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The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization

Colonial tunicates are the only chordates that regularly regenerate a fully functional whole body as part of their asexual life cycle, starting from specific epithelia and/or mesenchymal cells. In addition, in some species, whole-body regeneration (WBR) can also be triggered by extensive injuries, w...

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Autores principales: Ricci, Lorenzo, Salmon, Bastien, Olivier, Caroline, Andreoni-Pham, Rita, Chaurasia, Ankita, Alié, Alexandre, Tiozzo, Stefano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8882763/
https://www.ncbi.nlm.nih.gov/pubmed/35237607
http://dx.doi.org/10.3389/fcell.2022.843775
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author Ricci, Lorenzo
Salmon, Bastien
Olivier, Caroline
Andreoni-Pham, Rita
Chaurasia, Ankita
Alié, Alexandre
Tiozzo, Stefano
author_facet Ricci, Lorenzo
Salmon, Bastien
Olivier, Caroline
Andreoni-Pham, Rita
Chaurasia, Ankita
Alié, Alexandre
Tiozzo, Stefano
author_sort Ricci, Lorenzo
collection PubMed
description Colonial tunicates are the only chordates that regularly regenerate a fully functional whole body as part of their asexual life cycle, starting from specific epithelia and/or mesenchymal cells. In addition, in some species, whole-body regeneration (WBR) can also be triggered by extensive injuries, which deplete most of their tissues and organs and leave behind only small fragments of their body. In this manuscript, we characterized the onset of WBR in Botryllus schlosseri, one colonial tunicate long used as a laboratory model. We first analyzed the transcriptomic response to a WBR-triggering injury. Then, through morphological characterization, in vivo observations via time-lapse, vital dyes, and cell transplant assays, we started to reconstruct the dynamics of the cells triggering regeneration, highlighting an interplay between mesenchymal and epithelial cells. The dynamics described here suggest that WBR in B. schlosseri is initiated by extravascular tissue fragments derived from the injured individuals rather than particular populations of blood-borne cells, as has been described in closely related species. The morphological and molecular datasets here reported provide the background for future mechanistic studies of the WBR ontogenesis in B. schlosseri and allow to compare it with other regenerative processes occurring in other tunicate species and possibly independently evolved.
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spelling pubmed-88827632022-03-01 The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization Ricci, Lorenzo Salmon, Bastien Olivier, Caroline Andreoni-Pham, Rita Chaurasia, Ankita Alié, Alexandre Tiozzo, Stefano Front Cell Dev Biol Cell and Developmental Biology Colonial tunicates are the only chordates that regularly regenerate a fully functional whole body as part of their asexual life cycle, starting from specific epithelia and/or mesenchymal cells. In addition, in some species, whole-body regeneration (WBR) can also be triggered by extensive injuries, which deplete most of their tissues and organs and leave behind only small fragments of their body. In this manuscript, we characterized the onset of WBR in Botryllus schlosseri, one colonial tunicate long used as a laboratory model. We first analyzed the transcriptomic response to a WBR-triggering injury. Then, through morphological characterization, in vivo observations via time-lapse, vital dyes, and cell transplant assays, we started to reconstruct the dynamics of the cells triggering regeneration, highlighting an interplay between mesenchymal and epithelial cells. The dynamics described here suggest that WBR in B. schlosseri is initiated by extravascular tissue fragments derived from the injured individuals rather than particular populations of blood-borne cells, as has been described in closely related species. The morphological and molecular datasets here reported provide the background for future mechanistic studies of the WBR ontogenesis in B. schlosseri and allow to compare it with other regenerative processes occurring in other tunicate species and possibly independently evolved. Frontiers Media S.A. 2022-02-14 /pmc/articles/PMC8882763/ /pubmed/35237607 http://dx.doi.org/10.3389/fcell.2022.843775 Text en Copyright © 2022 Ricci, Salmon, Olivier, Andreoni-Pham, Chaurasia, Alié and Tiozzo. 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
Ricci, Lorenzo
Salmon, Bastien
Olivier, Caroline
Andreoni-Pham, Rita
Chaurasia, Ankita
Alié, Alexandre
Tiozzo, Stefano
The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization
title The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization
title_full The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization
title_fullStr The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization
title_full_unstemmed The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization
title_short The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization
title_sort onset of whole-body regeneration in botryllus schlosseri: morphological and molecular characterization
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8882763/
https://www.ncbi.nlm.nih.gov/pubmed/35237607
http://dx.doi.org/10.3389/fcell.2022.843775
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