Computer simulation of cellular patterning within the Drosophila pupal eye.
We present a computer simulation and associated experimental validation of assembly of glial-like support cells into the interweaving hexagonal lattice that spans the Drosophila pupal eye. This process of cell movements organizes the ommatidial array into a functional pattern. Unlike earlier simulations that focused on the arrangements of cells within individual ommatidia, here we examine the local movements that lead to large-scale organization of the emerging eye field. Simulations based on our experimental observations of cell adhesion, cell death, and cell movement successfully patterned a tracing of an emerging wild-type pupal eye. Surprisingly, altering cell adhesion had only a mild effect on patterning, contradicting our previous hypothesis that the patterning was primarily the result of preferential adhesion between IRM-class surface proteins. Instead, our simulations highlighted the importance of programmed cell death (PCD) as well as a previously unappreciated variable: the expansion of cells' apical surface areas, which promoted rearrangement of neighboring cells. We tested this prediction experimentally by preventing expansion in the apical area of individual cells: patterning was disrupted in a manner predicted by our simulations. Our work demonstrates the value of combining computer simulation with in vivo experiments to uncover novel mechanisms that are perpetuated throughout the eye field. It also demonstrates the utility of the Glazier-Graner-Hogeweg model (GGH) for modeling the links between local cellular interactions and emergent properties of developing epithelia as well as predicting unanticipated results in vivo.
Larson
David E
DE
The Genome Center at Washington University, St. Louis, Missouri, United States of America.
Johnson
Ruth I
RI
Swat
Maciej
M
Cordero
Julia B
JB
Glazier
James A
JA
Cagan
Ross L
RL
D000818:Animals; D017209:Apoptosis / Q000235:genetics / Q000502:physiology; D002448:Cell Adhesion; D002465:Cell Movement; D049109:Cell Proliferation; D054910:Compound Eye, Arthropod / Q000166:cytology / Q000254:growth & development / Q000648:ultrastructure; D003198:Computer Simulation; D004330:Drosophila / Q000254:growth & development*; D046529:Microscopy, Electron, Transmission; D008954:Models, Biological; D009024:Morphogenesis / Q000502:physiology*; D009154:Mutation; D011679:Pupa / Q000254:growth & development*; D013499:Surface Properties