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A simplified mechanism for anisotropic constriction in Drosophila mesoderm.

ABSTRACT: Understanding how forces and material properties give rise to tissue shapes is a fundamental issue in developmental biology. Although Drosophila gastrulation is a well-used system for investigating tissue morphogenesis, a consensus mechanical model that explains all the key features of this process does not exist. One key feature of Drosophila gastrulation is its anisotropy: the mesoderm constricts much more along one axis than along the other. Previous explanations have involved graded stress, anisotropic stresses or material properties, or mechanosensitive feedback. Here, we show that these mechanisms are not required to explain the anisotropy of constriction. Instead, constriction can be anisotropic if only two conditions are met: the tissue is elastic, as was demonstrated in our recent study; and the contractile domain is asymmetric. This conclusion is general and does not depend on the values of model parameters. Our model can explain results from classical tissue-grafting experiments and from more-recent laser ablation studies. Furthermore, our model may provide alternative explanations for experiments in other developmental systems, including C. elegans and zebrafish.

SUBMITTER: Doubrovinski K

PROVIDER: S-EPMC6307890 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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A simplified mechanism for anisotropic constriction in Drosophila mesoderm.

Doubrovinski Konstantin K Tchoufag Joel J Mandadapu Kranthi K

Development (Cambridge, England) 20181210 24

Understanding how forces and material properties give rise to tissue shapes is a fundamental issue in developmental biology. Although Drosophila gastrulation is a well-used system for investigating tissue morphogenesis, a consensus mechanical model that explains all the key features of this process does not exist. One key feature of Drosophila gastrulation is its anisotropy: the mesoderm constricts much more along one axis than along the other. Previous explanations have involved g ...[more]

PMID: 30401702

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Project description:A critical juncture in early development is the partitioning of cells that will adopt different fates into three germ layers: the ectoderm, the mesoderm, and the endoderm. This step is achieved through the internalization of specified cells from the outermost surface layer, through a process called gastrulation. In Drosophila, gastrulation is achieved through cell shape changes (i.e., apical constriction) that change tissue curvature and lead to the folding of a surface epithelium. Folding of embryonic tissue results in mesoderm and endoderm invagination, not as individual cells, but as collective tissue units. The tractability of Drosophila as a model system is best exemplified by how much we know about Drosophila gastrulation, from the signals that pattern the embryo to the molecular components that generate force, and how these components are organized to promote cell and tissue shape changes. For mesoderm invagination, graded signaling by the morphogen, Spätzle, sets up a gradient in transcriptional activity that leads to the expression of a secreted ligand (Folded gastrulation) and a transmembrane protein (T48). Together with the GPCR Mist, which is expressed in the mesoderm, and the GPCR Smog, which is expressed uniformly, these signals activate heterotrimeric G-protein and small Rho-family G-protein signaling to promote apical contractility and changes in cell and tissue shape. A notable feature of this signaling pathway is its intricate organization in both space and time. At the cellular level, signaling components and the cytoskeleton exhibit striking polarity, not only along the apical-basal cell axis, but also within the apical domain. Furthermore, gene expression controls a highly choreographed chain of events, the dynamics of which are critical for primordium invagination; it does not simply throw the cytoskeletal "on" switch. Finally, studies of Drosophila gastrulation have provided insight into how global tissue mechanics and movements are intertwined as multiple tissues simultaneously change shape. Overall, these studies have contributed to the view that cells respond to forces that propagate over great distances, demonstrating that cellular decisions, and, ultimately, tissue shape changes, proceed by integrating cues across an entire embryo.

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A simplified mechanism for anisotropic constriction in Drosophila mesoderm.

Publications

A simplified mechanism for anisotropic constriction in <i>Drosophila</i> mesoderm.

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