The alternative regenerative strategy of bearded dragon unveils the key processes underlying vertebrate tooth renewal

  1. Lotta Salomies
  2. Julia Eymann
  3. Imran Khan
  4. Nicolas Di-Poi  Is a corresponding author
  1. University of Helsinki, Finland

Abstract

Deep understanding of tooth regeneration is hampered by the lack of lifelong replacing oral dentition in most conventional models. Here, we show that the bearded dragon, one of the rare vertebrate species with both polyphyodont and monophyodont teeth, constitutes a key model for filling this gap, allowing direct comparison of extreme dentition types. Our developmental and high-throughput transcriptomic data of microdissected dental cells unveils the critical importance of successional dental lamina patterning, in addition to maintenance, for vertebrate tooth renewal. This patterning process happens at various levels, including directional growth but also gene expression levels, dynamics, and regionalization, and involves a large number of yet uncharacterized dental genes. Furthermore, the alternative renewal mechanism of bearded dragon dentition, with dual location of slow-cycling cells, demonstrates the importance of cell migration and functional specialization of putative epithelial stem/progenitor niches in tissue regeneration, while expanding the diversity of dental replacement strategies in vertebrates.

Data availability

All Illumina reads have been deposited on Dryad Digital Repository under the link https://datadryad.org/review?doi=doi:10.5061/dryad.k66jn2s. Primers used for qPCR and ISH probes are available in the Key Resources Table. All other data generated or analyzed during this study are included in the manuscript and Supplementary File 1.

The following data sets were generated

Article and author information

Author details

  1. Lotta Salomies

    Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1518-153X
  2. Julia Eymann

    Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8147-9161
  3. Imran Khan

    Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicolas Di-Poi

    Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    For correspondence
    nicolas.di-poi@helsinki.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3313-3016

Funding

Suomen Akatemia

  • Nicolas Di-Poi

Suomen Akatemia

  • Imran Khan

Integrative Life Science Doctoral Program

  • Lotta Salomies

Helsingin Yliopisto

  • Nicolas Di-Poi

Biocemtrum Helsinki

  • Nicolas Di-Poi

Institute of biotechnology

  • Nicolas Di-Poi

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

Reviewing Editor

  1. Karen E Sears, University of California, Los Angeles, United States

Ethics

Animal experimentation: All reptile captive breedings and experiments were approved by the Laboratory Animal Centre (LAC) of the University of Helsinki and/or the National Animal Experiment Board (ELLA) in Finland (license numbers ESLH-2007-07445/ym-23, ESAVI/7484/04.10.07/2016, and ESAVI/13139/04.10.05/2017).

Version history

  1. Received: April 15, 2019
  2. Accepted: August 16, 2019
  3. Accepted Manuscript published: August 16, 2019 (version 1)
  4. Version of Record published: September 13, 2019 (version 2)

Copyright

© 2019, Salomies 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. Lotta Salomies
  2. Julia Eymann
  3. Imran Khan
  4. Nicolas Di-Poi
(2019)
The alternative regenerative strategy of bearded dragon unveils the key processes underlying vertebrate tooth renewal
eLife 8:e47702.
https://doi.org/10.7554/eLife.47702

Share this article

https://doi.org/10.7554/eLife.47702

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