PUBLICATION

Interplay of Cell Shape and Division Orientation Promotes Robust Morphogenesis of Developing Epithelia

Authors
Xiong, F., Ma, W., Hiscock, T.W., Mosaliganti, K.R., Tentner, A.R., Brakke, K.A., Rannou, N., Gelas, A., Souhait, L., Swinburne, I.A., Obholzer, N.D., Megason, S.G.
ID
ZDB-PUB-141011-2
Date
2014
Source
Cell   159: 415-427 (Journal)
Registered Authors
Gelas, Arnaud, Megason, Sean, Mosaliganti, Kishore, Obholzer, Nikolaus, Souhait, Lydie, Swinburne, Ian, Tentner, Andrea, Xiong, Fengzhu
Keywords
none
MeSH Terms
  • Epithelial Cells/cytology*
  • Cell Count
  • Embryo, Nonmammalian/cytology
  • Models, Biological*
  • Cell Division
  • Morphogenesis*
  • Zebrafish/embryology*
  • Biomechanical Phenomena
  • Animals
  • Cell Shape
(all 10)
PubMed
25303534 Full text @ Cell
Abstract
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.
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Mutations / Transgenics
Allele Construct Type Affected Genomic Region
e112TgTransgenic Insertion
    hm1TgTransgenic Insertion
      hm13TgTransgenic Insertion
        hm15TgTransgenic Insertion
          hm25TgTransgenic Insertion
            hm29TgTransgenic Insertion
              hm30TgTransgenic Insertion
                hm31TgTransgenic Insertion
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                  Target Reagent Reagent Type
                  cdh1MO3-cdh1MRPHLNO
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                  Fish
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                  hm13Tg
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                  hm25Tg
                  hm29Tg
                  hm30Tg
                  hm31Tg
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                  Ab1-tjp1monoclonalIgG1Mouse
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                  Marker Marker Type Name
                  CitrineEFGCitrine
                  EGFPEFGEGFP
                  mCherryEFGmCherry
                  TomatoEFGTomato
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                  Citation
                  Xiong, F., Ma, W., Hiscock, T.W., Mosaliganti, K.R., Tentner, A.R., Brakke, K.A., Rannou, N., Gelas, A., Souhait, L., Swinburne, I.A., Obholzer, N.D., Megason, S.G. (2014) Interplay of Cell Shape and Division Orientation Promotes Robust Morphogenesis of Developing Epithelia. Cell. 159:415-427.