Oriented clonal cell dynamics enables accurate growth and shaping of vertebrate cartilage

  1. Marketa Kaucka
  2. Tomas Zikmund
  3. Marketa Tesarova
  4. Daniel Gyllborg
  5. Andreas Hellander
  6. Josef Jaros
  7. Jozef Kaiser
  8. Julian Petersen
  9. Bara Szarowska
  10. Phillip T Newton
  11. Vyacheslav Dyachuk
  12. Lei Li
  13. Hong Qian
  14. Anne-Sofie Johansson
  15. Yuji Mishina
  16. Josh Currie
  17. Elly M Tanaka
  18. Alek Erickson
  19. Andrew Dudley
  20. Hjalmar Brismar
  21. Paul Southam
  22. Enrico Coen
  23. Min Chen
  24. Lee S Weinstein
  25. Ales Hampl
  26. Ernest Arenas
  27. Andrei S Chagin
  28. Kaj Fried  Is a corresponding author
  29. Igor Adameyko  Is a corresponding author
  1. Karolinska Institutet, Sweden
  2. Brno University of Technology, Czech Republic
  3. Uppsala University, Sweden
  4. Masaryk University, Czech Republic
  5. Medical University Vienna, Austria
  6. University of Michigan School of dentistry, United States
  7. Technische Universität Dresden, Germany
  8. University of Nebraska Medical Center, United States
  9. Royal Institute of Technology, Sweden
  10. John Innes Centre, United Kingdom
  11. National Institutes of Health, United States

Abstract

Cartilaginous structures are at the core of embryo growth and shaping before the bone forms. Here we report a novel principle of vertebrate cartilage growth that is based on introducing transversally-oriented clones into pre-existing cartilage. This mechanism of growth uncouples the lateral expansion of curved cartilaginous sheets from the control of cartilage thickness, a process which might be the evolutionary mechanism underlying adaptations of facial shape. In rod-shaped cartilage structures (Meckel, ribs and skeletal elements in developing limbs), the transverse integration of clonal columns determines the well-defined diameter and resulting rod-like morphology. We were able to alter cartilage shape by experimentally manipulating clonal geometries. Using in silico modeling, we discovered that anisotropic proliferation might explain cartilage bending and groove formation at the macro-scale.

Article and author information

Author details

  1. Marketa Kaucka

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  2. Tomas Zikmund

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  3. Marketa Tesarova

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  4. Daniel Gyllborg

    Unit of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Andreas Hellander

    Department of Information Technology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. Josef Jaros

    Department of Histology and Embryology, Medical Faculty, Masaryk University, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  7. Jozef Kaiser

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  8. Julian Petersen

    Center for Brain Research, Medical University Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  9. Bara Szarowska

    Center for Brain Research, Medical University Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  10. Phillip T Newton

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  11. Vyacheslav Dyachuk

    Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  12. Lei Li

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  13. Hong Qian

    Department of Medicine, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  14. Anne-Sofie Johansson

    Department of Medicine, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  15. Yuji Mishina

    Department of Biologic and Materials Sciences, University of Michigan School of dentistry, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Josh Currie

    Center for Regenerative Therapies, Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  17. Elly M Tanaka

    Center for Regenerative Therapies, Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  18. Alek Erickson

    Department of Genetics, Cell Biology and Anatomy, University of Nebraska Medical Center, Omaha, United States
    Competing interests
    The authors declare that no competing interests exist.
  19. Andrew Dudley

    Department of Genetics, Cell Biology and Anatomy, University of Nebraska Medical Center, Omaha, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Hjalmar Brismar

    Science for Life Laboratory, Royal Institute of Technology, Solna, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0578-4003
  21. Paul Southam

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  22. Enrico Coen

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8454-8767
  23. Min Chen

    National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  24. Lee S Weinstein

    National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  25. Ales Hampl

    Department of Histology and Embryology, Medical Faculty, Masaryk University, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  26. Ernest Arenas

    Unit of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  27. Andrei S Chagin

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2696-5850
  28. Kaj Fried

    Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
    For correspondence
    kaj.fried@ki.se
    Competing interests
    The authors declare that no competing interests exist.
  29. Igor Adameyko

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    For correspondence
    igor.adameyko@ki.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5471-0356

Funding

European Molecular Biology Organization (ALTF 216-2013)

  • Marketa Kaucka

Svenska Sällskapet för Medicinsk Forskning

  • Marketa Kaucka

Svenska Forskningsrådet Formas

  • Andreas Hellander
  • Phillip T Newton
  • Andrei S Chagin
  • Kaj Fried
  • Igor Adameyko

Karolinska Institutet

  • Phillip T Newton
  • Andrei S Chagin
  • Kaj Fried
  • Igor Adameyko

Bertil Hållstens Forskningsstiftelse

  • Igor Adameyko

Åke Wiberg Stiftelse

  • Igor Adameyko

National Institutes of Health

  • Andreas Hellander

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal (mouse) work has been approved and permitted by the Ethical Committee on Animal Experiments (Norra Djurförsöksetiska Nämd, ethical permit N226/15 and N5/14) and conducted according to The Swedish Animal Agency´s Provisions and Guidelines for Animal Experimentation recommendations.

Reviewing Editor

  1. Marianne Bronner, California Institute of Technology, United States

Publication history

  1. Received: February 9, 2017
  2. Accepted: April 16, 2017
  3. Accepted Manuscript published: April 17, 2017 (version 1)
  4. Version of Record published: May 4, 2017 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Marketa Kaucka
  2. Tomas Zikmund
  3. Marketa Tesarova
  4. Daniel Gyllborg
  5. Andreas Hellander
  6. Josef Jaros
  7. Jozef Kaiser
  8. Julian Petersen
  9. Bara Szarowska
  10. Phillip T Newton
  11. Vyacheslav Dyachuk
  12. Lei Li
  13. Hong Qian
  14. Anne-Sofie Johansson
  15. Yuji Mishina
  16. Josh Currie
  17. Elly M Tanaka
  18. Alek Erickson
  19. Andrew Dudley
  20. Hjalmar Brismar
  21. Paul Southam
  22. Enrico Coen
  23. Min Chen
  24. Lee S Weinstein
  25. Ales Hampl
  26. Ernest Arenas
  27. Andrei S Chagin
  28. Kaj Fried
  29. Igor Adameyko
(2017)
Oriented clonal cell dynamics enables accurate growth and shaping of vertebrate cartilage
eLife 6:e25902.
https://doi.org/10.7554/eLife.25902

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