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Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish

Fin regeneration has been extensively studied in zebrafish, a genetic model organism. Little is known about regulators of this process in distant fish taxa, such as the Poeciliidae family, represented by the platyfish. Here, we used this species to investigate the plasticity of ray branching morphog...

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Autores principales: Rees, Lana, König, Désirée, Jaźwińska, Anna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9946992/
https://www.ncbi.nlm.nih.gov/pubmed/36846592
http://dx.doi.org/10.3389/fcell.2023.1134451
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author Rees, Lana
König, Désirée
Jaźwińska, Anna
author_facet Rees, Lana
König, Désirée
Jaźwińska, Anna
author_sort Rees, Lana
collection PubMed
description Fin regeneration has been extensively studied in zebrafish, a genetic model organism. Little is known about regulators of this process in distant fish taxa, such as the Poeciliidae family, represented by the platyfish. Here, we used this species to investigate the plasticity of ray branching morphogenesis following either straight amputation or excision of ray triplets. This approach revealed that ray branching can be conditionally shifted to a more distal position, suggesting non-autonomous regulation of bone patterning. To gain molecular insights into regeneration of fin-specific dermal skeleton elements, actinotrichia and lepidotrichia, we localized expression of the actinodin genes and bmp2 in the regenerative outgrowth. Blocking of the BMP type-I receptor suppressed phospho-Smad1/5 immunoreactivity, and impaired fin regeneration after blastema formation. The resulting phenotype was characterized by the absence of bone and actinotrichia restoration. In addition, the wound epidermis displayed extensive thickening. This malformation was associated with expanded Tp63 expression from the basal epithelium towards more superficial layers, suggesting abnormal tissue differentiation. Our data add to the increasing evidence for the integrative role of BMP signaling in epidermal and skeletal tissue formation during fin regeneration. This expands our understanding of common mechanisms guiding appendage restoration in diverse clades of teleosts.
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spelling pubmed-99469922023-02-24 Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish Rees, Lana König, Désirée Jaźwińska, Anna Front Cell Dev Biol Cell and Developmental Biology Fin regeneration has been extensively studied in zebrafish, a genetic model organism. Little is known about regulators of this process in distant fish taxa, such as the Poeciliidae family, represented by the platyfish. Here, we used this species to investigate the plasticity of ray branching morphogenesis following either straight amputation or excision of ray triplets. This approach revealed that ray branching can be conditionally shifted to a more distal position, suggesting non-autonomous regulation of bone patterning. To gain molecular insights into regeneration of fin-specific dermal skeleton elements, actinotrichia and lepidotrichia, we localized expression of the actinodin genes and bmp2 in the regenerative outgrowth. Blocking of the BMP type-I receptor suppressed phospho-Smad1/5 immunoreactivity, and impaired fin regeneration after blastema formation. The resulting phenotype was characterized by the absence of bone and actinotrichia restoration. In addition, the wound epidermis displayed extensive thickening. This malformation was associated with expanded Tp63 expression from the basal epithelium towards more superficial layers, suggesting abnormal tissue differentiation. Our data add to the increasing evidence for the integrative role of BMP signaling in epidermal and skeletal tissue formation during fin regeneration. This expands our understanding of common mechanisms guiding appendage restoration in diverse clades of teleosts. Frontiers Media S.A. 2023-02-09 /pmc/articles/PMC9946992/ /pubmed/36846592 http://dx.doi.org/10.3389/fcell.2023.1134451 Text en Copyright © 2023 Rees, König and Jaźwińska. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Rees, Lana
König, Désirée
Jaźwińska, Anna
Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish
title Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish
title_full Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish
title_fullStr Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish
title_full_unstemmed Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish
title_short Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish
title_sort regeneration of the dermal skeleton and wound epidermis formation depend on bmp signaling in the caudal fin of platyfish
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9946992/
https://www.ncbi.nlm.nih.gov/pubmed/36846592
http://dx.doi.org/10.3389/fcell.2023.1134451
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