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Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informativ...

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Autores principales: Kaul-Strehlow, Sabrina, Urata, Makoto, Minokawa, Takuya, Stach, Thomas, Wanninger, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4514687/
https://www.ncbi.nlm.nih.gov/pubmed/26225120
http://dx.doi.org/10.1007/s13127-015-0201-2
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author Kaul-Strehlow, Sabrina
Urata, Makoto
Minokawa, Takuya
Stach, Thomas
Wanninger, Andreas
author_facet Kaul-Strehlow, Sabrina
Urata, Makoto
Minokawa, Takuya
Stach, Thomas
Wanninger, Andreas
author_sort Kaul-Strehlow, Sabrina
collection PubMed
description Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.
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spelling pubmed-45146872015-07-27 Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords Kaul-Strehlow, Sabrina Urata, Makoto Minokawa, Takuya Stach, Thomas Wanninger, Andreas Org Divers Evol Original Article Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria. Springer Berlin Heidelberg 2015-01-31 2015 /pmc/articles/PMC4514687/ /pubmed/26225120 http://dx.doi.org/10.1007/s13127-015-0201-2 Text en © The Author(s) 2015 https://creativecommons.org/licenses/by/4.0/ Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
spellingShingle Original Article
Kaul-Strehlow, Sabrina
Urata, Makoto
Minokawa, Takuya
Stach, Thomas
Wanninger, Andreas
Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
title Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
title_full Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
title_fullStr Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
title_full_unstemmed Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
title_short Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
title_sort neurogenesis in directly and indirectly developing enteropneusts: of nets and cords
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4514687/
https://www.ncbi.nlm.nih.gov/pubmed/26225120
http://dx.doi.org/10.1007/s13127-015-0201-2
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