Cargando…

Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system

BACKGROUND: The gene regulatory network involved in tooth morphogenesis has been extremely well described in mammals and its modeling has allowed predictions of variations in regulatory pathway that may have led to evolution of tooth shapes. However, very little is known outside of mammals to unders...

Descripción completa

Detalles Bibliográficos
Autores principales: Debiais-Thibaud, Mélanie, Chiori, Roxane, Enault, Sébastien, Oulion, Silvan, Germon, Isabelle, Martinand-Mari, Camille, Casane, Didier, Borday-Birraux, Véronique
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4690397/
https://www.ncbi.nlm.nih.gov/pubmed/26704180
http://dx.doi.org/10.1186/s12862-015-0557-0
_version_ 1782407012285415424
author Debiais-Thibaud, Mélanie
Chiori, Roxane
Enault, Sébastien
Oulion, Silvan
Germon, Isabelle
Martinand-Mari, Camille
Casane, Didier
Borday-Birraux, Véronique
author_facet Debiais-Thibaud, Mélanie
Chiori, Roxane
Enault, Sébastien
Oulion, Silvan
Germon, Isabelle
Martinand-Mari, Camille
Casane, Didier
Borday-Birraux, Véronique
author_sort Debiais-Thibaud, Mélanie
collection PubMed
description BACKGROUND: The gene regulatory network involved in tooth morphogenesis has been extremely well described in mammals and its modeling has allowed predictions of variations in regulatory pathway that may have led to evolution of tooth shapes. However, very little is known outside of mammals to understand how this regulatory framework may also account for tooth shape evolution at the level of gnathostomes. In this work, we describe expression patterns and proliferation/apoptosis assays to uncover homologous regulatory pathways in the catshark Scyliorhinus canicula. RESULTS: Because of their similar structural and developmental features, gene expression patterns were described over the four developmental stages of both tooth and scale buds in the catshark. These gene expression patterns differ from mouse tooth development, and discrepancies are also observed between tooth and scale development within the catshark. However, a similar nested expression of Shh and Fgf suggests similar signaling involved in morphogenesis of all structures, although apoptosis assays do not support a strictly equivalent enamel knot system in sharks. Similarities in the topology of gene expression pattern, including Bmp signaling pathway, suggest that mouse molar development is more similar to scale bud development in the catshark. CONCLUSIONS: These results support the fact that no enamel knot, as described in mammalian teeth, can be described in the morphogenesis of shark teeth or scales. However, homologous signaling pathways are involved in growth and morphogenesis with variations in their respective expression patterns. We speculate that variations in this topology of expression are also a substrate for tooth shape evolution, notably in regulating the growth axis and symmetry of the developing structure. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0557-0) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4690397
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-46903972015-12-25 Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system Debiais-Thibaud, Mélanie Chiori, Roxane Enault, Sébastien Oulion, Silvan Germon, Isabelle Martinand-Mari, Camille Casane, Didier Borday-Birraux, Véronique BMC Evol Biol Research Article BACKGROUND: The gene regulatory network involved in tooth morphogenesis has been extremely well described in mammals and its modeling has allowed predictions of variations in regulatory pathway that may have led to evolution of tooth shapes. However, very little is known outside of mammals to understand how this regulatory framework may also account for tooth shape evolution at the level of gnathostomes. In this work, we describe expression patterns and proliferation/apoptosis assays to uncover homologous regulatory pathways in the catshark Scyliorhinus canicula. RESULTS: Because of their similar structural and developmental features, gene expression patterns were described over the four developmental stages of both tooth and scale buds in the catshark. These gene expression patterns differ from mouse tooth development, and discrepancies are also observed between tooth and scale development within the catshark. However, a similar nested expression of Shh and Fgf suggests similar signaling involved in morphogenesis of all structures, although apoptosis assays do not support a strictly equivalent enamel knot system in sharks. Similarities in the topology of gene expression pattern, including Bmp signaling pathway, suggest that mouse molar development is more similar to scale bud development in the catshark. CONCLUSIONS: These results support the fact that no enamel knot, as described in mammalian teeth, can be described in the morphogenesis of shark teeth or scales. However, homologous signaling pathways are involved in growth and morphogenesis with variations in their respective expression patterns. We speculate that variations in this topology of expression are also a substrate for tooth shape evolution, notably in regulating the growth axis and symmetry of the developing structure. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0557-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-24 /pmc/articles/PMC4690397/ /pubmed/26704180 http://dx.doi.org/10.1186/s12862-015-0557-0 Text en © Debiais-Thibaud et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Debiais-Thibaud, Mélanie
Chiori, Roxane
Enault, Sébastien
Oulion, Silvan
Germon, Isabelle
Martinand-Mari, Camille
Casane, Didier
Borday-Birraux, Véronique
Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
title Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
title_full Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
title_fullStr Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
title_full_unstemmed Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
title_short Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
title_sort tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4690397/
https://www.ncbi.nlm.nih.gov/pubmed/26704180
http://dx.doi.org/10.1186/s12862-015-0557-0
work_keys_str_mv AT debiaisthibaudmelanie toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT chioriroxane toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT enaultsebastien toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT oulionsilvan toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT germonisabelle toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT martinandmaricamille toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT casanedidier toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem
AT bordaybirrauxveronique toothandscalemorphogenesisinsharkanalternativeprocesstothemammalianenamelknotsystem