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Epithelial organ shape is generated by patterned actomyosin contractility and maintained by the extracellular matrix

Ali Nematbakhsh, Megan Levis, Nilay Kumar, Weitao Chen, Jeremiah J. Zartman, Mark Alber

2020PLoS Computational Biology44 citationsDOIOpen Access PDF

Abstract

Epithelial sheets define organ architecture during development. Here, we employed an iterative multiscale computational modeling and quantitative experimental approach to decouple direct and indirect effects of actomyosin-generated forces, nuclear positioning, extracellular matrix, and cell-cell adhesion in shaping Drosophila wing imaginal discs. Basally generated actomyosin forces generate epithelial bending of the wing disc pouch. Surprisingly, acute pharmacological inhibition of ROCK-driven actomyosin contractility does not impact the maintenance of tissue height or curved shape. Computational simulations show that ECM tautness provides only a minor contribution to modulating tissue shape. Instead, passive ECM pre-strain serves to maintain the shape independent from actomyosin contractility. These results provide general insight into how the subcellular forces are generated and maintained within individual cells to induce tissue curvature. Thus, the results suggest an important design principle of separable contributions from ECM prestrain and actomyosin tension during epithelial organogenesis and homeostasis.

Topics & Concepts

Extracellular matrixContractilityCell biologyFocal adhesionActinImaginal discMatrix (chemical analysis)BiophysicsTension (geology)BiologyChemistryAnatomyPhenotypeMaterials scienceBiochemistryPhosphorylationMetallurgyChromatographyGeneUltimate tensile strengthEndocrinologyCellular Mechanics and Interactions3D Printing in Biomedical ResearchDevelopmental Biology and Gene Regulation
Epithelial organ shape is generated by patterned actomyosin contractility and maintained by the extracellular matrix | Litcius