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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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2017-10-01
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Series: | eLife |
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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. |
first_indexed | 2024-04-11T09:06:58Z |
format | Article |
id | doaj.art-4518e37c94fc401b9cba33b61c98ac59 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-11T09:06:58Z |
publishDate | 2017-10-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT yuweili planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage AT angli planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage AT jasonjunge planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage AT mariannebronner planarcellpolaritysignalingcoordinatesorientedcelldivisionandcellrearrangementinclonallyexpandinggrowthplatecartilage |