E-cadherin tunes tissue mechanical behavior before and during morphogenetic tissue flows

Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how cell-cell adhesion influences mechanics in both static and dynamically flowing confluent epithelial tissues. Here, we systematically modulate E-cad...

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Published inCurrent biology Vol. 34; no. 15; pp. 3367 - 3379.e5
Main Authors Wang, Xun, Cupo, Christian M., Ostvar, Sassan, Countryman, Andrew D., Kasza, Karen E.
Format Journal Article
LanguageEnglish
Published England Elsevier Inc 05.08.2024
Subjects
Actomyosin - metabolism
Animals
Biomechanical Phenomena
Cadherins - metabolism
Cell Adhesion - physiology
cell-cell adhesion
convergent extension
Drosophila melanogaster - metabolism
Drosophila melanogaster - physiology
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
E-cadherin
Embryo, Nonmammalian - metabolism
Embryo, Nonmammalian - physiology
epithelial morphogenesis
Morphogenesis
tissue fluidity
cell-cell adhesion
epithelial morphogenesis
E-cadherin
convergent extension
tissue fluidity
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Abstract Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how cell-cell adhesion influences mechanics in both static and dynamically flowing confluent epithelial tissues. Here, we systematically modulate E-cadherin-mediated adhesion in the Drosophila embryo and study the effects on the mechanical behavior of the germband epithelium before and during dramatic tissue remodeling and flow associated with body axis elongation. Before axis elongation, we find that increasing E-cadherin levels produces tissue comprising more elongated cells and predicted to be more fluid-like, providing reduced resistance to tissue flow. During axis elongation, we find that the dominant effect of E-cadherin is tuning the speed at which cells proceed through rearrangement events. Before and during axis elongation, E-cadherin levels influence patterns of actomyosin-dependent forces, supporting the notion that E-cadherin tunes tissue mechanics in part through effects on actomyosin. Notably, the effects of ∼4-fold changes in E-cadherin levels on overall tissue structure and flow are relatively weak, suggesting that the system is tolerant to changes in absolute E-cadherin levels over this range where an intact tissue is formed. Taken together, these findings reveal dual—and sometimes opposing—roles for E-cadherin-mediated adhesion in controlling tissue structure and dynamics in vivo, which result in unexpected relationships between adhesion and flow in confluent tissues. •Elevated E-cadherin levels produce tissues with more elongated cells•E-cadherin levels tune the speed of cell rearrangements in elongating tissues•E-cadherin levels tune tissue mechanics in part through effects on actomyosin•Drosophila axis elongation is robust to 4-fold changes in E-cadherin levels Wang et al. quantitatively study how E-cadherin levels influence tissue structure and dynamics in the Drosophila embryo before and during body axis elongation. They find that E-cadherin levels tune cell shapes and cell rearrangement speeds, in part via effects on actomyosin, and uncover that axis elongation is resilient to changes in E-cadherin levels.
AbstractList Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how cell-cell adhesion influences mechanics in both static and dynamically flowing confluent epithelial tissues. Here, we systematically modulate E-cadherin-mediated adhesion in the Drosophila embryo and study the effects on the mechanical behavior of the germband epithelium before and during dramatic tissue remodeling and flow associated with body axis elongation. Before axis elongation, we find that increasing E-cadherin levels produces tissue comprising more elongated cells and predicted to be more fluid-like, providing reduced resistance to tissue flow. During axis elongation, we find that the dominant effect of E-cadherin is tuning the speed at which cells proceed through rearrangement events. Before and during axis elongation, E-cadherin levels influence patterns of actomyosin-dependent forces, supporting the notion that E-cadherin tunes tissue mechanics in part through effects on actomyosin. Notably, the effects of ∼4-fold changes in E-cadherin levels on overall tissue structure and flow are relatively weak, suggesting that the system is tolerant to changes in absolute E-cadherin levels over this range where an intact tissue is formed. Taken together, these findings reveal dual-and sometimes opposing-roles for E-cadherin-mediated adhesion in controlling tissue structure and dynamics in vivo, which result in unexpected relationships between adhesion and flow in confluent tissues.
Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how cell-cell adhesion influences mechanics in both static and dynamically flowing confluent epithelial tissues. Here, we systematically modulate E-cadherin-mediated adhesion in the Drosophila embryo and study the effects on the mechanical behavior of the germband epithelium before and during dramatic tissue remodeling and flow associated with body axis elongation. Before axis elongation, we find that increasing E-cadherin levels produces tissue comprising more elongated cells and predicted to be more fluid-like, providing reduced resistance to tissue flow. During axis elongation, we find that the dominant effect of E-cadherin is tuning the speed at which cells proceed through rearrangement events. Before and during axis elongation, E-cadherin levels influence patterns of actomyosin-dependent forces, supporting the notion that E-cadherin tunes tissue mechanics in part through effects on actomyosin. Notably, the effects of ∼4-fold changes in E-cadherin levels on overall tissue structure and flow are relatively weak, suggesting that the system is tolerant to changes in absolute E-cadherin levels over this range where an intact tissue is formed. Taken together, these findings reveal dual—and sometimes opposing—roles for E-cadherin-mediated adhesion in controlling tissue structure and dynamics in vivo, which result in unexpected relationships between adhesion and flow in confluent tissues. •Elevated E-cadherin levels produce tissues with more elongated cells•E-cadherin levels tune the speed of cell rearrangements in elongating tissues•E-cadherin levels tune tissue mechanics in part through effects on actomyosin•Drosophila axis elongation is robust to 4-fold changes in E-cadherin levels Wang et al. quantitatively study how E-cadherin levels influence tissue structure and dynamics in the Drosophila embryo before and during body axis elongation. They find that E-cadherin levels tune cell shapes and cell rearrangement speeds, in part via effects on actomyosin, and uncover that axis elongation is resilient to changes in E-cadherin levels.
Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how cell-cell adhesion influences mechanics in both static and dynamically flowing confluent epithelial tissues. Here, we systematically modulate E-cadherin-mediated adhesion in the Drosophila embryo and study the effects on the mechanical behavior of the germband epithelium before and during dramatic tissue remodeling and flow associated with body axis elongation. Before axis elongation, we find that increasing E-cadherin levels produces tissue comprising more elongated cells and predicted to be more fluid-like, providing reduced resistance to tissue flow. During axis elongation, we find that the dominant effect of E-cadherin is tuning the speed at which cells proceed through rearrangement events. Before and during axis elongation, E-cadherin levels influence patterns of actomyosin-dependent forces, supporting the notion that E-cadherin tunes tissue mechanics in part through effects on actomyosin. Notably, the effects of ∼4-fold changes in E-cadherin levels on overall tissue structure and flow are relatively weak, suggesting that the system is tolerant to changes in absolute E-cadherin levels over this range where an intact tissue is formed. Taken together, these findings reveal dual-and sometimes opposing-roles for E-cadherin-mediated adhesion in controlling tissue structure and dynamics in vivo, which result in unexpected relationships between adhesion and flow in confluent tissues.Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how cell-cell adhesion influences mechanics in both static and dynamically flowing confluent epithelial tissues. Here, we systematically modulate E-cadherin-mediated adhesion in the Drosophila embryo and study the effects on the mechanical behavior of the germband epithelium before and during dramatic tissue remodeling and flow associated with body axis elongation. Before axis elongation, we find that increasing E-cadherin levels produces tissue comprising more elongated cells and predicted to be more fluid-like, providing reduced resistance to tissue flow. During axis elongation, we find that the dominant effect of E-cadherin is tuning the speed at which cells proceed through rearrangement events. Before and during axis elongation, E-cadherin levels influence patterns of actomyosin-dependent forces, supporting the notion that E-cadherin tunes tissue mechanics in part through effects on actomyosin. Notably, the effects of ∼4-fold changes in E-cadherin levels on overall tissue structure and flow are relatively weak, suggesting that the system is tolerant to changes in absolute E-cadherin levels over this range where an intact tissue is formed. Taken together, these findings reveal dual-and sometimes opposing-roles for E-cadherin-mediated adhesion in controlling tissue structure and dynamics in vivo, which result in unexpected relationships between adhesion and flow in confluent tissues.
Author Ostvar, Sassan
Wang, Xun
Cupo, Christian M.
Countryman, Andrew D.
Kasza, Karen E.
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Keywords cell-cell adhesion
epithelial morphogenesis
E-cadherin
convergent extension
tissue fluidity
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  start-page: 82
  year: 2012
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  article-title: Epithelial machines that shape the embryo
  publication-title: Trends Cell Biol.
  doi: 10.1016/j.tcb.2011.10.005
  contributor:
    fullname: Davidson
– volume: 13
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  article-title: Mechanical coupling between endoderm invagination and axis extension in Drosophila
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.1002292
  contributor:
    fullname: Lye
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Snippet Adhesion between epithelial cells enables the remarkable mechanical behavior of epithelial tissues during morphogenesis. However, it remains unclear how...
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SubjectTerms Actomyosin - metabolism
Animals
Biomechanical Phenomena
Cadherins - metabolism
Cell Adhesion - physiology
cell-cell adhesion
convergent extension
Drosophila melanogaster - metabolism
Drosophila melanogaster - physiology
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
E-cadherin
Embryo, Nonmammalian - metabolism
Embryo, Nonmammalian - physiology
epithelial morphogenesis
Morphogenesis
tissue fluidity
Title E-cadherin tunes tissue mechanical behavior before and during morphogenetic tissue flows
URI https://dx.doi.org/10.1016/j.cub.2024.06.038
https://www.ncbi.nlm.nih.gov/pubmed/39013464
https://www.proquest.com/docview/3081771456/abstract/
Volume 34
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