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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Published inThe Journal of cell biology Vol. 220; no. 11; p. 1
Main Authors Bhide, Sourabh, Gombalova, Denisa, Mönke, Gregor, Stegmaier, Johannes, Zinchenko, Valentyna, Kreshuk, Anna, Belmonte, Julio M, Leptin, Maria
Format Journal Article
LanguageEnglish
Published United States Rockefeller University Press 01.11.2021
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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Abstract 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.
AbstractList 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.
This paper shows that adjacent cells with similar genetic capabilities to change their own shape enter a tug of war that determines which cell shrinks and which expands. For a cell to contract, its neighbors must yield, requiring a nonlinear stress–strain response in the mechanism governing its physical properties. 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.
Author Zinchenko, Valentyna
Kreshuk, Anna
Bhide, Sourabh
Stegmaier, Johannes
Belmonte, Julio M
Leptin, Maria
Mönke, Gregor
Gombalova, Denisa
AuthorAffiliation 2 Collaboration for Joint PhD Degree between European Molecular Biology Laboratory and Faculty of Biosciences, Heidelberg University, Heidelberg, Germany
1 Director’s Research Unit, European Molecular Biology Laboratory, Heidelberg, Germany
5 Department of Physics, North Carolina State University, Raleigh, NC
6 Quantitative and Computational Developmental Biology Cluster, North Carolina State University, Raleigh, NC
7 European Molecular Biology Organization, Heidelberg, Germany
3 Institute of Imaging and Computer Vision, Rheinisch-Westfälische Technische Hochschule Aachen University, Aachen, Germany
4 Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
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– name: 7 European Molecular Biology Organization, Heidelberg, Germany
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  surname: Leptin
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D. Gombalova and G. Mönke contributed equally to this paper.
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Snippet 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...
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...
This paper shows that adjacent cells with similar genetic capabilities to change their own shape enter a tug of war that determines which cell shrinks and...
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StartPage 1
SubjectTerms 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
Title Mechanical competition alters the cellular interpretation of an endogenous genetic program
URI https://www.ncbi.nlm.nih.gov/pubmed/34449835
https://www.proquest.com/docview/2593663970/abstract/
https://search.proquest.com/docview/2566037654
https://pubmed.ncbi.nlm.nih.gov/PMC8406609
Volume 220
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