Patterned cortical tension mediated by N-cadherin controls cell geometric order in the Drosophila eye

Chan, Eunice HoYee; Shivakumar, Pruthvi Chavadimane; Clément, Raphaël; Laugier, Edith; Lenne, Pierre-François

doi:10.7554/elife.22796

Cited by 54 publications

(77 citation statements)

References 84 publications

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“…We computed the averaged opening dynamics following laser cuts for each type of junctions, and extracted the corresponding initial recoil velocity ( Figure 3C, 3D). As previously demonstrated (Chan et al 2017), this revealed a gradation of tensions according to junction type. Homotypic EN|EN junctions have the lowest tensions, E|E junctions have intermediate tensions, and heterotypic EN|E junctions have the highest tensions ( Figure 3F).…”

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiasupporting

confidence: 78%

“…To achieve this, we turned to the retina of Drosophila, composed of highly stereotyped groups of cells called ommatidia ( Figure 3A). Previous studies showed that cone cell shapes and arrangements in ommatidia are determined by differential tensions (Hayashi & Carthew 2004;Käfer et al 2007;Hilgenfeldt et al 2008;Chan et al 2017). These tensions were shown to be determined by the amounts of Myo-II and E-and N-cadherins recruited at the considered junctions (Chan et al 2017).…”

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

“…Previous studies showed that cone cell shapes and arrangements in ommatidia are determined by differential tensions (Hayashi & Carthew 2004;Käfer et al 2007;Hilgenfeldt et al 2008;Chan et al 2017). These tensions were shown to be determined by the amounts of Myo-II and E-and N-cadherins recruited at the considered junctions (Chan et al 2017). These amounts were in turn shown to be determined by the "identity" of junctions, that is, by the types of cadherins expressed in the two contacting cells (Chan et al 2017).…”

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

“…These tensions were shown to be determined by the amounts of Myo-II and E-and N-cadherins recruited at the considered junctions (Chan et al 2017). These amounts were in turn shown to be determined by the "identity" of junctions, that is, by the types of cadherins expressed in the two contacting cells (Chan et al 2017). Based on these previous results, we categorized junctions according to the cadherins expressed in the contacting cells.…”

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

“…Homotypic EN|EN junctions have the lowest tensions, E|E junctions have intermediate tensions, and heterotypic EN|E junctions have the highest tensions ( Figure 3F). Note that tensions are directly related to the amounts of Myo-II present at these junctions (Chan et al 2017). To perform force inference in this system, we averaged ommatidia geometry over N=51 ommatidia, and segmented the resulting image ( Figure 3A, 3B).…”

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

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Force inference predicts local and tissue-scale stress patterns in epithelia

Kong

Loison

Shivakumar

et al. 2018

Preprint

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Morphogenesis relies on the active generation of forces, and the transmission of these forces to surrounding cells and tissues. Hence measuring forces directly in developing embryos is an essential task to study the mechanics of development. Among the experimental techniques that have emerged to measure forces in epithelial tissues, force inference is particularly appealing. Indeed it only requires a snapshot of the tissue, as it relies on the topology and geometry of cell contacts, assuming that forces are balanced at each vertex. However, establishing force inference as a reliable technique requires thorough validation in multiple conditions. Here we performed systematic comparisons of force inference with laser ablation experiments in three distinct Drosophila epithelia. We show that force inference accurately predicts single junction tensions, tension patterns in stereotyped groups of cells, and tissue-scale stress patterns, in wild type and mutant conditions. We emphasize its ability to capture the distribution of forces at different scales from a single image, which gives it a critical advantage over perturbative techniques such as laser ablation. Our results demonstrate that force inference is a reliable and efficient method to quantify the mechanics of epithelial tissues during morphogenesis.

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Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiasupporting

confidence: 78%

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

Section: -Stereotyped Tension Patterns In Wild Type and Mutant Ommatidiamentioning

confidence: 99%

See 3 more Smart Citations

Force inference predicts local and tissue-scale stress patterns in epithelia

Kong

Loison

Shivakumar

et al. 2018

Preprint

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Drosophila Retinal Patterning

Spencer¹,

Johnson²,

Setu³

2020

Encyclopedia of Life Sciences

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The Drosophila eye is an outstanding model system for exploring fundamental mechanisms of growth and development. The adult eye is composed of a perfect hexagonal lattice of ∼750 unit eyes, or ommatidia, each containing precisely 20 well‐characterized cells. The eye develops from the eye/antennal imaginal disc, a flattened epithelial sac. During larval and pupal development, cells in the disc grow and undergo compartmentalisation, cell cycle arrest, differentiation, directed movement, and apoptosis, all utilising gene networks and signalling pathways similar to those in vertebrates. The genetic accessibility of Drosophila , together with the precision of eye development, makes the fly retina an extremely useful system with which to investigate the roles of genes and signalling pathways in development. Key Concepts Adult Drosophila eyes contain ∼750 ommatidia, or unit eyes; each ommatidium is made up of precisely 20 cells, each of which can be identified by its position and protein expression. Like other adult structures in Drosophila , the eye develops from an imaginal disc, a flattened sac of epithelial cells that develops during larval and pupal stages. Drosophila retinal development utilises gene regulatory networks similar to those in human eye development. Photoreceptor differentiation requires passage of the morphogenetic furrow, an invagination in eye disc that moves across the tissue from posterior to anterior during larval development. Photoreceptors differentiate during larval stages using signals emanating from previously differentiated cells, rather than through lineage restrictions. During pupal development, accessory cells differentiate and apoptosis reduces the number of cells in each ommatidium to 20. Cell interactions during pupal development produce the precise hexagonal lattice characteristic of the adult Drosophila eye.

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Different Biomechanical Cell Behaviors in an Epithelium Drive Collective Epithelial Cell Extrusion

Balasubramaniam,

Jain,

Dang

et al. 2024

Advanced Science

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In vertebrates, many organs, such as the kidney and the mammary gland form ductal structures based on the folding of epithelial sheets. The development of these organs relies on coordinated sorting of different cell lineages in both time and space, through mechanisms that remain largely unclear. Tissues are composed of several cell types with distinct biomechanical properties, particularly at cell‐cell and cell‐substrate boundaries. One hypothesis is that adjacent epithelial layers work in a coordinated manner to shape the tissue. Using in vitro experiments on model epithelial cells, differential expression of atypical Protein Kinase C iota (aPKCi), a key junctional polarity protein, is shown to reinforce cell epithelialization and trigger sorting by tuning cell mechanical properties at the tissue level. In a broader perspective, it is shown that in a heterogeneous epithelial monolayer, in which cell sorting occurs, forces arising from epithelial cell growth under confinement by surrounding cells with different biomechanical properties are sufficient to promote collective cell extrusion and generate emerging 3D organization related to spheroids and buds. Overall, this research sheds light on the role of aPKCi and the biomechanical interplay between distinct epithelial cell lineages in shaping tissue organization, providing insights into the understanding of tissue and organ development.

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Patterned cortical tension mediated by N-cadherin controls cell geometric order in the Drosophila eye

Cited by 54 publications

References 84 publications

Force inference predicts local and tissue-scale stress patterns in epithelia

Force inference predicts local and tissue-scale stress patterns in epithelia

Drosophila Retinal Patterning

Different Biomechanical Cell Behaviors in an Epithelium Drive Collective Epithelial Cell Extrusion

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