Abstract
Reciprocal interactions between epithelial and neural crest-derived mesenchymal cells have been recognized in the evolutionary modulation of tetrapod odontodes, skeletal structures that include the teeth and tooth-integrated basal tissue. Using cell-tracking experiments, it has been demonstrated that mandibular neural crest cells, labelled during migration, extensively populate dental papillae of all tooth phenotypes of the lobe-finned fish, the Australian lungfish (Neoceratodus forsteri). Here, I report on an extension of this experimental study that earliest migrating NC cells are able to differentiate into odontogenic ectomesenchyme. Using vital dye cell-tracking to mark the mesencephalic neural crest prior to migration, I have found that the corresponding population of earliest migratory cells selectively relocated to dental papillae of both temporary and permanent dentitions of Neoceratodus. I noticed a gradient in distribution of the labelled cells which populated posterior teeth, pterygoid and prearticular (including associated trabecular and Meckelian cartilages; major relocation) much more densely than those in anterior marginal positions, temporary and vomeral permanent teeth (minor relocation). Contrary to mice and zebrafish, the odontogenic potency of mesencephalic neural crest cells is already programmed at the onset of the migration event in lungfish. This may imply that the morphogenic potential of mesencephalic neural crest cells to form teeth has been heterochronically shifted and constrained to later migratory populations of neural crest cells during the developmental evolution of derived tetrapods, or/and arrested in their expression in the oral development of some modern osteichthyans.
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All images documenting the experiment are housed at the Center for Interdisciplinary Biosciences of the Pavol Jozef Šafárik University in Košice, Slovak Republic.
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Acknowledgements
I thank Prof. Jean Joss for her support of my experimentation using lungfish embryos, Debra Birch for her assistance with the confocal microscope and Libby Eyre for collection of lungfish eggs. I also thank the anonymous reviewers for their helpful comments and suggestions on an earlier version of this article. I am grateful to Janet Ahlberg, a professional editor and translator, for her kind help with improving the grammar of the revised manuscript. Finally, I would like to thank to my family for support and to dedicate this article in honor of my father.
Funding
This project was supported by a Macquarie University Research Development grant, the project “Open scientific community for modern interdisciplinary research in medicine” (OPENMED), ITMS2014 + : 313011V455, supported by the Operational Programme Integrated Infrastructure, funded by the European Regional Development Fund, and by the Slovak Research and Development Agency (APVV-18–0251).
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M.K. designed the study, carried out experiments and wrote the paper.
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All experimental procedures were conducted according to protocols approved by Macquarie University´s Animal Ethics Committee (AEC approval # 2003–001).
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Communicated by: Robert Reisz
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Kundrát, M. Earliest migratory cephalic NC cells are potent to differentiate into dental ectomesenchyme of the two lungfish dentitions: tetrapodomorph ancestral condition of unconstrained capability of mesencephalic NC cells to form oral teeth. Sci Nat 108, 37 (2021). https://doi.org/10.1007/s00114-021-01750-0
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DOI: https://doi.org/10.1007/s00114-021-01750-0