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

TitleMechanochemical regulation of oscillatory follicle cell dynamics in the developing Drosophila egg chamber.
Publication TypeJournal Article
Year of Publication2014
AuthorsKoride S, He L, Xiong L-P, Lan G, Montell DJ, Sun SX
JournalMol Biol Cell
Volume25
Issue22
Pagination3709-16
Date Published2014 Nov 05
ISSN1939-4586
KeywordsAnimals, Biomechanical Phenomena, Cell Size, Drosophila melanogaster, Female, Gene Expression, Insect Proteins, Mechanotransduction, Cellular, Models, Biological, Morphogenesis, Myosins, Oogenesis, Organ Size, Ovarian Follicle, rho-Associated Kinases, Zygote
Abstract

<p>During tissue elongation from stage 9 to stage 10 in Drosophila oogenesis, the egg chamber increases in length by ∼1.7-fold while increasing in volume by eightfold. During these stages, spontaneous oscillations in the contraction of cell basal surfaces develop in a subset of follicle cells. This patterned activity is required for elongation of the egg chamber; however, the mechanisms generating the spatiotemporal pattern have been unclear. Here we use a combination of quantitative modeling and experimental perturbation to show that mechanochemical interactions are sufficient to generate oscillations of myosin contractile activity in the observed spatiotemporal pattern. We propose that follicle cells in the epithelial layer contract against pressure in the expanding egg chamber. As tension in the epithelial layer increases, Rho kinase signaling activates myosin assembly and contraction. The activation process is cooperative, leading to a limit cycle in the myosin dynamics. Our model produces asynchronous oscillations in follicle cell area and myosin content, consistent with experimental observations. In addition, we test the prediction that removal of the basal lamina will increase the average oscillation period. The model demonstrates that in principle, mechanochemical interactions are sufficient to drive patterning and morphogenesis, independent of patterned gene expression.</p>

DOI10.1091/mbc.E14-04-0875
Alternate JournalMol. Biol. Cell
PubMed ID24943847
PubMed Central IDPMC4230628
Grant List1R01GM075305 / GM / NIGMS NIH HHS / United States
R01 GM075305 / GM / NIGMS NIH HHS / United States
U54 CA143868 / CA / NCI NIH HHS / United States
R01 GM073164 / GM / NIGMS NIH HHS / United States
1U54CA143868-01 / CA / NCI NIH HHS / United States
R01GM73164 / GM / NIGMS NIH HHS / United States