Interplay of cell shape and division orientation promotes robust morphogenesis of developing epithelia.

Journal Article (Journal Article)

Epithelial cells acquire functionally important shapes (e.g., squamous, cuboidal, columnar) during development. Here, we combine theory, quantitative imaging, and perturbations to analyze how tissue geometry, cell divisions, and mechanics interact to shape the presumptive enveloping layer (pre-EVL) on the zebrafish embryonic surface. We find that, under geometrical constraints, pre-EVL flattening is regulated by surface cell number changes following differentially oriented cell divisions. The division pattern is, in turn, determined by the cell shape distribution, which forms under geometrical constraints by cell-cell mechanical coupling. An integrated mathematical model of this shape-division feedback loop recapitulates empirical observations. Surprisingly, the model predicts that cell shape is robust to changes of tissue surface area, cell volume, and cell number, which we confirm in vivo. Further simulations and perturbations suggest the parameter linking cell shape and division orientation contributes to epithelial diversity. Together, our work identifies an evolvable design logic that enables robust cell-level regulation of tissue-level development.

Full Text

Duke Authors

Cited Authors

  • Xiong, F; Ma, W; Hiscock, TW; Mosaliganti, KR; Tentner, AR; Brakke, KA; Rannou, N; Gelas, A; Souhait, L; Swinburne, IA; Obholzer, ND; Megason, SG

Published Date

  • October 2014

Published In

Volume / Issue

  • 159 / 2

Start / End Page

  • 415 - 427

PubMed ID

  • 25303534

Pubmed Central ID

  • PMC4273647

Electronic International Standard Serial Number (EISSN)

  • 1097-4172

International Standard Serial Number (ISSN)

  • 0092-8674

Digital Object Identifier (DOI)

  • 10.1016/j.cell.2014.09.007

Language

  • eng