Topological progression in proliferating epithelia is driven by a unique variation in polygon distribution

• Published in: PloS one Vol. 8; no. 11; p. e79227
• Main Authors: Sánchez-Gutiérrez, Daniel, Sáez, Aurora, Pascual, Alberto, Escudero, Luis M
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 05-11-2013; Public Library of Science (PLoS)
• Subjects: Algorithms; Analysis of Variance; Animals; Cell Division; Cell Polarity; Cell Proliferation; Cell Shape; Computer Simulation; Developmental stages; Divergence; Drosophila; Drosophila - cytology; Drosophila - growth & development; Epithelial cells; Epithelial Cells - cytology; Epithelium; Epithelium - growth & development; Imaginal Discs - growth & development; Insects; Larva - growth & development; Larvae; Models, Biological; Morphogenesis; Polarity; Principal Component Analysis; Pupa - growth & development; Social networks; Variation; Wings, Animal - cytology; Wings, Animal - growth & development; Spain
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0079227

Morphogenesis is consequence of lots of small coordinated variations that occur during development. In proliferating stages, tissue growth is coupled to changes in shape and organization. A number of studies have analyzed the topological properties of proliferating epithelia using the Drosophila wing disc as a model. These works are based in the existence of a fixed distribution of these epithelial cells according to their number of sides. Cell division, cell rearrangements or a combination of both mechanisms have been proposed to be responsible for this polygonal assembling. Here, we have used different system biology methods to compare images from two close proliferative stages that present high morphological similarity. This approach enables us to search for traces of epithelial organization. First, we show that geometrical and network characteristics of individual cells are mainly dependent on their number of sides. Second, we find a significant divergence between the distribution of polygons in epithelia from mid-third instar larva versus early prepupa. We show that this alteration propagates into changes in epithelial organization. Remarkably, only the variation in polygon distribution driven by morphogenesis leads to progression in epithelial organization. In addition, we identify the relevant features that characterize these rearrangements. Our results reveal signs of epithelial homogenization during the growing phase, before the planar cell polarity pathway leads to the hexagonal packing of the epithelium during pupal stages.