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Mechanochemical regulation of oscillatory follicle cell dynamics in the developing Drosophila egg chamber.

Koride S, He L, Xiong LP, Lan G, Montell DJ, Sun SX - Mol. Biol. Cell (2014)

Bottom Line: We propose that follicle cells in the epithelial layer contract against pressure in the expanding egg chamber.The activation process is cooperative, leading to a limit cycle in the myosin dynamics.The model demonstrates that in principle, mechanochemical interactions are sufficient to drive patterning and morphogenesis, independent of patterned gene expression.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD 21218.

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Follicle cell length and myosin oscillations. (A) Plot showing oscillations in cell length (blue) and myosin content (red). Increase in myosin content corresponds to decrease in cell length. (B) Oscillation period distribution for different initial conditions (ICs), showing that the range is between 5 and 7 min and is independent of ICs. (C) Phase distribution of oscillations in 120 cells, showing that the oscillations are asynchronous. The phases are uniformly distributed around 2π. (D, E) Phase diagrams of oscillatory behavior with and without basal lamina. The system generally exhibits asynchronous oscillations or steady nonoscillatory behavior. There is a small synchronous oscillation regime without basal lamina (white), although this would require a high internal pressure. The red circle indicates, in our model, the region close to the physiological situation.
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Figure 3: Follicle cell length and myosin oscillations. (A) Plot showing oscillations in cell length (blue) and myosin content (red). Increase in myosin content corresponds to decrease in cell length. (B) Oscillation period distribution for different initial conditions (ICs), showing that the range is between 5 and 7 min and is independent of ICs. (C) Phase distribution of oscillations in 120 cells, showing that the oscillations are asynchronous. The phases are uniformly distributed around 2π. (D, E) Phase diagrams of oscillatory behavior with and without basal lamina. The system generally exhibits asynchronous oscillations or steady nonoscillatory behavior. There is a small synchronous oscillation regime without basal lamina (white), although this would require a high internal pressure. The red circle indicates, in our model, the region close to the physiological situation.

Mentions: When multiple follicle cells are mechanically connected in the epithelium, our model simulations show that the cells will oscillate along the D-V axis with an average period of ∼5–7 min (He, Wang, et al., 2010). The oscillation amplitude ranges from 0.5 to 2 μm, which also is what experiments observe (He, Wang, et al., 2010). Experiments show that oscillations in myosin intensity are correlated with and precede oscillations in basal cell area in follicle cells (He, Wang, et al., 2010). In our model, normalized activated myosin also shows oscillations with periods similar to those of oscillations in cell length. Figure 3A shows myosin and cell length oscillations on the same plot. Myosin activation precedes reduction in cell length as observed in vivo. We fit a cosine function to the computed oscillations and obtain the phase of oscillation for each cell. We find that this system at long times shows a uniform distribution of oscillatory phase (Figure 3C). This suggests that the oscillations are asynchronous. If oscillations are synchronous, all cells would have a similar phase, and the phase distribution would be more concentrated. We do find a synchronous phase in other parameter regimes (Figure 3, D and E). The observed oscillations are also independent of initial starting configurations of the model (Figure 3B).


Mechanochemical regulation of oscillatory follicle cell dynamics in the developing Drosophila egg chamber.

Koride S, He L, Xiong LP, Lan G, Montell DJ, Sun SX - Mol. Biol. Cell (2014)

Follicle cell length and myosin oscillations. (A) Plot showing oscillations in cell length (blue) and myosin content (red). Increase in myosin content corresponds to decrease in cell length. (B) Oscillation period distribution for different initial conditions (ICs), showing that the range is between 5 and 7 min and is independent of ICs. (C) Phase distribution of oscillations in 120 cells, showing that the oscillations are asynchronous. The phases are uniformly distributed around 2π. (D, E) Phase diagrams of oscillatory behavior with and without basal lamina. The system generally exhibits asynchronous oscillations or steady nonoscillatory behavior. There is a small synchronous oscillation regime without basal lamina (white), although this would require a high internal pressure. The red circle indicates, in our model, the region close to the physiological situation.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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Figure 3: Follicle cell length and myosin oscillations. (A) Plot showing oscillations in cell length (blue) and myosin content (red). Increase in myosin content corresponds to decrease in cell length. (B) Oscillation period distribution for different initial conditions (ICs), showing that the range is between 5 and 7 min and is independent of ICs. (C) Phase distribution of oscillations in 120 cells, showing that the oscillations are asynchronous. The phases are uniformly distributed around 2π. (D, E) Phase diagrams of oscillatory behavior with and without basal lamina. The system generally exhibits asynchronous oscillations or steady nonoscillatory behavior. There is a small synchronous oscillation regime without basal lamina (white), although this would require a high internal pressure. The red circle indicates, in our model, the region close to the physiological situation.
Mentions: When multiple follicle cells are mechanically connected in the epithelium, our model simulations show that the cells will oscillate along the D-V axis with an average period of ∼5–7 min (He, Wang, et al., 2010). The oscillation amplitude ranges from 0.5 to 2 μm, which also is what experiments observe (He, Wang, et al., 2010). Experiments show that oscillations in myosin intensity are correlated with and precede oscillations in basal cell area in follicle cells (He, Wang, et al., 2010). In our model, normalized activated myosin also shows oscillations with periods similar to those of oscillations in cell length. Figure 3A shows myosin and cell length oscillations on the same plot. Myosin activation precedes reduction in cell length as observed in vivo. We fit a cosine function to the computed oscillations and obtain the phase of oscillation for each cell. We find that this system at long times shows a uniform distribution of oscillatory phase (Figure 3C). This suggests that the oscillations are asynchronous. If oscillations are synchronous, all cells would have a similar phase, and the phase distribution would be more concentrated. We do find a synchronous phase in other parameter regimes (Figure 3, D and E). The observed oscillations are also independent of initial starting configurations of the model (Figure 3B).

Bottom Line: We propose that follicle cells in the epithelial layer contract against pressure in the expanding egg chamber.The activation process is cooperative, leading to a limit cycle in the myosin dynamics.The model demonstrates that in principle, mechanochemical interactions are sufficient to drive patterning and morphogenesis, independent of patterned gene expression.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD 21218.

Show MeSH
Related in: MedlinePlus