scutoid-shaped. Future studies of epithelial tissues in other organisms will likely reveal the presence of scutoids across species.…”

Section: Current Biologymentioning

confidence: 94%

Epithelial Packing: Even the Best of Friends Must Part

Nelson

2018

Current Biology

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Geometric constraints alter cell arrangements within curved epithelial tissues

Cited by 44 publications

References 66 publications

Scutoids are a geometrical solution to three-dimensional packing of epithelia

Scutoids are a geometrical solution to three-dimensional packing of epithelia

Shh induces symmetry breaking in the presomitic mesoderm by inducing tissue shear and orientated cell rearrangements

Epithelial Packing: Even the Best of Friends Must Part

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