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Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa

BACKGROUND: Metazoan lineages exhibit a wide range of regenerative capabilities that vary among developmental stage and tissue type. The most robust regenerative abilities are apparent in the phyla Cnidaria, Platyhelminthes, and Echinodermata, whose members are capable of whole-body regeneration (WB...

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Autores principales: Cary, Gregory A., Wolff, Andrew, Zueva, Olga, Pattinato, Joseph, Hinman, Veronica F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6385403/
https://www.ncbi.nlm.nih.gov/pubmed/30795750
http://dx.doi.org/10.1186/s12915-019-0633-9
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author Cary, Gregory A.
Wolff, Andrew
Zueva, Olga
Pattinato, Joseph
Hinman, Veronica F.
author_facet Cary, Gregory A.
Wolff, Andrew
Zueva, Olga
Pattinato, Joseph
Hinman, Veronica F.
author_sort Cary, Gregory A.
collection PubMed
description BACKGROUND: Metazoan lineages exhibit a wide range of regenerative capabilities that vary among developmental stage and tissue type. The most robust regenerative abilities are apparent in the phyla Cnidaria, Platyhelminthes, and Echinodermata, whose members are capable of whole-body regeneration (WBR). This phenomenon has been well characterized in planarian and hydra models, but the molecular mechanisms of WBR are less established within echinoderms, or any other deuterostome system. Thus, it is not clear to what degree aspects of this regenerative ability are shared among metazoa. RESULTS: We characterize regeneration in the larval stage of the Bat Star (Patiria miniata). Following bisection along the anterior-posterior axis, larvae progress through phases of wound healing and re-proportioning of larval tissues. The overall number of proliferating cells is reduced following bisection, and we find evidence for a re-deployment of genes with known roles in embryonic axial patterning. Following axial respecification, we observe a significant localization of proliferating cells to the wound region. Analyses of transcriptome data highlight the molecular signatures of functions that are common to regeneration, including specific signaling pathways and cell cycle controls. Notably, we find evidence for temporal similarities among orthologous genes involved in regeneration from published Platyhelminth and Cnidarian regeneration datasets. CONCLUSIONS: These analyses show that sea star larval regeneration includes phases of wound response, axis respecification, and wound-proximal proliferation. Commonalities of the overall process of regeneration, as well as gene usage between this deuterostome and other species with divergent evolutionary origins reveal a deep similarity of whole-body regeneration among the metazoa. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0633-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-63854032019-03-01 Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa Cary, Gregory A. Wolff, Andrew Zueva, Olga Pattinato, Joseph Hinman, Veronica F. BMC Biol Research Article BACKGROUND: Metazoan lineages exhibit a wide range of regenerative capabilities that vary among developmental stage and tissue type. The most robust regenerative abilities are apparent in the phyla Cnidaria, Platyhelminthes, and Echinodermata, whose members are capable of whole-body regeneration (WBR). This phenomenon has been well characterized in planarian and hydra models, but the molecular mechanisms of WBR are less established within echinoderms, or any other deuterostome system. Thus, it is not clear to what degree aspects of this regenerative ability are shared among metazoa. RESULTS: We characterize regeneration in the larval stage of the Bat Star (Patiria miniata). Following bisection along the anterior-posterior axis, larvae progress through phases of wound healing and re-proportioning of larval tissues. The overall number of proliferating cells is reduced following bisection, and we find evidence for a re-deployment of genes with known roles in embryonic axial patterning. Following axial respecification, we observe a significant localization of proliferating cells to the wound region. Analyses of transcriptome data highlight the molecular signatures of functions that are common to regeneration, including specific signaling pathways and cell cycle controls. Notably, we find evidence for temporal similarities among orthologous genes involved in regeneration from published Platyhelminth and Cnidarian regeneration datasets. CONCLUSIONS: These analyses show that sea star larval regeneration includes phases of wound response, axis respecification, and wound-proximal proliferation. Commonalities of the overall process of regeneration, as well as gene usage between this deuterostome and other species with divergent evolutionary origins reveal a deep similarity of whole-body regeneration among the metazoa. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0633-9) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-22 /pmc/articles/PMC6385403/ /pubmed/30795750 http://dx.doi.org/10.1186/s12915-019-0633-9 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
Cary, Gregory A.
Wolff, Andrew
Zueva, Olga
Pattinato, Joseph
Hinman, Veronica F.
Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
title Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
title_full Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
title_fullStr Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
title_full_unstemmed Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
title_short Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
title_sort analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6385403/
https://www.ncbi.nlm.nih.gov/pubmed/30795750
http://dx.doi.org/10.1186/s12915-019-0633-9
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