A dynamic cell adhesion surface regulates tissue architecture in growth plate cartilage

Sarah M. Romereim, Nicholas H. Conoan, Baojiang Chen, Andrew T Dudley

Research output: Contribution to journalArticle

26 Citations (Scopus)

Abstract

The architecture and morphogenetic properties of tissues are founded in the tissue-specific regulation of cell behaviors. In endochondral bones, the growth plate cartilage promotes bone elongation via regulated chondrocyte maturation within an ordered, three-dimensional cell array. A key event in the process that generates this cell array is the transformation of disordered resting chondrocytes into clonal columns of discoid proliferative cells aligned with the primary growth vector. Previous analysis showed that column-forming chondrocytes display planar cell divisions, and the resulting daughter cells rearrange by ~90° to align with the lengthening column. However, these previous studies provided limited information about the mechanisms underlying this dynamic process. Here we present new mechanistic insights generated by application of a novel time-lapse confocal microscopy method along with immunofluorescence and electron microscopy. We show that, during cell division, daughter chondrocytes establish a cell-cell adhesion surface enriched in cadherins and β-catenin. Rearrangement into columns occurs concomitant with expansion of this adhesion surface in a process more similar to cell spreading than to migration. Column formation requires cell-cell adhesion, as reducing cadherin binding via chelation of extracellular calcium inhibits chondrocyte rearrangement. Importantly, physical indicators of cell polarity, such as cell body alignment, are not prerequisites for oriented cell behavior. Our results support a model in which regulation of adhesive surface dynamics and cortical tension by extrinsic signaling modifies the thermodynamic landscape to promote organization of daughter cells in the context of the three-dimensional growth plate tissue.

Original languageEnglish (US)
Pages (from-to)2085-2095
Number of pages11
JournalDevelopment (Cambridge)
Volume141
Issue number10
DOIs
StatePublished - 2014

Fingerprint

Growth Plate
Cell Adhesion
Cartilage
Chondrocytes
Cadherins
Cell Division
Bone Plates
Catenins
Cell Polarity
Bone Development
Thermodynamics
Fluorescence Microscopy
Confocal Microscopy
Adhesives
Electron Microscopy
Calcium
Bone and Bones

Keywords

  • Adhesion
  • Chondrogenesis
  • Mouse
  • Polarity

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology

Cite this

A dynamic cell adhesion surface regulates tissue architecture in growth plate cartilage. / Romereim, Sarah M.; Conoan, Nicholas H.; Chen, Baojiang; Dudley, Andrew T.

In: Development (Cambridge), Vol. 141, No. 10, 2014, p. 2085-2095.

Research output: Contribution to journalArticle

Romereim, Sarah M. ; Conoan, Nicholas H. ; Chen, Baojiang ; Dudley, Andrew T. / A dynamic cell adhesion surface regulates tissue architecture in growth plate cartilage. In: Development (Cambridge). 2014 ; Vol. 141, No. 10. pp. 2085-2095.
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