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Epithelial organ shape is generated by patterned actomyosin contractility and maintained by the extracellular matrix
- Source :
- PLoS Computational Biology, Vol 16, Iss 8, p e1008105 (2020), PLoS Computational Biology, PLoS computational biology, vol 16, iss 8
- Publication Year :
- 2020
- Publisher :
- Public Library of Science (PLoS), 2020.
-
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.<br />Author summary The regulation and maintenance of an organ’s shape is a major outstanding problem in developmental biology. An iterative approach combining multiscale computational modelling and quantitative experimental approach was used to decouple direct and indirect roles of subcellular mechanical forces, nuclear positioning, and extracellular matrix in shaping the major axis of the wing pouch during the larval stage in fruit flies, which serves as a prototypical system for investigating epithelial morphogenesis. The research findings in this paper demonstrate that subcellular mechanical forces can effectively generate the curved tissue profile, while extracellular matrix is necessary for preserving the bent shape even in the absence of subcellular mechanical forces once the shape is generated. The developed integrated multiscale modelling environment can be readily extended to generate and test hypothesized novel mechanisms of developmental dynamics of other systems, including organoids that consist of several cellular and extracellular matrix layers.
- Subjects :
- 0301 basic medicine
Bending
Cell Membranes
Mathematical Sciences
Epithelium
Extracellular matrix
0302 clinical medicine
Wings
Potential Energy
Morphogenesis
Wings, Animal
Phosphorylation
Biology (General)
Staining
0303 health sciences
Ecology
Chemistry
Physics
Drosophila Melanogaster
Classical Mechanics
Eukaryota
Cell Staining
Adhesion
Animal Models
Actomyosin
Biological Sciences
Deformation
Cell biology
Extracellular Matrix
Insects
Imaginal disc
medicine.anatomical_structure
Computational Theory and Mathematics
Imaginal Discs
Experimental Organism Systems
Modeling and Simulation
Physical Sciences
Drosophila
Cellular Structures and Organelles
Research Article
Arthropoda
Bioinformatics
QH301-705.5
Organogenesis
Bioengineering
Research and Analysis Methods
Contractility
03 medical and health sciences
Cellular and Molecular Neuroscience
Model Organisms
Information and Computing Sciences
Extracellular
medicine
Genetics
Animals
Molecular Biology
Ecology, Evolution, Behavior and Systematics
030304 developmental biology
Basement membrane
Damage Mechanics
Wing
Animal
Organisms
Biology and Life Sciences
Cell Biology
Invertebrates
Cell staining
030104 developmental biology
Specimen Preparation and Treatment
Biophysics
Animal Studies
Generic health relevance
Zoology
Entomology
030217 neurology & neurosurgery
Developmental Biology
Subjects
Details
- Language :
- English
- ISSN :
- 15537358
- Volume :
- 16
- Issue :
- 8
- Database :
- OpenAIRE
- Journal :
- PLoS Computational Biology
- Accession number :
- edsair.doi.dedup.....3941d08a9811a56311464341fee7dabc