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Pattern of fin rays along the antero-posterior axis based on their connection to distal radials

BACKGROUND: Teleost paired fins are composed of two endoskeletal domains, proximal and distal radials, and an exoskeletal domain, the fin ray. The zebrafish pectoral fin displays elaborately patterned radials along the anteroposterior (AP) axis. Radials are considered homologous to tetrapod limb ske...

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Autores principales: Hamada, Hiroki, Uemoto, Toshiaki, Tanaka, Yoshitaka, Honda, Yuki, Kitajima, Keiichi, Umeda, Tetsuya, Kawakami, Atsushi, Shinya, Minori, Kawakami, Koichi, Tamura, Koji, Abe, Gembu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6751676/
https://www.ncbi.nlm.nih.gov/pubmed/31548912
http://dx.doi.org/10.1186/s40851-019-0145-z
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author Hamada, Hiroki
Uemoto, Toshiaki
Tanaka, Yoshitaka
Honda, Yuki
Kitajima, Keiichi
Umeda, Tetsuya
Kawakami, Atsushi
Shinya, Minori
Kawakami, Koichi
Tamura, Koji
Abe, Gembu
author_facet Hamada, Hiroki
Uemoto, Toshiaki
Tanaka, Yoshitaka
Honda, Yuki
Kitajima, Keiichi
Umeda, Tetsuya
Kawakami, Atsushi
Shinya, Minori
Kawakami, Koichi
Tamura, Koji
Abe, Gembu
author_sort Hamada, Hiroki
collection PubMed
description BACKGROUND: Teleost paired fins are composed of two endoskeletal domains, proximal and distal radials, and an exoskeletal domain, the fin ray. The zebrafish pectoral fin displays elaborately patterned radials along the anteroposterior (AP) axis. Radials are considered homologous to tetrapod limb skeletons, and their patterning mechanisms in embryonic development are similar to those of limb development. Nevertheless, the pattern along the AP axis in fin rays has not been well described in the zebrafish pectoral fin, although several recent reports have revealed that fin ray development shares some cellular and genetic properties with fin/limb endoskeleton development. Thus, fin ray morphogenesis may involve developmental mechanisms for AP patterning in the fin/limb endoskeleton, and may have a specific pattern along the AP axis. RESULTS: We conducted detailed morphological observations on fin rays and their connection to distal radials by comparing intra- and inter-strain zebrafish specimens. Although the number of fin rays varied, pectoral fin rays could be categorized into three domains along the AP axis, according to the connection between the fin rays and distal radials; additionally, the number of fin rays varied in the posterior part of the three domains. This result was confirmed by observation of the morphogenesis process of fin rays and distal radials, which showed altered localization of distal radials in the middle domain. We also evaluated the expression pattern of lhx genes, which have AP patterning activity in limb development, in fin rays and during distal radial development and found these genes to be expressed during morphogenesis in both fin rays and distal radials. CONCLUSION: The fin ray and its connection to the endoskeleton are patterned along the AP axis, and the pattern along the AP axis in the fin ray and the radial connection is constructed by the developmental mechanism related to AP patterning in the limb/fin bud. Our results indicate the possibility that the developmental mechanisms of fin rays and their connection are comparable to those of the distal element of the limb skeleton. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40851-019-0145-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-67516762019-09-23 Pattern of fin rays along the antero-posterior axis based on their connection to distal radials Hamada, Hiroki Uemoto, Toshiaki Tanaka, Yoshitaka Honda, Yuki Kitajima, Keiichi Umeda, Tetsuya Kawakami, Atsushi Shinya, Minori Kawakami, Koichi Tamura, Koji Abe, Gembu Zoological Lett Research Article BACKGROUND: Teleost paired fins are composed of two endoskeletal domains, proximal and distal radials, and an exoskeletal domain, the fin ray. The zebrafish pectoral fin displays elaborately patterned radials along the anteroposterior (AP) axis. Radials are considered homologous to tetrapod limb skeletons, and their patterning mechanisms in embryonic development are similar to those of limb development. Nevertheless, the pattern along the AP axis in fin rays has not been well described in the zebrafish pectoral fin, although several recent reports have revealed that fin ray development shares some cellular and genetic properties with fin/limb endoskeleton development. Thus, fin ray morphogenesis may involve developmental mechanisms for AP patterning in the fin/limb endoskeleton, and may have a specific pattern along the AP axis. RESULTS: We conducted detailed morphological observations on fin rays and their connection to distal radials by comparing intra- and inter-strain zebrafish specimens. Although the number of fin rays varied, pectoral fin rays could be categorized into three domains along the AP axis, according to the connection between the fin rays and distal radials; additionally, the number of fin rays varied in the posterior part of the three domains. This result was confirmed by observation of the morphogenesis process of fin rays and distal radials, which showed altered localization of distal radials in the middle domain. We also evaluated the expression pattern of lhx genes, which have AP patterning activity in limb development, in fin rays and during distal radial development and found these genes to be expressed during morphogenesis in both fin rays and distal radials. CONCLUSION: The fin ray and its connection to the endoskeleton are patterned along the AP axis, and the pattern along the AP axis in the fin ray and the radial connection is constructed by the developmental mechanism related to AP patterning in the limb/fin bud. Our results indicate the possibility that the developmental mechanisms of fin rays and their connection are comparable to those of the distal element of the limb skeleton. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40851-019-0145-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-09-18 /pmc/articles/PMC6751676/ /pubmed/31548912 http://dx.doi.org/10.1186/s40851-019-0145-z Text en © The Author(s). 2019 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
Hamada, Hiroki
Uemoto, Toshiaki
Tanaka, Yoshitaka
Honda, Yuki
Kitajima, Keiichi
Umeda, Tetsuya
Kawakami, Atsushi
Shinya, Minori
Kawakami, Koichi
Tamura, Koji
Abe, Gembu
Pattern of fin rays along the antero-posterior axis based on their connection to distal radials
title Pattern of fin rays along the antero-posterior axis based on their connection to distal radials
title_full Pattern of fin rays along the antero-posterior axis based on their connection to distal radials
title_fullStr Pattern of fin rays along the antero-posterior axis based on their connection to distal radials
title_full_unstemmed Pattern of fin rays along the antero-posterior axis based on their connection to distal radials
title_short Pattern of fin rays along the antero-posterior axis based on their connection to distal radials
title_sort pattern of fin rays along the antero-posterior axis based on their connection to distal radials
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6751676/
https://www.ncbi.nlm.nih.gov/pubmed/31548912
http://dx.doi.org/10.1186/s40851-019-0145-z
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