title: Mechanochemical regulation of oscillatory follicle cell dynamics in the developing Drosophila egg chamber.
abstract: 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.
authors.affiliation: Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD 21218.
authors.forename: Sarita
authors.initials: S
authors.lastname: Koride
authors.affiliation: Howard Hughes Medical Institute, Department of Genetics, Harvard Medical School, Boston, MA 02115.
authors.forename: Li
authors.initials: L
authors.lastname: He
authors.affiliation: Department of Physics, George Washington University, Washington, DC 20052.
authors.forename: Li-Ping
authors.initials: LP
authors.lastname: Xiong
authors.affiliation: Department of Physics, George Washington University, Washington, DC 20052.
authors.forename: Ganhui
authors.initials: G
authors.lastname: Lan
authors.affiliation: Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA 93106.
authors.forename: Denise J
authors.initials: DJ
authors.lastname: Montell
authors.affiliation: Johns Hopkins Physical Sciences-Oncology Center, Johns Hopkins University, Baltimore, MD 21218 Department of Mechanical Engineering, Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21218 ssun@jhu.edu.
authors.forename: Sean X
authors.initials: SX
authors.lastname: Sun
mesh_terms: D000818:Animals; D001696:Biomechanical Phenomena; D048429:Cell Size; D004331:Drosophila melanogaster / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D005260:Female; D015870:Gene Expression; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D040542:Mechanotransduction, Cellular / Q000235:genetics*; D008954:Models, Biological; D009024:Morphogenesis / Q000235:genetics*; D009218:Myosins / Q000235:genetics* / Q000378:metabolism; D009866:Oogenesis / Q000235:genetics; D009929:Organ Size; D006080:Ovarian Follicle / Q000166:cytology / Q000254:growth & development / Q000378:metabolism; D015053:Zygote / Q000254:growth & development / Q000378:metabolism*; D054460:rho-Associated Kinases / Q000235:genetics / Q000378:metabolism
chemical_list: D019476:Insect Proteins; D054460:rho-Associated Kinases; D009218:Myosins