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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.


Related in: MedlinePlus

Verifications of the model assumptions and fitting of parameters.(A) Sketch of our model. Contractility destabilizes an initially homogenous cortex into a central ring, whereas PCP-driven preferential anterior polymerization localizes the ring on the edge. (B) Measurement of the angle between lateral and basal membrane during the elongation (2.5 increase) and ring migration (1.5 increase) process, which indicates their relative tensions (n > 15 for each time point). Basal tension increases with time.  is the basal contractility,  is the lateral contractility and θ is the angle between lateral and basal membranes. We have the geometric relation . (C) PIV analysis of cortical flows in late stage embryos. (D) Linear negative correlation between local actin intensity and velocity gradients, as extracted from PIV. Actin intensity and velocities have been rescaled in the dimensionless units described in the main text and in Appendix 2: rescaling. (E) Comparison between intensity and velocity profiles and our theoretical predictions (data extracted from C). The velocity field is rescaled by the average velocity.DOI:http://dx.doi.org/10.7554/eLife.09206.015
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fig5: Verifications of the model assumptions and fitting of parameters.(A) Sketch of our model. Contractility destabilizes an initially homogenous cortex into a central ring, whereas PCP-driven preferential anterior polymerization localizes the ring on the edge. (B) Measurement of the angle between lateral and basal membrane during the elongation (2.5 increase) and ring migration (1.5 increase) process, which indicates their relative tensions (n > 15 for each time point). Basal tension increases with time. is the basal contractility, is the lateral contractility and θ is the angle between lateral and basal membranes. We have the geometric relation . (C) PIV analysis of cortical flows in late stage embryos. (D) Linear negative correlation between local actin intensity and velocity gradients, as extracted from PIV. Actin intensity and velocities have been rescaled in the dimensionless units described in the main text and in Appendix 2: rescaling. (E) Comparison between intensity and velocity profiles and our theoretical predictions (data extracted from C). The velocity field is rescaled by the average velocity.DOI:http://dx.doi.org/10.7554/eLife.09206.015

Mentions: In order to probe quantitatively these findings, we follow the theory of active gels (Kruse et al., 2005; Prost et al., 2015) to develop a very simple biophysical model of the actomyosin cortex as a viscous contractile gel, undergoing steady turnover (see Appendix 1: Physical modeling of the Ciona cortical flows for details). Such models generically predict spontaneous accumulations of actomyosin. Indeed, if the actomyosin concentration is slightly higher in a given region, then the contractile stress is also locally higher compared to the surroundings. Because of this initially small imbalance, surrounding actomyosin fibers flow towards the accumulation, making it even denser and even more contractile (Recho et al., 2013). This self-reinforcing loop, which concentrates actomyosin in a single spot at the cortex with filaments flowing towards the ring, is resisted by their depolymerization and effective diffusion (Figure 5A), which favor a homogenous cortex.10.7554/eLife.09206.015Figure 5.Verifications of the model assumptions and fitting of parameters.


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)

Verifications of the model assumptions and fitting of parameters.(A) Sketch of our model. Contractility destabilizes an initially homogenous cortex into a central ring, whereas PCP-driven preferential anterior polymerization localizes the ring on the edge. (B) Measurement of the angle between lateral and basal membrane during the elongation (2.5 increase) and ring migration (1.5 increase) process, which indicates their relative tensions (n > 15 for each time point). Basal tension increases with time.  is the basal contractility,  is the lateral contractility and θ is the angle between lateral and basal membranes. We have the geometric relation . (C) PIV analysis of cortical flows in late stage embryos. (D) Linear negative correlation between local actin intensity and velocity gradients, as extracted from PIV. Actin intensity and velocities have been rescaled in the dimensionless units described in the main text and in Appendix 2: rescaling. (E) Comparison between intensity and velocity profiles and our theoretical predictions (data extracted from C). The velocity field is rescaled by the average velocity.DOI:http://dx.doi.org/10.7554/eLife.09206.015
© Copyright Policy
Related In: Results  -  Collection

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

fig5: Verifications of the model assumptions and fitting of parameters.(A) Sketch of our model. Contractility destabilizes an initially homogenous cortex into a central ring, whereas PCP-driven preferential anterior polymerization localizes the ring on the edge. (B) Measurement of the angle between lateral and basal membrane during the elongation (2.5 increase) and ring migration (1.5 increase) process, which indicates their relative tensions (n > 15 for each time point). Basal tension increases with time. is the basal contractility, is the lateral contractility and θ is the angle between lateral and basal membranes. We have the geometric relation . (C) PIV analysis of cortical flows in late stage embryos. (D) Linear negative correlation between local actin intensity and velocity gradients, as extracted from PIV. Actin intensity and velocities have been rescaled in the dimensionless units described in the main text and in Appendix 2: rescaling. (E) Comparison between intensity and velocity profiles and our theoretical predictions (data extracted from C). The velocity field is rescaled by the average velocity.DOI:http://dx.doi.org/10.7554/eLife.09206.015
Mentions: In order to probe quantitatively these findings, we follow the theory of active gels (Kruse et al., 2005; Prost et al., 2015) to develop a very simple biophysical model of the actomyosin cortex as a viscous contractile gel, undergoing steady turnover (see Appendix 1: Physical modeling of the Ciona cortical flows for details). Such models generically predict spontaneous accumulations of actomyosin. Indeed, if the actomyosin concentration is slightly higher in a given region, then the contractile stress is also locally higher compared to the surroundings. Because of this initially small imbalance, surrounding actomyosin fibers flow towards the accumulation, making it even denser and even more contractile (Recho et al., 2013). This self-reinforcing loop, which concentrates actomyosin in a single spot at the cortex with filaments flowing towards the ring, is resisted by their depolymerization and effective diffusion (Figure 5A), which favor a homogenous cortex.10.7554/eLife.09206.015Figure 5.Verifications of the model assumptions and fitting of parameters.

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.


Related in: MedlinePlus