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Assembly and positioning of actomyosin rings by contractility and planar cell polarity.

Sehring IM, Recho P, Denker E, Kourakis M, Mathiesen B, Hannezo E, Dong B, Jiang D - Elife (2015)

Bottom Line: Intriguingly, rings always form at the cells' anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex.We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results.We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events.

View Article: PubMed Central - PubMed

Affiliation: Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.

ABSTRACT
The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to self-assemble and reposition actomyosin rings, which play an essential role for cell elongation. Intriguingly, rings always form at the cells' anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex. Our drug and genetic manipulations uncover a tug-of-war between contractility, which localizes cortical flows toward the equator and PCP, which tries to reposition them. We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results. We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events.

No MeSH data available.


Comparison of the model and experimental filament average velocity during development and blebbistatin repositioning.Black arrow indicates the blebbistatin treatment.DOI:http://dx.doi.org/10.7554/eLife.09206.021
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fig12: Comparison of the model and experimental filament average velocity during development and blebbistatin repositioning.Black arrow indicates the blebbistatin treatment.DOI:http://dx.doi.org/10.7554/eLife.09206.021

Mentions: Maximal velocity estimated by PIV is of the order of v ≈ 50 nm s−1 and decays to zero over roughly a fourth of the cell length that is 3 μm. Over the same length, intensity of actin fluorescence can increase roughly of one half of its base value leading ρ − ρ0 ∼ 0.5ρ0. We thus obtain (χρ0)/η ≈ 0.03 s−1. This ratio is in agreement with the estimates of (Julicher et al., 2007; Rubinstein et al., 2009), which suggest χρ0 ≈ 103 Pa, η ≈ 104–105 Pa · s. We then obtain . For the numerical model, to fit the experimental data, we postulated that C increases linearly in time from to thus assuming an increase of the (homogeneous) cortical tension of roughly 1.5 as measured experimentally during the course of development (see Appendix figure 5B of the main text where an elongation of 72% is related to an increase of the rescaled tension from 1.2 to 1.8, hence the assumed 1.5 increase). Notice that this is this increase that dictates the ring migration dynamic. Indeed, from the average filament velocity v ≈ 30 nm s−1, it would take ∼3 min for the ring to migrate from the side to center position (a ∼6 μm distance) if the internal flow were driving the ring positioning.10.7554/eLife.09206.020Appendix figure 4.Comparison of the model and experimental anterior and posterior lateral domains during normal development blebbistatin treatment.


Assembly and positioning of actomyosin rings by contractility and planar cell polarity.

Sehring IM, Recho P, Denker E, Kourakis M, Mathiesen B, Hannezo E, Dong B, Jiang D - Elife (2015)

Comparison of the model and experimental filament average velocity during development and blebbistatin repositioning.Black arrow indicates the blebbistatin treatment.DOI:http://dx.doi.org/10.7554/eLife.09206.021
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4612727&req=5

fig12: Comparison of the model and experimental filament average velocity during development and blebbistatin repositioning.Black arrow indicates the blebbistatin treatment.DOI:http://dx.doi.org/10.7554/eLife.09206.021
Mentions: Maximal velocity estimated by PIV is of the order of v ≈ 50 nm s−1 and decays to zero over roughly a fourth of the cell length that is 3 μm. Over the same length, intensity of actin fluorescence can increase roughly of one half of its base value leading ρ − ρ0 ∼ 0.5ρ0. We thus obtain (χρ0)/η ≈ 0.03 s−1. This ratio is in agreement with the estimates of (Julicher et al., 2007; Rubinstein et al., 2009), which suggest χρ0 ≈ 103 Pa, η ≈ 104–105 Pa · s. We then obtain . For the numerical model, to fit the experimental data, we postulated that C increases linearly in time from to thus assuming an increase of the (homogeneous) cortical tension of roughly 1.5 as measured experimentally during the course of development (see Appendix figure 5B of the main text where an elongation of 72% is related to an increase of the rescaled tension from 1.2 to 1.8, hence the assumed 1.5 increase). Notice that this is this increase that dictates the ring migration dynamic. Indeed, from the average filament velocity v ≈ 30 nm s−1, it would take ∼3 min for the ring to migrate from the side to center position (a ∼6 μm distance) if the internal flow were driving the ring positioning.10.7554/eLife.09206.020Appendix figure 4.Comparison of the model and experimental anterior and posterior lateral domains during normal development blebbistatin treatment.

Bottom Line: Intriguingly, rings always form at the cells' anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex.We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results.We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events.

View Article: PubMed Central - PubMed

Affiliation: Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.

ABSTRACT
The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to self-assemble and reposition actomyosin rings, which play an essential role for cell elongation. Intriguingly, rings always form at the cells' anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex. Our drug and genetic manipulations uncover a tug-of-war between contractility, which localizes cortical flows toward the equator and PCP, which tries to reposition them. We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results. We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events.

No MeSH data available.