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A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars

BACKGROUND: Echinoderms are a phylum of marine invertebrates with close phylogenetic relationships to chordates. Many members of the phylum Echinodermata are capable of extensive post-traumatic regeneration and life-long indeterminate growth. Different from regeneration, the life-long elongation of...

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Autores principales: Mashanov, Vladimir, Whaley, Lauren, Davis, Kenneth, Heinzeller, Thomas, Machado, Denis Jacob, Reid, Robert W., Kofsky, Janice, Janies, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9004015/
https://www.ncbi.nlm.nih.gov/pubmed/35413857
http://dx.doi.org/10.1186/s12983-022-00461-0
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author Mashanov, Vladimir
Whaley, Lauren
Davis, Kenneth
Heinzeller, Thomas
Machado, Denis Jacob
Reid, Robert W.
Kofsky, Janice
Janies, Daniel
author_facet Mashanov, Vladimir
Whaley, Lauren
Davis, Kenneth
Heinzeller, Thomas
Machado, Denis Jacob
Reid, Robert W.
Kofsky, Janice
Janies, Daniel
author_sort Mashanov, Vladimir
collection PubMed
description BACKGROUND: Echinoderms are a phylum of marine invertebrates with close phylogenetic relationships to chordates. Many members of the phylum Echinodermata are capable of extensive post-traumatic regeneration and life-long indeterminate growth. Different from regeneration, the life-long elongation of the main body axis in adult echinoderms has received little attention. The anatomical location and the nature of the dividing progenitor cells contributing to adults’ growth is unknown. RESULTS: We show that the proliferating cells that drive the life-long growth of adult brittle star arms are mostly localized to the subterminal (second from the tip) arm segment. Each of the major anatomical structures contains dividing progenitors. These structures include: the radial nerve, water-vascular canal, and arm coelomic wall. Some of those proliferating progenitor cells are capable of multiple rounds of cell division. Within the nervous system, the progenitor cells were identified as a subset of radial glial cells that do not express Brn1/2/4, a transcription factor with a conserved role in the neuronal fate specification. In addition to characterizing the growth zone and the nature of the precursor cells, we provide a description of the microanatomy of the four distal-most arm segments contrasting the distal with the proximal segments, which are more mature. CONCLUSIONS: The growth of the adult brittle star arms occurs via proliferation of progenitor cells in the distal segments, which are most abundant in the second segment from the tip. At least some of the progenitors are capable of multiple rounds of cell division. Within the nervous system the dividing cells were identified as Brn1/2/4-negative radial glial cells. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12983-022-00461-0.
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spelling pubmed-90040152022-04-13 A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars Mashanov, Vladimir Whaley, Lauren Davis, Kenneth Heinzeller, Thomas Machado, Denis Jacob Reid, Robert W. Kofsky, Janice Janies, Daniel Front Zool Research BACKGROUND: Echinoderms are a phylum of marine invertebrates with close phylogenetic relationships to chordates. Many members of the phylum Echinodermata are capable of extensive post-traumatic regeneration and life-long indeterminate growth. Different from regeneration, the life-long elongation of the main body axis in adult echinoderms has received little attention. The anatomical location and the nature of the dividing progenitor cells contributing to adults’ growth is unknown. RESULTS: We show that the proliferating cells that drive the life-long growth of adult brittle star arms are mostly localized to the subterminal (second from the tip) arm segment. Each of the major anatomical structures contains dividing progenitors. These structures include: the radial nerve, water-vascular canal, and arm coelomic wall. Some of those proliferating progenitor cells are capable of multiple rounds of cell division. Within the nervous system, the progenitor cells were identified as a subset of radial glial cells that do not express Brn1/2/4, a transcription factor with a conserved role in the neuronal fate specification. In addition to characterizing the growth zone and the nature of the precursor cells, we provide a description of the microanatomy of the four distal-most arm segments contrasting the distal with the proximal segments, which are more mature. CONCLUSIONS: The growth of the adult brittle star arms occurs via proliferation of progenitor cells in the distal segments, which are most abundant in the second segment from the tip. At least some of the progenitors are capable of multiple rounds of cell division. Within the nervous system the dividing cells were identified as Brn1/2/4-negative radial glial cells. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12983-022-00461-0. BioMed Central 2022-04-12 /pmc/articles/PMC9004015/ /pubmed/35413857 http://dx.doi.org/10.1186/s12983-022-00461-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Mashanov, Vladimir
Whaley, Lauren
Davis, Kenneth
Heinzeller, Thomas
Machado, Denis Jacob
Reid, Robert W.
Kofsky, Janice
Janies, Daniel
A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
title A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
title_full A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
title_fullStr A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
title_full_unstemmed A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
title_short A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
title_sort subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9004015/
https://www.ncbi.nlm.nih.gov/pubmed/35413857
http://dx.doi.org/10.1186/s12983-022-00461-0
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