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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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Effects of the basal lamina and mosaic analysis. (A) Images of basal lamina (labeled with collagen–green fluorescent protein [GFP]) and myosin (myosin-mCherry) in control conditions. The relative positions of collagen and myosin fibers remains unchanged, suggesting that basal lamina could be mechanically coupled to basal myosin. Scale bar, 20 μm. (B) Egg chambers stained with collagen-GFP from stage 8 to stage 10 in control conditions, at the beginning of collagenase treatment (t = 0 min), and after collagenase treatment (t = 30 min). (C) Experimental measurements on follicle oscillations upon disruption of basal lamina. The distribution of oscillation periods became longer. The average egg chamber width became smaller (inset). (D) Modeling predictions of oscillation period as a function of stiffness of the basal lamina. Collagenase treatment reduces basal lamina stiffness and increases oscillation period for several values of P and Fmax. The predicted egg chamber radius also becomes smaller as basal lamina stiffness is reduced, in agreement with experiments. (E) It is possible to abolish myosin contraction in some follicle cells using constitutively relaxing cells (ROCK RNAi–expressing cells); these cells (green) do not oscillate. It is then possible to examine the interaction between the wild-type cells (blue and red) and mutant cells (green). (F) Experiments and modeling show that there are no changes to oscillatory period in neighboring wild-type cells (blue) or wild-type cells directly neighboring mutant cells (green). Mutant cells, however, cease to oscillate. The oscillatory period is unchanged in neighboring versus nonneighboring wild-type cells (inset).
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Figure 5: Effects of the basal lamina and mosaic analysis. (A) Images of basal lamina (labeled with collagen–green fluorescent protein [GFP]) and myosin (myosin-mCherry) in control conditions. The relative positions of collagen and myosin fibers remains unchanged, suggesting that basal lamina could be mechanically coupled to basal myosin. Scale bar, 20 μm. (B) Egg chambers stained with collagen-GFP from stage 8 to stage 10 in control conditions, at the beginning of collagenase treatment (t = 0 min), and after collagenase treatment (t = 30 min). (C) Experimental measurements on follicle oscillations upon disruption of basal lamina. The distribution of oscillation periods became longer. The average egg chamber width became smaller (inset). (D) Modeling predictions of oscillation period as a function of stiffness of the basal lamina. Collagenase treatment reduces basal lamina stiffness and increases oscillation period for several values of P and Fmax. The predicted egg chamber radius also becomes smaller as basal lamina stiffness is reduced, in agreement with experiments. (E) It is possible to abolish myosin contraction in some follicle cells using constitutively relaxing cells (ROCK RNAi–expressing cells); these cells (green) do not oscillate. It is then possible to examine the interaction between the wild-type cells (blue and red) and mutant cells (green). (F) Experiments and modeling show that there are no changes to oscillatory period in neighboring wild-type cells (blue) or wild-type cells directly neighboring mutant cells (green). Mutant cells, however, cease to oscillate. The oscillatory period is unchanged in neighboring versus nonneighboring wild-type cells (inset).

Mentions: In the egg chamber, the basal lamina is a highly cross-linked and complex structure, with collagens comprising ∼50% of the protein (Kalluri, 2003). Follicle cells adhere to the basal lamina via integrin-mediated adhesions that contain focal adhesion proteins such as talin and paxillin (Figure 5A and Supplemental Figure S8). We examined the effect of the basal lamina on follicle cell oscillations by treating wild-type cells with collagenase to partially remove the basal lamina surrounding the egg chamber (Figure 5B). Figure 5C shows the distribution of oscillation periods for control and collagenase-treated samples. On collagenase treatment, some cells no longer exhibit oscillations. Other cells show an increased oscillation period. The mean period in the control condition is 5.6 min, which increases to 10.6 min. In addition, the egg chamber radius decreases by ∼20% upon collagenase treatment (Figure 5C, inset).


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)

Effects of the basal lamina and mosaic analysis. (A) Images of basal lamina (labeled with collagen–green fluorescent protein [GFP]) and myosin (myosin-mCherry) in control conditions. The relative positions of collagen and myosin fibers remains unchanged, suggesting that basal lamina could be mechanically coupled to basal myosin. Scale bar, 20 μm. (B) Egg chambers stained with collagen-GFP from stage 8 to stage 10 in control conditions, at the beginning of collagenase treatment (t = 0 min), and after collagenase treatment (t = 30 min). (C) Experimental measurements on follicle oscillations upon disruption of basal lamina. The distribution of oscillation periods became longer. The average egg chamber width became smaller (inset). (D) Modeling predictions of oscillation period as a function of stiffness of the basal lamina. Collagenase treatment reduces basal lamina stiffness and increases oscillation period for several values of P and Fmax. The predicted egg chamber radius also becomes smaller as basal lamina stiffness is reduced, in agreement with experiments. (E) It is possible to abolish myosin contraction in some follicle cells using constitutively relaxing cells (ROCK RNAi–expressing cells); these cells (green) do not oscillate. It is then possible to examine the interaction between the wild-type cells (blue and red) and mutant cells (green). (F) Experiments and modeling show that there are no changes to oscillatory period in neighboring wild-type cells (blue) or wild-type cells directly neighboring mutant cells (green). Mutant cells, however, cease to oscillate. The oscillatory period is unchanged in neighboring versus nonneighboring wild-type cells (inset).
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Figure 5: Effects of the basal lamina and mosaic analysis. (A) Images of basal lamina (labeled with collagen–green fluorescent protein [GFP]) and myosin (myosin-mCherry) in control conditions. The relative positions of collagen and myosin fibers remains unchanged, suggesting that basal lamina could be mechanically coupled to basal myosin. Scale bar, 20 μm. (B) Egg chambers stained with collagen-GFP from stage 8 to stage 10 in control conditions, at the beginning of collagenase treatment (t = 0 min), and after collagenase treatment (t = 30 min). (C) Experimental measurements on follicle oscillations upon disruption of basal lamina. The distribution of oscillation periods became longer. The average egg chamber width became smaller (inset). (D) Modeling predictions of oscillation period as a function of stiffness of the basal lamina. Collagenase treatment reduces basal lamina stiffness and increases oscillation period for several values of P and Fmax. The predicted egg chamber radius also becomes smaller as basal lamina stiffness is reduced, in agreement with experiments. (E) It is possible to abolish myosin contraction in some follicle cells using constitutively relaxing cells (ROCK RNAi–expressing cells); these cells (green) do not oscillate. It is then possible to examine the interaction between the wild-type cells (blue and red) and mutant cells (green). (F) Experiments and modeling show that there are no changes to oscillatory period in neighboring wild-type cells (blue) or wild-type cells directly neighboring mutant cells (green). Mutant cells, however, cease to oscillate. The oscillatory period is unchanged in neighboring versus nonneighboring wild-type cells (inset).
Mentions: In the egg chamber, the basal lamina is a highly cross-linked and complex structure, with collagens comprising ∼50% of the protein (Kalluri, 2003). Follicle cells adhere to the basal lamina via integrin-mediated adhesions that contain focal adhesion proteins such as talin and paxillin (Figure 5A and Supplemental Figure S8). We examined the effect of the basal lamina on follicle cell oscillations by treating wild-type cells with collagenase to partially remove the basal lamina surrounding the egg chamber (Figure 5B). Figure 5C shows the distribution of oscillation periods for control and collagenase-treated samples. On collagenase treatment, some cells no longer exhibit oscillations. Other cells show an increased oscillation period. The mean period in the control condition is 5.6 min, which increases to 10.6 min. In addition, the egg chamber radius decreases by ∼20% upon collagenase treatment (Figure 5C, inset).

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