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A shift in anterior–posterior positional information underlies the fin-to-limb evolution

The pectoral fins of ancestral fishes had multiple proximal elements connected to their pectoral girdles. During the fin-to-limb transition, anterior proximal elements were lost and only the most posterior one remained as the humerus. Thus, we hypothesised that an evolutionary alteration occurred in...

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Autores principales: Onimaru, Koh, Kuraku, Shigehiro, Takagi, Wataru, Hyodo, Susumu, Sharpe, James, Tanaka, Mikiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4538735/
https://www.ncbi.nlm.nih.gov/pubmed/26283004
http://dx.doi.org/10.7554/eLife.07048
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author Onimaru, Koh
Kuraku, Shigehiro
Takagi, Wataru
Hyodo, Susumu
Sharpe, James
Tanaka, Mikiko
author_facet Onimaru, Koh
Kuraku, Shigehiro
Takagi, Wataru
Hyodo, Susumu
Sharpe, James
Tanaka, Mikiko
author_sort Onimaru, Koh
collection PubMed
description The pectoral fins of ancestral fishes had multiple proximal elements connected to their pectoral girdles. During the fin-to-limb transition, anterior proximal elements were lost and only the most posterior one remained as the humerus. Thus, we hypothesised that an evolutionary alteration occurred in the anterior–posterior (AP) patterning system of limb buds. In this study, we examined the pectoral fin development of catshark (Scyliorhinus canicula) and revealed that the AP positional values in fin buds are shifted more posteriorly than mouse limb buds. Furthermore, examination of Gli3 function and regulation shows that catshark fins lack a specific AP patterning mechanism, which restricts its expression to an anterior domain in tetrapods. Finally, experimental perturbation of AP patterning in catshark fin buds results in an expansion of posterior values and loss of anterior skeletal elements. Together, these results suggest that a key genetic event of the fin-to-limb transformation was alteration of the AP patterning network. DOI: http://dx.doi.org/10.7554/eLife.07048.001
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spelling pubmed-45387352015-08-25 A shift in anterior–posterior positional information underlies the fin-to-limb evolution Onimaru, Koh Kuraku, Shigehiro Takagi, Wataru Hyodo, Susumu Sharpe, James Tanaka, Mikiko eLife Developmental Biology and Stem Cells The pectoral fins of ancestral fishes had multiple proximal elements connected to their pectoral girdles. During the fin-to-limb transition, anterior proximal elements were lost and only the most posterior one remained as the humerus. Thus, we hypothesised that an evolutionary alteration occurred in the anterior–posterior (AP) patterning system of limb buds. In this study, we examined the pectoral fin development of catshark (Scyliorhinus canicula) and revealed that the AP positional values in fin buds are shifted more posteriorly than mouse limb buds. Furthermore, examination of Gli3 function and regulation shows that catshark fins lack a specific AP patterning mechanism, which restricts its expression to an anterior domain in tetrapods. Finally, experimental perturbation of AP patterning in catshark fin buds results in an expansion of posterior values and loss of anterior skeletal elements. Together, these results suggest that a key genetic event of the fin-to-limb transformation was alteration of the AP patterning network. DOI: http://dx.doi.org/10.7554/eLife.07048.001 eLife Sciences Publications, Ltd 2015-08-18 /pmc/articles/PMC4538735/ /pubmed/26283004 http://dx.doi.org/10.7554/eLife.07048 Text en © 2015, Onimaru et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology and Stem Cells
Onimaru, Koh
Kuraku, Shigehiro
Takagi, Wataru
Hyodo, Susumu
Sharpe, James
Tanaka, Mikiko
A shift in anterior–posterior positional information underlies the fin-to-limb evolution
title A shift in anterior–posterior positional information underlies the fin-to-limb evolution
title_full A shift in anterior–posterior positional information underlies the fin-to-limb evolution
title_fullStr A shift in anterior–posterior positional information underlies the fin-to-limb evolution
title_full_unstemmed A shift in anterior–posterior positional information underlies the fin-to-limb evolution
title_short A shift in anterior–posterior positional information underlies the fin-to-limb evolution
title_sort shift in anterior–posterior positional information underlies the fin-to-limb evolution
topic Developmental Biology and Stem Cells
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4538735/
https://www.ncbi.nlm.nih.gov/pubmed/26283004
http://dx.doi.org/10.7554/eLife.07048
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