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Published April 2015 | Published + Supplemental Material
Journal Article Open

Dynamic imaging of the growth plate cartilage reveals multiple contributors to skeletal morphogenesis

Abstract

The diverse morphology of vertebrate skeletal system is genetically controlled, yet the means by which cells shape the skeleton remains to be fully illuminated. Here we perform quantitative analyses of cell behaviours in the growth plate cartilage, the template for long bone formation, to gain insights into this process. Using a robust avian embryonic organ culture, we employ time-lapse two-photon laser scanning microscopy to observe proliferative cells' behaviours during cartilage growth, resulting in cellular trajectories with a spreading displacement mainly along the tissue elongation axis. We build a novel software toolkit of quantitative methods to segregate the contributions of various cellular processes to the cellular trajectories. We find that convergent-extension, mitotic cell division, and daughter cell rearrangement do not contribute significantly to the observed growth process; instead, extracellular matrix deposition and cell volume enlargement are the key contributors to embryonic cartilage elongation.

Additional Information

© 2015 Macmillan Publishers Limited. This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 17 November 2014; Accepted 27 February 2015; Published 13 April 2015. We thank Jason Alexander Junge, Masahiro Kitano and Carol Readhead for comments on the manuscript. Alaa I. Abdelhamid, Marcela Artiga, Luca Caneparo, David Huss, Ali Lashgari, Ang Li and Greg Shackleford for discussion and sharing reagents. This work was supported by California Institute of Regenerative Medicine (CIRM) Postdoctoral Fellowship, Dental Research Center at Qassim University (Saudi Arabia), Caltech Biological Imaging Center, the CHLA Translational Biomedical Imaging Laboratory, and the USC Translational Imaging Center. Author contributions: All the authors designed the experiments, and Y.L., T.V.T. and V.T. initiated this project. T.V.T designed the mold for organ culture and helped optimize imaging conditions. Y.L., D.S.K. and T.V.T. performed organ culture and live imaging. V.T. and Y.L. performed quantitative analysis. R.L. constructed the transgenic quail. Y.L. performed all other experiments. Y.L, V.T. and S.E.F. wrote the manuscript.

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Supplemental Material - ncomms7798-s1.pdf

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