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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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(A) (a–d) Egg chambers labeled with 4′,6-diamidino-2-phenylindole and myosin-mCherry (surface view) at stage 8 (a), early stage 9 (b), late stage 9 (c), and stage 10 (d). Maximum-intensity projection of the z-stacks shows the early-stage apical concentrated myosin and basal accumulation of myosin after stage 9. Scale bar, 50 μm. (B) Mechanical model. Cartoon of surface view of a Drosophila egg chamber showing the D-V and A-P axes. Cells are modeled as springs of stiffness kc in the D-V direction and are connected in the A-P direction through angular springs of stiffness kas and preferred angle β as shown in C. (D) Zoomed-in midsection of the egg chamber. (E) Connection to the basal lamina. Each cell is identified by the angular positions of its ends, θ. (F) Biochemical model. Molecular pathway governing the activation of myosin contraction in response to tension. Fi (blue arrow) represents contractile force from the ith cell, and Fi−1 and Fi+1 (red arrows) represent forces on the ith cell by neighboring cells.
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Figure 1: (A) (a–d) Egg chambers labeled with 4′,6-diamidino-2-phenylindole and myosin-mCherry (surface view) at stage 8 (a), early stage 9 (b), late stage 9 (c), and stage 10 (d). Maximum-intensity projection of the z-stacks shows the early-stage apical concentrated myosin and basal accumulation of myosin after stage 9. Scale bar, 50 μm. (B) Mechanical model. Cartoon of surface view of a Drosophila egg chamber showing the D-V and A-P axes. Cells are modeled as springs of stiffness kc in the D-V direction and are connected in the A-P direction through angular springs of stiffness kas and preferred angle β as shown in C. (D) Zoomed-in midsection of the egg chamber. (E) Connection to the basal lamina. Each cell is identified by the angular positions of its ends, θ. (F) Biochemical model. Molecular pathway governing the activation of myosin contraction in response to tension. Fi (blue arrow) represents contractile force from the ith cell, and Fi−1 and Fi+1 (red arrows) represent forces on the ith cell by neighboring cells.

Mentions: The Drosophila ovary is composed of strings of developing egg chambers of increasing size and maturity (Figure 1, A–D). Each egg chamber contains 16 germ cells surrounded by a monolayer of epithelial follicle cells. Egg chambers increase in volume over time while also becoming elongated. Follicle cell shape oscillations begin during stage 9 of development in a subset of cells near the center and correlate with increasing basal myosin content due to activation of Rho GTPase and Rho-associated protein kinase, ROCK (He, Wang, et al., 2010). The maximal level of myosin activity and the number of cells undergoing oscillations increases during stage 9 until most of the epithelium shows high myosin activity at stage 10 (Figure 1, B–D). These observed oscillations in the basal surface area of follicle cells restrict the egg chamber width and thus promote tissue elongation and morphogenesis. Autonomous periodic oscillations have been explored in other areas in biology (Winfree, 1980; Goldbeter, 1996; Ferrel et al., 2011). Here we propose a mechanochemical model of cell contractility in the developing epithelium and investigate the spatial and temporal patterns in these oscillations using a combination of experiments and modeling. The model couples contractile forces generated by cells with mechanical tension from the external environment, including both the underlying germline cells and the overlying basal lamina. The model predicts that a cell can adjust its contractile force in response to external forces, and in some parameter regimes, the interplay of external tension and cell contractility leads to oscillations. Our model is based on the hypothesis that pressure on cells in the epithelium exerted by the growing germline cells induces the activation of the Rho-ROCK pathway (Amano et al., 1997; Pellegrin and Mellor, 2007; Zhao et al., 2007), which leads to negative feedback in the form of myosin contractility. We model a section of the egg chamber as circular arrays of cells connected to each other in a staggered manner (Figure 1, C–E). Cells are coupled mechanically to each other, as well as to the basal lamina, through mechanical springs in the circumferential and radial direction and angular springs in the axial direction. Forces developed by follicle cells are also under biochemical regulation. We investigate the interplay of biochemical signaling and mechanical forces during follicle cell length oscillations. The model predicts that the internal pressure of the egg chamber influences contractility of follicle cells. During egg chamber growth, increasing chamber pressure increases stress fiber formation and myosin contractility. Because cells are also mechanically coupled to each other, oscillations in any single cell are also coupled to oscillations in neighboring cells. Depending on parameters, oscillations could in principle become synchronized. However, since only asynchronous oscillations are observed experimentally, the model suggests the ranges of pressure and contractile forces that are consistent with these observations.


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)

(A) (a–d) Egg chambers labeled with 4′,6-diamidino-2-phenylindole and myosin-mCherry (surface view) at stage 8 (a), early stage 9 (b), late stage 9 (c), and stage 10 (d). Maximum-intensity projection of the z-stacks shows the early-stage apical concentrated myosin and basal accumulation of myosin after stage 9. Scale bar, 50 μm. (B) Mechanical model. Cartoon of surface view of a Drosophila egg chamber showing the D-V and A-P axes. Cells are modeled as springs of stiffness kc in the D-V direction and are connected in the A-P direction through angular springs of stiffness kas and preferred angle β as shown in C. (D) Zoomed-in midsection of the egg chamber. (E) Connection to the basal lamina. Each cell is identified by the angular positions of its ends, θ. (F) Biochemical model. Molecular pathway governing the activation of myosin contraction in response to tension. Fi (blue arrow) represents contractile force from the ith cell, and Fi−1 and Fi+1 (red arrows) represent forces on the ith cell by neighboring cells.
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Related In: Results  -  Collection

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Figure 1: (A) (a–d) Egg chambers labeled with 4′,6-diamidino-2-phenylindole and myosin-mCherry (surface view) at stage 8 (a), early stage 9 (b), late stage 9 (c), and stage 10 (d). Maximum-intensity projection of the z-stacks shows the early-stage apical concentrated myosin and basal accumulation of myosin after stage 9. Scale bar, 50 μm. (B) Mechanical model. Cartoon of surface view of a Drosophila egg chamber showing the D-V and A-P axes. Cells are modeled as springs of stiffness kc in the D-V direction and are connected in the A-P direction through angular springs of stiffness kas and preferred angle β as shown in C. (D) Zoomed-in midsection of the egg chamber. (E) Connection to the basal lamina. Each cell is identified by the angular positions of its ends, θ. (F) Biochemical model. Molecular pathway governing the activation of myosin contraction in response to tension. Fi (blue arrow) represents contractile force from the ith cell, and Fi−1 and Fi+1 (red arrows) represent forces on the ith cell by neighboring cells.
Mentions: The Drosophila ovary is composed of strings of developing egg chambers of increasing size and maturity (Figure 1, A–D). Each egg chamber contains 16 germ cells surrounded by a monolayer of epithelial follicle cells. Egg chambers increase in volume over time while also becoming elongated. Follicle cell shape oscillations begin during stage 9 of development in a subset of cells near the center and correlate with increasing basal myosin content due to activation of Rho GTPase and Rho-associated protein kinase, ROCK (He, Wang, et al., 2010). The maximal level of myosin activity and the number of cells undergoing oscillations increases during stage 9 until most of the epithelium shows high myosin activity at stage 10 (Figure 1, B–D). These observed oscillations in the basal surface area of follicle cells restrict the egg chamber width and thus promote tissue elongation and morphogenesis. Autonomous periodic oscillations have been explored in other areas in biology (Winfree, 1980; Goldbeter, 1996; Ferrel et al., 2011). Here we propose a mechanochemical model of cell contractility in the developing epithelium and investigate the spatial and temporal patterns in these oscillations using a combination of experiments and modeling. The model couples contractile forces generated by cells with mechanical tension from the external environment, including both the underlying germline cells and the overlying basal lamina. The model predicts that a cell can adjust its contractile force in response to external forces, and in some parameter regimes, the interplay of external tension and cell contractility leads to oscillations. Our model is based on the hypothesis that pressure on cells in the epithelium exerted by the growing germline cells induces the activation of the Rho-ROCK pathway (Amano et al., 1997; Pellegrin and Mellor, 2007; Zhao et al., 2007), which leads to negative feedback in the form of myosin contractility. We model a section of the egg chamber as circular arrays of cells connected to each other in a staggered manner (Figure 1, C–E). Cells are coupled mechanically to each other, as well as to the basal lamina, through mechanical springs in the circumferential and radial direction and angular springs in the axial direction. Forces developed by follicle cells are also under biochemical regulation. We investigate the interplay of biochemical signaling and mechanical forces during follicle cell length oscillations. The model predicts that the internal pressure of the egg chamber influences contractility of follicle cells. During egg chamber growth, increasing chamber pressure increases stress fiber formation and myosin contractility. Because cells are also mechanically coupled to each other, oscillations in any single cell are also coupled to oscillations in neighboring cells. Depending on parameters, oscillations could in principle become synchronized. However, since only asynchronous oscillations are observed experimentally, the model suggests the ranges of pressure and contractile forces that are consistent with these observations.

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