Signals from the brain and olfactory epithelium control shaping of the mammalian nasal capsule cartilage

  1. Marketa Kaucka
  2. Julian Petersen
  3. Marketa Tesarova
  4. Bara Szarowska
  5. Maria Eleni Kastriti
  6. Meng Xie
  7. Anna Kicheva
  8. Karl Annusver
  9. Maria Kasper
  10. Orsolya Symmons
  11. Leslie Pan
  12. Francois Spitz
  13. Jozef Kaiser
  14. Maria Hovorakova
  15. Tomas Zikmund
  16. Kazunori Sunadome
  17. Michael P Matise
  18. Hui Wang
  19. Ulrika Marklund
  20. Hind Abdo
  21. Patrik Ernfors
  22. Pascal Maire
  23. Maud Wurmser
  24. Andrei S Chagin
  25. Kaj Fried
  26. Igor Adameyko  Is a corresponding author
  1. Karolinska Institutet, Sweden
  2. Brno University of Technology, Czech Republic
  3. Medical University of Vienna, Austria
  4. Institute of Science and Technology, Austria
  5. University of Pennsylvania, United States
  6. European Molecular Biology Laboratory, Germany
  7. The Czech Academy of Sciences, Czech Republic
  8. Rutgers-Robert Wood Johnson Medical School, United States
  9. Institute Cochin, France

Abstract

Facial shape is the basis for facial recognition and categorization. Facial features reflect the underlying geometry of the skeletal structures. Here we reveal that cartilaginous nasal capsule (corresponding to upper jaw and face) is shaped by signals generated by neural structures: brain and olfactory epithelium. Brain-derived Sonic Hedgehog (SHH) enables the induction of nasal septum and posterior nasal capsule, whereas the formation of a capsule roof is controlled by signals from the olfactory epithelium. Unexpectedly, the cartilage of the nasal capsule turned out to be important for shaping membranous facial bones during development. This suggests that conserved neurosensory structures could benefit from protection and have evolved signals inducing cranial cartilages encasing them. Experiments with mutant mice revealed that the genomic regulatory regions controlling production of SHH in the nervous system contribute to facial cartilage morphogenesis, which might be a mechanism responsible for the adaptive evolution of animal faces and snouts.

Data availability

All data obtained including tomographic reconstructions will be freely available upon request since some datasets are considerably heavy (1TB and more) and depositing the full data is unfeasible. We have made a subset of the datasets available on the Dryad Digital Repository (http://datadryad.org/review?doi=doi:10.5061/dryad.f1s76f2).

The following data sets were generated

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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8781-9769
  2. Julian Petersen

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    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. Bara Szarowska

    Department of Molecular Neurosciences, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Maria Eleni Kastriti

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. Meng Xie

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  7. Anna Kicheva

    Institute of Science and Technology, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  8. Karl Annusver

    Department of Biosciences and Nutrition, Karolinska Institutet, Huddinge, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  9. Maria Kasper

    Department of Biosciences and Nutrition, Karolinska Institutet, Huddinge, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  10. Orsolya Symmons

    Department of Bioengineering, University of Pennsylvania, Pennsylvania, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Leslie Pan

    Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Francois Spitz

    Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Jozef Kaiser

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  14. Maria Hovorakova

    Department of Developmental Biology, The Czech Academy of Sciences, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  15. Tomas Zikmund

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  16. Kazunori Sunadome

    Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  17. Michael P Matise

    Department of Neuroscience and Cell Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. Hui Wang

    Department of Neuroscience and Cell Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, United States
    Competing interests
    The authors declare that no competing interests exist.
  19. Ulrika Marklund

    Department of Medical Biochemistry and Biophysics, 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:" 0000-0003-1426-1271
  20. Hind Abdo

    Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  21. Patrik Ernfors

    Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  22. Pascal Maire

    Department of Development, Reproduction and Cancer, Institute Cochin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  23. Maud Wurmser

    Department of Development, Reproduction and Cancer, Institute Cochin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  24. 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
  25. Kaj Fried

    Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  26. 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

Vetenskapsrådet

  • Julian Petersen
  • Andrei S Chagin
  • Igor Adameyko

Svenska Sällskapet för Medicinsk Forskning

  • Marketa Kaucka

Bertil Hållstens Forskningsstiftelse

  • Igor Adameyko

Åke Wiberg Stiftelse

  • Igor Adameyko

Karolinska Institutet

  • Ulrika Marklund
  • Andrei S Chagin
  • Kaj Fried
  • Igor Adameyko

Ministerstvo Vnitra České Republiky

  • Marketa Tesarova
  • Tomas Zikmund

Central European Institute of Technology

  • Marketa Tesarova
  • Tomas Zikmund

Grantová Agentura České Republiky

  • Maria Hovorakova

H2020 European Research Council (680037)

  • Anna Kicheva

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 work was approved and permitted by the Local Ethical Committee on Animal Experiments (North Stockholm Animal Ethics Committee) and conducted according to The Swedish Animal Agency´s Provisions and Guidelines for Animal Experimentation recommendations. Permit numbers S40/13 and N226/15, granted by South Stockholm Animal Ethics Committee.The part, which was done in Austria at the Medical University of Vienna and IST was performed in accordance with license BMWFW-66.018/0006-WF/V/3b/2016 and BMWFW-66.009/0163-WF/V/3b/2016 granted by the Austrian BMWFW.

Reviewing Editor

  1. Richard M White, Memorial Sloan Kettering Cancer Center, United States

Publication history

  1. Received: December 19, 2017
  2. Accepted: June 12, 2018
  3. Accepted Manuscript published: June 13, 2018 (version 1)
  4. Version of Record published: June 26, 2018 (version 2)
  5. Version of Record updated: June 29, 2018 (version 3)

Copyright

© 2018, Kaucka et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Marketa Kaucka
  2. Julian Petersen
  3. Marketa Tesarova
  4. Bara Szarowska
  5. Maria Eleni Kastriti
  6. Meng Xie
  7. Anna Kicheva
  8. Karl Annusver
  9. Maria Kasper
  10. Orsolya Symmons
  11. Leslie Pan
  12. Francois Spitz
  13. Jozef Kaiser
  14. Maria Hovorakova
  15. Tomas Zikmund
  16. Kazunori Sunadome
  17. Michael P Matise
  18. Hui Wang
  19. Ulrika Marklund
  20. Hind Abdo
  21. Patrik Ernfors
  22. Pascal Maire
  23. Maud Wurmser
  24. Andrei S Chagin
  25. Kaj Fried
  26. Igor Adameyko
(2018)
Signals from the brain and olfactory epithelium control shaping of the mammalian nasal capsule cartilage
eLife 7:e34465.
https://doi.org/10.7554/eLife.34465

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