Unit Operations of Tissue Development: Epithelial Folding

Zartman, Jeremiah J.; Shvartsman, Stanislav Y.

doi:10.1146/annurev-chembioeng-073009-100919

Cited by 42 publications

(32 citation statements)

References 86 publications

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“…Epithelial sheets adopt complex three-dimensional shapes through a sequence of folding steps during animal development 1 – 3 . Epithelial folding is instrumental during processes such as embryonic gastrulation 4 and neural tube 5 and eye 6 formation, and defects in epithelial folding can lead to severe developmental disorders in humans 7 .…”

Section: Introductionmentioning

confidence: 99%

Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms

et al. 2018

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Epithelial folding transforms simple sheets of cells into complex three-dimensional tissues and organs during animal development. Epithelial folding has mainly been attributed to mechanical forces generated by an apically localized actomyosin network, however, contributions of forces generated at basal and lateral cell surfaces remain largely unknown. Here we show that a local decrease of basal tension and an increased lateral tension, but not apical constriction, drive the formation of two neighboring folds in developing Drosophila wing imaginal discs. Spatially defined reduction of extracellular matrix density results in local decrease of basal tension in the first fold; fluctuations in F-actin lead to increased lateral tension in the second fold. Simulations using a 3D vertex model show that the two distinct mechanisms can drive epithelial folding. Our combination of lateral and basal tension measurements with a mechanical tissue model reveals how simple modulations of surface and edge tension drive complex three-dimensional morphological changes.

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Section: Introductionmentioning

confidence: 99%

Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms

et al. 2018

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“…Epithelial morphogenesis is similar to origami (Zartman and Shvartsman, 2010), since in both processes a two-dimensional sheet (of cells, or paper) is patterned (with gene-expression patterns, or folds) to guide its transformation into a 3D structure. However, epithelial morphogenesis is clearly more complex.…”

Section: Introductionmentioning

confidence: 99%

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

2017

Self Cite

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Summary Understanding the mechanisms driving tissue and organ formation requires knowledge across scales. How do signaling pathways specify distinct tissue types? How does the patterning system control morphogenesis? How do these processes evolve? The Drosophila egg chamber, where EGF and BMP signaling intersect to specify unique cell types that construct epithelial tubes for specialized eggshell structures, has provided a tractable system to ask these questions. Work there has elucidated connections between scales of development, including across evolutionary scales, and fostered the development of quantitative modeling tools. These tools and general principles can be applied towards understanding other developmental processes across organisms.

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“…The interaction of self-deforming, connected cells results in a global three-dimensional shape-shifting of a cell sheet or tissue. However, cell sheet folding in animal model organisms frequently involves other processes such as cell division, migration and intercalation, which obscure the specific role of cell shape changes [ 62 – 67 , 70 – 80 ].…”

Section: Introductionmentioning

confidence: 99%

Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Höhn

Hallmann

2016

BMC Dev Biol

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Background: The multicellular volvocine alga Pleodorina is intermediate in organismal complexity between its unicellular relative, Chlamydomonas, and its multicellular relative, Volvox, which shows complete division of labor between different cell types. The volvocine green microalgae form a group of genera closely related to the genus Volvox within the order Volvocales (Chlorophyta). Embryos of multicellular volvocine algae consist of a cellular monolayer that, depending on the species, is either bowl-shaped or comprises a sphere. During embryogenesis, multicellular volvocine embryos turn their cellular monolayer right-side out to expose their flagella. This process is called 'inversion' and serves as simple model for epithelial folding in metazoa. While the development of spherical Volvox embryos has been the subject of detailed studies, the inversion process of bowl-shaped embryos is less well understood. Therefore, it has been unclear how the inversion of a sphere might have evolved from less complicated processes.

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Unit Operations of Tissue Development: Epithelial Folding

Cited by 42 publications

References 86 publications

Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms

Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

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