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Altered developmental programs and oriented cell divisions lead to bulky bones during salamander limb regeneration

Author

Listed:
  • Marketa Kaucka

    (Max Planck Institute for Evolutionary Biology)

  • Alberto Joven Araus

    (Karolinska Institute)

  • Marketa Tesarova

    (Brno University of Technology)

  • Joshua D. Currie

    (Wake Forest University)

  • Johan Boström

    (Medical University Vienna)

  • Michaela Kavkova

    (Brno University of Technology)

  • Julian Petersen

    (Medical University Vienna
    University of Leipzig Medical Center)

  • Zeyu Yao

    (Karolinska Institute)

  • Anass Bouchnita

    (Uppsala University
    The University of Texas at El Paso)

  • Andreas Hellander

    (Uppsala University)

  • Tomas Zikmund

    (Brno University of Technology)

  • Ahmed Elewa

    (Karolinska Institute
    University of Barcelona)

  • Phillip T. Newton

    (Karolinska Institute
    Astrid Lindgren Children’s Hospital, Karolinska University Hospital)

  • Ji-Feng Fei

    (The Research Institute of Molecular Pathology (IMP)
    Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences)

  • Andrei S. Chagin

    (Karolinska Institutet
    University of Gothenburg)

  • Kaj Fried

    (Karolinska Institute)

  • Elly M. Tanaka

    (The Research Institute of Molecular Pathology (IMP))

  • Jozef Kaiser

    (Brno University of Technology)

  • András Simon

    (Karolinska Institute)

  • Igor Adameyko

    (Medical University Vienna
    Karolinska Institutet)

Abstract

There are major differences in duration and scale at which limb development and regeneration proceed, raising the question to what extent regeneration is a recapitulation of development. We address this by analyzing skeletal elements using a combination of micro-CT imaging, molecular profiling and clonal cell tracing. We find that, in contrast to development, regenerative skeletal growth is accomplished based entirely on cartilage expansion prior to ossification, not limiting the transversal cartilage expansion and resulting in bulkier skeletal parts. The oriented extension of salamander cartilage and bone appear similar to the development of basicranial synchondroses in mammals, as we found no evidence for cartilage stem cell niches or growth plate-like structures during neither development nor regeneration. Both regenerative and developmental ossification in salamanders start from the cortical bone and proceeds inwards, showing the diversity of schemes for the synchrony of cortical and endochondral ossification among vertebrates.

Suggested Citation

  • Marketa Kaucka & Alberto Joven Araus & Marketa Tesarova & Joshua D. Currie & Johan Boström & Michaela Kavkova & Julian Petersen & Zeyu Yao & Anass Bouchnita & Andreas Hellander & Tomas Zikmund & Ahmed, 2022. "Altered developmental programs and oriented cell divisions lead to bulky bones during salamander limb regeneration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34266-w
    DOI: 10.1038/s41467-022-34266-w
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    References listed on IDEAS

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    1. Phillip T. Newton & Lei Li & Baoyi Zhou & Christoph Schweingruber & Maria Hovorakova & Meng Xie & Xiaoyan Sun & Lakshmi Sandhow & Artem V. Artemov & Evgeny Ivashkin & Simon Suter & Vyacheslav Dyachuk , 2019. "A radical switch in clonality reveals a stem cell niche in the epiphyseal growth plate," Nature, Nature, vol. 567(7747), pages 234-238, March.
    2. Henry M. Kronenberg, 2003. "Developmental regulation of the growth plate," Nature, Nature, vol. 423(6937), pages 332-336, May.
    3. Kimberly L. Cooper & Karen E. Sears & Aysu Uygur & Jennifer Maier & Karl-Stephan Baczkowski & Margaret Brosnahan & Doug Antczak & Julian A. Skidmore & Clifford J. Tabin, 2014. "Patterning and post-patterning modes of evolutionary digit loss in mammals," Nature, Nature, vol. 511(7507), pages 41-45, July.
    4. Shawon Debnath & Alisha R. Yallowitz & Jason McCormick & Sarfaraz Lalani & Tuo Zhang & Ren Xu & Na Li & Yifang Liu & Yeon Suk Yang & Mark Eiseman & Jae-Hyuck Shim & Meera Hameed & John H. Healey & Mat, 2018. "Discovery of a periosteal stem cell mediating intramembranous bone formation," Nature, Nature, vol. 562(7725), pages 133-139, October.
    5. Koji Mizuhashi & Wanida Ono & Yuki Matsushita & Naoko Sakagami & Akira Takahashi & Thomas L. Saunders & Takashi Nagasawa & Henry M. Kronenberg & Noriaki Ono, 2018. "Resting zone of the growth plate houses a unique class of skeletal stem cells," Nature, Nature, vol. 563(7730), pages 254-258, November.
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