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Research Article

Mechanical constraint from growing jaw facilitates mammalian dental diversity

Elodie Renvoisé, Kathryn D. Kavanagh, Vincent Lazzari, Teemu J. Häkkinen, Ritva Rice, Sophie Pantalacci, Isaac Salazar-Ciudad, and Jukka Jernvall
  1. aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland;
  2. bBiology Department, University of Massachusetts Dartmouth, Dartmouth, MA 02747;
  3. cInstitut de Paleoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironments, UMR CNRS 7262, University of Poitiers, 86022 Poitiers cedex, France;
  4. dUnivLyon, École Normale Supérieure de Lyon, University Claude Bernard, CNRS UMR 5239, INSERM U1210, Laboratoire de Biologie et Modélisation de la Cellule, F-69007 Lyon, France;
  5. eDepartament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain

See allHide authors and affiliations

PNAS August 29, 2017 114 (35) 9403-9408; first published August 14, 2017; https://doi.org/10.1073/pnas.1707410114
Elodie Renvoisé
aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland;
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  • For correspondence: jernvall@fastmail.fm erenvoise@yahoo.fr
Kathryn D. Kavanagh
bBiology Department, University of Massachusetts Dartmouth, Dartmouth, MA 02747;
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Vincent Lazzari
cInstitut de Paleoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironments, UMR CNRS 7262, University of Poitiers, 86022 Poitiers cedex, France;
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Teemu J. Häkkinen
aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland;
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Ritva Rice
aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland;
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Sophie Pantalacci
dUnivLyon, École Normale Supérieure de Lyon, University Claude Bernard, CNRS UMR 5239, INSERM U1210, Laboratoire de Biologie et Modélisation de la Cellule, F-69007 Lyon, France;
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Isaac Salazar-Ciudad
aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland;
eDepartament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain
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Jukka Jernvall
aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland;
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  • For correspondence: jernvall@fastmail.fm erenvoise@yahoo.fr
  1. Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved July 17, 2017 (received for review May 9, 2017)

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Significance

Good examples of the relative autonomy of organ development are teeth, and for decades researchers have cultured isolated mouse teeth on a petri dish by starting from the earliest recognizable stage. We have cultured cheek teeth of voles, another species of rodent, and show how the cultured vole teeth lack their species-specific morphology. Based on computational modeling, 3D imaging, and experiments in which we culture mouse and vole teeth between microscopic braces, we suggest that the development of vole tooth shape requires the lateral support of the jaw. Because mice lack the vole-specific morphology, the requirement of the jaw for tooth shape has not been possible to uncover previously. Comparative studies are required for the understanding of organogenesis.

Abstract

Much of the basic information about individual organ development comes from studies using model species. Whereas conservation of gene regulatory networks across higher taxa supports generalizations made from a limited number of species, generality of mechanistic inferences remains to be tested in tissue culture systems. Here, using mammalian tooth explants cultured in isolation, we investigate self-regulation of patterning by comparing developing molars of the mouse, the model species of mammalian research, and the bank vole. A distinct patterning difference between the vole and the mouse molars is the alternate cusp offset present in the vole. Analyses of both species using 3D reconstructions of developing molars and jaws, computational modeling of cusp patterning, and tooth explants cultured with small braces show that correct cusp offset requires constraints on the lateral expansion of the developing tooth. Vole molars cultured without the braces lose their cusp offset, and mouse molars cultured with the braces develop a cusp offset. Our results suggest that cusp offset, which changes frequently in mammalian evolution, is more dependent on the 3D support of the developing jaw than other aspects of tooth shape. This jaw–tooth integration of a specific aspect of the tooth phenotype indicates that organs may outsource specific aspects of their morphology to be regulated by adjacent body parts or organs. Comparative studies of morphologically different species are needed to infer the principles of organogenesis.

  • evodevo
  • patterning
  • odontogenesis
  • diversity
  • tissue engineering

Footnotes

  • ↵1To whom correspondence may be addressed. Email: jernvall{at}fastmail.fm or erenvoise{at}yahoo.fr.
  • Author contributions: E.R., K.D.K., and J.J. designed research; E.R., K.D.K., V.L., T.J.H., R.R., S.P., I.S.-C., and J.J. performed research; V.L., T.J.H., R.R., S.P., and I.S.-C. contributed new reagents/analytic tools; E.R., K.D.K., V.L., and J.J. analyzed data; and E.R., K.D.K., and J.J. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1707410114/-/DCSupplemental.

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Mechanical constraint and dental diversity
Elodie Renvoisé, Kathryn D. Kavanagh, Vincent Lazzari, Teemu J. Häkkinen, Ritva Rice, Sophie Pantalacci, Isaac Salazar-Ciudad, Jukka Jernvall
Proceedings of the National Academy of Sciences Aug 2017, 114 (35) 9403-9408; DOI: 10.1073/pnas.1707410114

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Mechanical constraint and dental diversity
Elodie Renvoisé, Kathryn D. Kavanagh, Vincent Lazzari, Teemu J. Häkkinen, Ritva Rice, Sophie Pantalacci, Isaac Salazar-Ciudad, Jukka Jernvall
Proceedings of the National Academy of Sciences Aug 2017, 114 (35) 9403-9408; DOI: 10.1073/pnas.1707410114
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Proceedings of the National Academy of Sciences: 114 (35)
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