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Hydraulic fracture during epithelial stretching.

Casares L, Vincent R, Zalvidea D, Campillo N, Navajas D, Arroyo M, Trepat X - Nat Mater (2015)

Bottom Line: Here, we demonstrate that for a variety of synthetic and physiological hydrogel substrates the formation of epithelial cracks is caused by tissue stretching independently of epithelial tension.We show that the origin of the cracks is hydraulic; they result from a transient pressure build-up in the substrate during stretch and compression manoeuvres.Our findings demonstrate that epithelial integrity is determined in a tension-independent manner by the coupling between tissue stretching and matrix hydraulics.

View Article: PubMed Central - PubMed

Affiliation: Institute for Bioengineering of Catalonia, 08028 Barcelona, Spain.

ABSTRACT
The origin of fracture in epithelial cell sheets subject to stretch is commonly attributed to excess tension in the cells' cytoskeleton, in the plasma membrane, or in cell-cell contacts. Here, we demonstrate that for a variety of synthetic and physiological hydrogel substrates the formation of epithelial cracks is caused by tissue stretching independently of epithelial tension. We show that the origin of the cracks is hydraulic; they result from a transient pressure build-up in the substrate during stretch and compression manoeuvres. After pressure equilibration, cracks heal readily through actomyosin-dependent mechanisms. The observed phenomenology is captured by the theory of poroelasticity, which predicts the size and healing dynamics of epithelial cracks as a function of the stiffness, geometry and composition of the hydrogel substrate. Our findings demonstrate that epithelial integrity is determined in a tension-independent manner by the coupling between tissue stretching and matrix hydraulics.

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Cracks are independent of epithelial tensiona, Time-lapse imaging of patterned clusters (top) and zoomed regions (bottom) of MDCK cells expressing LifeAct-GFP before and after application of successive pulses of 10 min and 1s duration. Arrowheads point at cracks. The acquisition time of each snap shot is marked by a black dot on the time axis. b, Percentage of junctions with cracks after stretch pulses of 1 s, 1 min or 10 min duration. Stretch pulses were applied consecutively to each pattern, in a random order and spaced by >15 min (n=6 different patterns). c,d, Colour maps showing traction forces (top) and epithelial tension (bottom) before, during and after a 10 min (c) or 1 s (d) stretch pulses. Phase contrast images on the left show the measured MDCK cell cluster. e,f, Schemes illustrating the physical meaning of traction and tension in the epithelial clusters. g,h, Traction forces and tension during and after a 10 min duration and 10% strain pulse versus a 0% strain (both normalized to baseline levels). i,j, Traction forces and tension after stretch pulses of different duration normalized to baseline levels. Error bars in g-j show SEM of n=6 clusters per condition. Epithelial clusters are 80 μm in diameter.
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Figure 2: Cracks are independent of epithelial tensiona, Time-lapse imaging of patterned clusters (top) and zoomed regions (bottom) of MDCK cells expressing LifeAct-GFP before and after application of successive pulses of 10 min and 1s duration. Arrowheads point at cracks. The acquisition time of each snap shot is marked by a black dot on the time axis. b, Percentage of junctions with cracks after stretch pulses of 1 s, 1 min or 10 min duration. Stretch pulses were applied consecutively to each pattern, in a random order and spaced by >15 min (n=6 different patterns). c,d, Colour maps showing traction forces (top) and epithelial tension (bottom) before, during and after a 10 min (c) or 1 s (d) stretch pulses. Phase contrast images on the left show the measured MDCK cell cluster. e,f, Schemes illustrating the physical meaning of traction and tension in the epithelial clusters. g,h, Traction forces and tension during and after a 10 min duration and 10% strain pulse versus a 0% strain (both normalized to baseline levels). i,j, Traction forces and tension after stretch pulses of different duration normalized to baseline levels. Error bars in g-j show SEM of n=6 clusters per condition. Epithelial clusters are 80 μm in diameter.

Mentions: To further characterize the cracks we subjected the clusters to a series of three stretch pulses of the same magnitude (10% strain) but different duration (1 s, 1 min, 10 min), applied in random order and spaced by 30 min intervals (Fig. 2a). These experiments showed that the number and size of the cracks increased with the duration of stretch; in response to 10 min pulses, most cell-cell junctions exhibited cracks, whereas in response to 1 s pulses cracks were largely absent (Fig. 2b).


Hydraulic fracture during epithelial stretching.

Casares L, Vincent R, Zalvidea D, Campillo N, Navajas D, Arroyo M, Trepat X - Nat Mater (2015)

Cracks are independent of epithelial tensiona, Time-lapse imaging of patterned clusters (top) and zoomed regions (bottom) of MDCK cells expressing LifeAct-GFP before and after application of successive pulses of 10 min and 1s duration. Arrowheads point at cracks. The acquisition time of each snap shot is marked by a black dot on the time axis. b, Percentage of junctions with cracks after stretch pulses of 1 s, 1 min or 10 min duration. Stretch pulses were applied consecutively to each pattern, in a random order and spaced by >15 min (n=6 different patterns). c,d, Colour maps showing traction forces (top) and epithelial tension (bottom) before, during and after a 10 min (c) or 1 s (d) stretch pulses. Phase contrast images on the left show the measured MDCK cell cluster. e,f, Schemes illustrating the physical meaning of traction and tension in the epithelial clusters. g,h, Traction forces and tension during and after a 10 min duration and 10% strain pulse versus a 0% strain (both normalized to baseline levels). i,j, Traction forces and tension after stretch pulses of different duration normalized to baseline levels. Error bars in g-j show SEM of n=6 clusters per condition. Epithelial clusters are 80 μm in diameter.
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Figure 2: Cracks are independent of epithelial tensiona, Time-lapse imaging of patterned clusters (top) and zoomed regions (bottom) of MDCK cells expressing LifeAct-GFP before and after application of successive pulses of 10 min and 1s duration. Arrowheads point at cracks. The acquisition time of each snap shot is marked by a black dot on the time axis. b, Percentage of junctions with cracks after stretch pulses of 1 s, 1 min or 10 min duration. Stretch pulses were applied consecutively to each pattern, in a random order and spaced by >15 min (n=6 different patterns). c,d, Colour maps showing traction forces (top) and epithelial tension (bottom) before, during and after a 10 min (c) or 1 s (d) stretch pulses. Phase contrast images on the left show the measured MDCK cell cluster. e,f, Schemes illustrating the physical meaning of traction and tension in the epithelial clusters. g,h, Traction forces and tension during and after a 10 min duration and 10% strain pulse versus a 0% strain (both normalized to baseline levels). i,j, Traction forces and tension after stretch pulses of different duration normalized to baseline levels. Error bars in g-j show SEM of n=6 clusters per condition. Epithelial clusters are 80 μm in diameter.
Mentions: To further characterize the cracks we subjected the clusters to a series of three stretch pulses of the same magnitude (10% strain) but different duration (1 s, 1 min, 10 min), applied in random order and spaced by 30 min intervals (Fig. 2a). These experiments showed that the number and size of the cracks increased with the duration of stretch; in response to 10 min pulses, most cell-cell junctions exhibited cracks, whereas in response to 1 s pulses cracks were largely absent (Fig. 2b).

Bottom Line: Here, we demonstrate that for a variety of synthetic and physiological hydrogel substrates the formation of epithelial cracks is caused by tissue stretching independently of epithelial tension.We show that the origin of the cracks is hydraulic; they result from a transient pressure build-up in the substrate during stretch and compression manoeuvres.Our findings demonstrate that epithelial integrity is determined in a tension-independent manner by the coupling between tissue stretching and matrix hydraulics.

View Article: PubMed Central - PubMed

Affiliation: Institute for Bioengineering of Catalonia, 08028 Barcelona, Spain.

ABSTRACT
The origin of fracture in epithelial cell sheets subject to stretch is commonly attributed to excess tension in the cells' cytoskeleton, in the plasma membrane, or in cell-cell contacts. Here, we demonstrate that for a variety of synthetic and physiological hydrogel substrates the formation of epithelial cracks is caused by tissue stretching independently of epithelial tension. We show that the origin of the cracks is hydraulic; they result from a transient pressure build-up in the substrate during stretch and compression manoeuvres. After pressure equilibration, cracks heal readily through actomyosin-dependent mechanisms. The observed phenomenology is captured by the theory of poroelasticity, which predicts the size and healing dynamics of epithelial cracks as a function of the stiffness, geometry and composition of the hydrogel substrate. Our findings demonstrate that epithelial integrity is determined in a tension-independent manner by the coupling between tissue stretching and matrix hydraulics.

Show MeSH
Related in: MedlinePlus