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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

Physical constraints at the margin maintain epithelial tension in the wing.(A) Cartoon depicting a pupal wing at 32 hAPF. Dashed double-sided arrows depict the proximal-distal (PD) and anterior-posterior (AP) axes. The PD axis is defined by a regression line passing through selected sensory organs (red dots) that are easily identifiable in Ecad::GFP expressing wings. The x axis is defined to correspond to the PD axis pointing distally, and the y axis is defined to correspond to the AP axis pointing anteriorly. L2–L5 indicate longitudinal veins 2–5. Brown dashed line outlines the cuticular sac surrounding the wing epithelium. Scale bar 20 µm. (B, B′) Show the distal end of a wild-type (WT) Ecad::GFP-expressing wing at 24 hAPF (greyscale in B, B′) and the same wing 3.5 min after laser ablation in the space between wing margin and cuticle (magenta in B′). The blue dashed line indicates the site of laser ablation. (B′′) Shows wing margin displacement measured with respect to the cuticle (brown dashed line in B′) along the white dotted line in (B′). Experimental points (magenta) were interpolated by a polynomial (blue line). (C–F) Show 32 hAPF wings that were unperturbed (C) or subjected to laser ablation at 22 hAPF (D–F). Ablation of the connections between the wing margin and the cuticle were performed in different regions, indicated by blue dashed lines in (D–F), and lead to altered wing shapes at 32 hAPF compared to the unperturbed control (C). Scale bar 100 µm.DOI:http://dx.doi.org/10.7554/eLife.07090.003
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fig1: Physical constraints at the margin maintain epithelial tension in the wing.(A) Cartoon depicting a pupal wing at 32 hAPF. Dashed double-sided arrows depict the proximal-distal (PD) and anterior-posterior (AP) axes. The PD axis is defined by a regression line passing through selected sensory organs (red dots) that are easily identifiable in Ecad::GFP expressing wings. The x axis is defined to correspond to the PD axis pointing distally, and the y axis is defined to correspond to the AP axis pointing anteriorly. L2–L5 indicate longitudinal veins 2–5. Brown dashed line outlines the cuticular sac surrounding the wing epithelium. Scale bar 20 µm. (B, B′) Show the distal end of a wild-type (WT) Ecad::GFP-expressing wing at 24 hAPF (greyscale in B, B′) and the same wing 3.5 min after laser ablation in the space between wing margin and cuticle (magenta in B′). The blue dashed line indicates the site of laser ablation. (B′′) Shows wing margin displacement measured with respect to the cuticle (brown dashed line in B′) along the white dotted line in (B′). Experimental points (magenta) were interpolated by a polynomial (blue line). (C–F) Show 32 hAPF wings that were unperturbed (C) or subjected to laser ablation at 22 hAPF (D–F). Ablation of the connections between the wing margin and the cuticle were performed in different regions, indicated by blue dashed lines in (D–F), and lead to altered wing shapes at 32 hAPF compared to the unperturbed control (C). Scale bar 100 µm.DOI:http://dx.doi.org/10.7554/eLife.07090.003

Mentions: The emergence of two-dimensional stresses in the plane of the wing blade suggests that there are physical constraints on the movement of wing epithelial cells near the margin. We wondered whether there might be a matrix connecting the wing epithelium to the overlying pupal cuticle in this region. To investigate this, we used a laser to destroy the region between the margin of the E-Cadherin:GFP expressing wing epithelium and the cuticle after the two had separated as a consequence of molting. Although this treatment does not apparently damage either the wing or the cuticle, it causes the wing epithelium to rapidly retract away from the cuticle within seconds (Figure 1A–B′′, Video 1). Laser ablation causes epithelial retraction when performed at any region along the wing blade margin—anteriorly, posteriorly or distally. During tissue flows, the now disconnected margin moves even further away from the cuticle, producing abnormal wing shapes (Figure 1C–F). This shows that the wing is physically restrained by apical extracellular matrix connections to the overlying cuticle, and that these connections are required to shape the wing during tissue flows.10.7554/eLife.07090.003Figure 1.Physical constraints at the margin maintain epithelial tension in the wing.


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)

Physical constraints at the margin maintain epithelial tension in the wing.(A) Cartoon depicting a pupal wing at 32 hAPF. Dashed double-sided arrows depict the proximal-distal (PD) and anterior-posterior (AP) axes. The PD axis is defined by a regression line passing through selected sensory organs (red dots) that are easily identifiable in Ecad::GFP expressing wings. The x axis is defined to correspond to the PD axis pointing distally, and the y axis is defined to correspond to the AP axis pointing anteriorly. L2–L5 indicate longitudinal veins 2–5. Brown dashed line outlines the cuticular sac surrounding the wing epithelium. Scale bar 20 µm. (B, B′) Show the distal end of a wild-type (WT) Ecad::GFP-expressing wing at 24 hAPF (greyscale in B, B′) and the same wing 3.5 min after laser ablation in the space between wing margin and cuticle (magenta in B′). The blue dashed line indicates the site of laser ablation. (B′′) Shows wing margin displacement measured with respect to the cuticle (brown dashed line in B′) along the white dotted line in (B′). Experimental points (magenta) were interpolated by a polynomial (blue line). (C–F) Show 32 hAPF wings that were unperturbed (C) or subjected to laser ablation at 22 hAPF (D–F). Ablation of the connections between the wing margin and the cuticle were performed in different regions, indicated by blue dashed lines in (D–F), and lead to altered wing shapes at 32 hAPF compared to the unperturbed control (C). Scale bar 100 µm.DOI:http://dx.doi.org/10.7554/eLife.07090.003
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Related In: Results  -  Collection

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fig1: Physical constraints at the margin maintain epithelial tension in the wing.(A) Cartoon depicting a pupal wing at 32 hAPF. Dashed double-sided arrows depict the proximal-distal (PD) and anterior-posterior (AP) axes. The PD axis is defined by a regression line passing through selected sensory organs (red dots) that are easily identifiable in Ecad::GFP expressing wings. The x axis is defined to correspond to the PD axis pointing distally, and the y axis is defined to correspond to the AP axis pointing anteriorly. L2–L5 indicate longitudinal veins 2–5. Brown dashed line outlines the cuticular sac surrounding the wing epithelium. Scale bar 20 µm. (B, B′) Show the distal end of a wild-type (WT) Ecad::GFP-expressing wing at 24 hAPF (greyscale in B, B′) and the same wing 3.5 min after laser ablation in the space between wing margin and cuticle (magenta in B′). The blue dashed line indicates the site of laser ablation. (B′′) Shows wing margin displacement measured with respect to the cuticle (brown dashed line in B′) along the white dotted line in (B′). Experimental points (magenta) were interpolated by a polynomial (blue line). (C–F) Show 32 hAPF wings that were unperturbed (C) or subjected to laser ablation at 22 hAPF (D–F). Ablation of the connections between the wing margin and the cuticle were performed in different regions, indicated by blue dashed lines in (D–F), and lead to altered wing shapes at 32 hAPF compared to the unperturbed control (C). Scale bar 100 µm.DOI:http://dx.doi.org/10.7554/eLife.07090.003
Mentions: The emergence of two-dimensional stresses in the plane of the wing blade suggests that there are physical constraints on the movement of wing epithelial cells near the margin. We wondered whether there might be a matrix connecting the wing epithelium to the overlying pupal cuticle in this region. To investigate this, we used a laser to destroy the region between the margin of the E-Cadherin:GFP expressing wing epithelium and the cuticle after the two had separated as a consequence of molting. Although this treatment does not apparently damage either the wing or the cuticle, it causes the wing epithelium to rapidly retract away from the cuticle within seconds (Figure 1A–B′′, Video 1). Laser ablation causes epithelial retraction when performed at any region along the wing blade margin—anteriorly, posteriorly or distally. During tissue flows, the now disconnected margin moves even further away from the cuticle, producing abnormal wing shapes (Figure 1C–F). This shows that the wing is physically restrained by apical extracellular matrix connections to the overlying cuticle, and that these connections are required to shape the wing during tissue flows.10.7554/eLife.07090.003Figure 1.Physical constraints at the margin maintain epithelial tension in the wing.

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