Mechanical competition alters the cellular interpretation of an endogenous genetic program

The intrinsic genetic program of a cell is not sufficient to explain all of the cell's activities. External mechanical stimuli are increasingly recognized as determinants of cell behavior. In the epithelial folding event that constitutes the beginning of gastrulation in Drosophila, the genetic...

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Bibliographic Details
Published in:The Journal of cell biology 2021-11, Vol.220 (11), p.1
Main Authors: Bhide, Sourabh, Gombalova, Denisa, Mönke, Gregor, Stegmaier, Johannes, Zinchenko, Valentyna, Kreshuk, Anna, Belmonte, Julio M, Leptin, Maria
Format: Article
Language:English
Subjects:
Actin
Actin Cytoskeleton - genetics
Actins - genetics
Actomyosin
Actomyosin - genetics
Animals
Biophysics
Cell Shape - genetics
Contractility
Cytoskeleton
Cytoskeleton - genetics
Drosophila melanogaster - genetics
Drosophila Proteins - genetics
Folding
Gastrulation
Gastrulation - genetics
Mechanical properties
Mechanical stimuli
Mesoderm
Mesoderm - physiology
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Summary:The intrinsic genetic program of a cell is not sufficient to explain all of the cell's activities. External mechanical stimuli are increasingly recognized as determinants of cell behavior. In the epithelial folding event that constitutes the beginning of gastrulation in Drosophila, the genetic program of the future mesoderm leads to the establishment of a contractile actomyosin network that triggers apical constriction of cells and thereby tissue folding. However, some cells do not constrict but instead stretch, even though they share the same genetic program as their constricting neighbors. We show here that tissue-wide interactions force these cells to expand even when an otherwise sufficient amount of apical, active actomyosin is present. Models based on contractile forces and linear stress-strain responses do not reproduce experimental observations, but simulations in which cells behave as ductile materials with nonlinear mechanical properties do. Our models show that this behavior is a general emergent property of actomyosin networks in a supracellular context, in accordance with our experimental observations of actin reorganization within stretching cells.
ISSN:0021-9525
1540-8140
DOI:10.1083/jcb.202104107