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

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 multic...

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Main Authors: Yuwei Li, Ang Li, Jason Junge, Marianne Bronner
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/23279
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author Yuwei Li
Ang Li
Jason Junge
Marianne Bronner
author_facet Yuwei Li
Ang Li
Jason Junge
Marianne Bronner
author_sort Yuwei Li
collection DOAJ
description 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.
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spelling doaj.art-4518e37c94fc401b9cba33b61c98ac592022-12-22T04:32:35ZengeLife Sciences Publications LtdeLife2050-084X2017-10-01610.7554/eLife.23279Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilageYuwei Li0https://orcid.org/0000-0001-7753-4869Ang Li1Jason Junge2Marianne Bronner3https://orcid.org/0000-0003-4274-1862Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United StatesDepartment of Pathology, University of Southern California, Keck School of Medicine, Los Angeles, United StatesTranslational Imaging Center, University of Southern California, Los Angeles, United StatesDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, United StatesBoth 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.https://elifesciences.org/articles/23279cell polarityplanar cell polarity signalingcartilage development
spellingShingle Yuwei Li
Ang Li
Jason Junge
Marianne Bronner
Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
eLife
cell polarity
planar cell polarity signaling
cartilage development
title Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
title_full Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
title_fullStr Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
title_full_unstemmed Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
title_short Planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
title_sort planar cell polarity signaling coordinates oriented cell division and cell rearrangement in clonally expanding growth plate cartilage
topic cell polarity
planar cell polarity signaling
cartilage development
url https://elifesciences.org/articles/23279
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AT angli planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage
AT jasonjunge planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage
AT mariannebronner planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage