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Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing.

Etournay R, Popović M, Merkel M, Nandi A, Blasse C, Aigouy B, Brandl H, Myers G, Salbreux G, Jülicher F, Eaton S - Elife (2015)

Bottom Line: We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape.We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape.We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

ABSTRACT
How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

No MeSH data available.


Related in: MedlinePlus

Method to determine stresses in WT and dumpyov1 mutant.(A, B) Enlarged regions of the wing epithelium at 22.5 hAPF, before (A) and 50 s after (B) circular laser ablation in the epithelium. The green circle depicts the 14 µm circular cut in diameter. The red ellipse is a fit to the manually segmented perimeter of the cut region at 50 s. Minor (blue) and major (magenta) axes of this ellipse are used to define orthogonal kymographs. Scale bar 20 µm. (C, D) Kymographs defined in (B). Arrowheads depict the lines that were segmented using Fiji. Δx shows the relative increase in wing tissue displacement along the major and minor axes after the cut. (E) Graph showing an example of the relative tissue displacement along the major and minor axes. These displacements are used to estimate the initial velocity gradient of recoil after laser ablation (‘Materials and methods’, Analysis of circular laser ablations). The initial velocity gradient reflects the isotropic and and anisotropic stresses in the tissue. (F, G) Comparison of stresses between WT control and dumpyov1 mutant wings. Circular cuts were performed in nine different locations as depicted in Figure 2I,I′. Error bars show standard deviation over five replicates for each location and genotype.DOI:http://dx.doi.org/10.7554/eLife.07090.008
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fig2s3: Method to determine stresses in WT and dumpyov1 mutant.(A, B) Enlarged regions of the wing epithelium at 22.5 hAPF, before (A) and 50 s after (B) circular laser ablation in the epithelium. The green circle depicts the 14 µm circular cut in diameter. The red ellipse is a fit to the manually segmented perimeter of the cut region at 50 s. Minor (blue) and major (magenta) axes of this ellipse are used to define orthogonal kymographs. Scale bar 20 µm. (C, D) Kymographs defined in (B). Arrowheads depict the lines that were segmented using Fiji. Δx shows the relative increase in wing tissue displacement along the major and minor axes after the cut. (E) Graph showing an example of the relative tissue displacement along the major and minor axes. These displacements are used to estimate the initial velocity gradient of recoil after laser ablation (‘Materials and methods’, Analysis of circular laser ablations). The initial velocity gradient reflects the isotropic and and anisotropic stresses in the tissue. (F, G) Comparison of stresses between WT control and dumpyov1 mutant wings. Circular cuts were performed in nine different locations as depicted in Figure 2I,I′. Error bars show standard deviation over five replicates for each location and genotype.DOI:http://dx.doi.org/10.7554/eLife.07090.008

Mentions: To ask how the dumpyov1 mutation influenced PD tension in the wing blade, we performed circular laser cuts covering about 5–10 cells in different regions of WT and dumpyov1 wings (Figure 2I,I′, Figure 2—figure supplement 3). We observed a recoil of the ablated region, indicating that the blade epithelium is under tension. From the recoil, we can compare both the isotropic and the anisotropic components of epithelial stress in WT and dumpyov1 mutant wings (Figure 2I,I′ and Figure 2—figure supplement 3). These stress patterns differ between WT and dumpyov1 wings. The orientation of anisotropic stress in dumpyov1 is somewhat splayed and not as well aligned with the PD axis. Furthermore, anisotropic tension in dumpyov1 wings tends to be reduced in the central region and increased anteriorly and posteriorly.


Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing.

Etournay R, Popović M, Merkel M, Nandi A, Blasse C, Aigouy B, Brandl H, Myers G, Salbreux G, Jülicher F, Eaton S - Elife (2015)

Method to determine stresses in WT and dumpyov1 mutant.(A, B) Enlarged regions of the wing epithelium at 22.5 hAPF, before (A) and 50 s after (B) circular laser ablation in the epithelium. The green circle depicts the 14 µm circular cut in diameter. The red ellipse is a fit to the manually segmented perimeter of the cut region at 50 s. Minor (blue) and major (magenta) axes of this ellipse are used to define orthogonal kymographs. Scale bar 20 µm. (C, D) Kymographs defined in (B). Arrowheads depict the lines that were segmented using Fiji. Δx shows the relative increase in wing tissue displacement along the major and minor axes after the cut. (E) Graph showing an example of the relative tissue displacement along the major and minor axes. These displacements are used to estimate the initial velocity gradient of recoil after laser ablation (‘Materials and methods’, Analysis of circular laser ablations). The initial velocity gradient reflects the isotropic and and anisotropic stresses in the tissue. (F, G) Comparison of stresses between WT control and dumpyov1 mutant wings. Circular cuts were performed in nine different locations as depicted in Figure 2I,I′. Error bars show standard deviation over five replicates for each location and genotype.DOI:http://dx.doi.org/10.7554/eLife.07090.008
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Related In: Results  -  Collection

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fig2s3: Method to determine stresses in WT and dumpyov1 mutant.(A, B) Enlarged regions of the wing epithelium at 22.5 hAPF, before (A) and 50 s after (B) circular laser ablation in the epithelium. The green circle depicts the 14 µm circular cut in diameter. The red ellipse is a fit to the manually segmented perimeter of the cut region at 50 s. Minor (blue) and major (magenta) axes of this ellipse are used to define orthogonal kymographs. Scale bar 20 µm. (C, D) Kymographs defined in (B). Arrowheads depict the lines that were segmented using Fiji. Δx shows the relative increase in wing tissue displacement along the major and minor axes after the cut. (E) Graph showing an example of the relative tissue displacement along the major and minor axes. These displacements are used to estimate the initial velocity gradient of recoil after laser ablation (‘Materials and methods’, Analysis of circular laser ablations). The initial velocity gradient reflects the isotropic and and anisotropic stresses in the tissue. (F, G) Comparison of stresses between WT control and dumpyov1 mutant wings. Circular cuts were performed in nine different locations as depicted in Figure 2I,I′. Error bars show standard deviation over five replicates for each location and genotype.DOI:http://dx.doi.org/10.7554/eLife.07090.008
Mentions: To ask how the dumpyov1 mutation influenced PD tension in the wing blade, we performed circular laser cuts covering about 5–10 cells in different regions of WT and dumpyov1 wings (Figure 2I,I′, Figure 2—figure supplement 3). We observed a recoil of the ablated region, indicating that the blade epithelium is under tension. From the recoil, we can compare both the isotropic and the anisotropic components of epithelial stress in WT and dumpyov1 mutant wings (Figure 2I,I′ and Figure 2—figure supplement 3). These stress patterns differ between WT and dumpyov1 wings. The orientation of anisotropic stress in dumpyov1 is somewhat splayed and not as well aligned with the PD axis. Furthermore, anisotropic tension in dumpyov1 wings tends to be reduced in the central region and increased anteriorly and posteriorly.

Bottom Line: We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape.We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape.We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

ABSTRACT
How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

No MeSH data available.


Related in: MedlinePlus