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Published October 10, 2017 | Published
Journal Article Open

Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage

Abstract

Both oriented cell divisions and cell rearrangements are critical for proper embryogenesis and organogenesis. However, little is known about how these two cellular events are integrated. Here we examine the linkage between these processes in chick limb cartilage. By combining retroviral-based multicolor clonal analysis with live imaging, the results show that single chondrocyte precursors can generate both single-column and multi-column clones through oriented division followed by cell rearrangements. Focusing on single column formation, we show that this stereotypical tissue architecture is established by a pivot-like process between sister cells. After mediolateral cell division, N-cadherin is enriched in the post-cleavage furrow; then one cell pivots around the other, resulting in stacking into a column. Perturbation analyses demonstrate that planar cell polarity signaling enables cells to pivot in the direction of limb elongation via this N-cadherin-mediated coupling. Our work provides new insights into the mechanisms generating appropriate tissue architecture of limb skeleton.

Additional Information

© 2017 Copyright Li et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 14 November 2016; Accepted: 15 September 2017; Published: 10 October 2017. This project is supported by DE024157 to MEB We thank Professor Carlos Lois, Professor Cheng-Ming Chuong and Caltech Biological Imaging Facility for sharing equipment. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Competing interests: Marianne Bronner: Senior Editor, eLife. The other authors declare that no competing interests exist. Author contributions: Yuwei Li, Conceived and designed the project, Constructed reagents and performed experiments, Performed quantitative analyses, Wrote the manuscript; Ang Li, Performed quantitative and statistical analysis, Helpful discussion; Jason Junge, Performed bioinformatic analyses of Frizzled-7 and Dishevelled-2 proteins, Helpful discussion; Marianne Bronner, Funding acquisition, Conceived and designed the project, Wrote the manuscript.

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August 19, 2023
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