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Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)

BACKGROUND: The structure and development of the nervous system in Lophotrochozoa has long been recognized as one of the most important subjects for phylogenetic and evolutionary discussion. Many recent papers have presented comprehensive data on the structure and development of catecholaminergic, s...

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Autores principales: Starunov, Viktor V., Voronezhskaya, Elena E., Nezlin, Leonid P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5445494/
https://www.ncbi.nlm.nih.gov/pubmed/28559917
http://dx.doi.org/10.1186/s12983-017-0211-3
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author Starunov, Viktor V.
Voronezhskaya, Elena E.
Nezlin, Leonid P.
author_facet Starunov, Viktor V.
Voronezhskaya, Elena E.
Nezlin, Leonid P.
author_sort Starunov, Viktor V.
collection PubMed
description BACKGROUND: The structure and development of the nervous system in Lophotrochozoa has long been recognized as one of the most important subjects for phylogenetic and evolutionary discussion. Many recent papers have presented comprehensive data on the structure and development of catecholaminergic, serotonergic and FMRFamidergic parts of the nervous system. However, relatively few papers contain detailed descriptions of the nervous system in Annelida, one of the largest taxa of Lophotrochozoa. The polychaete species Platynereis dumerilii has recently become one of the more popular model animals in evolutionary and developmental biology. The goal of the present study was to provide a detailed description of its neuronal development. The data obtained will contribute to a better understanding of the basic features of neuronal development in polychaetes. RESULTS: We have studied the development of the nervous system in P. dumerilii utilizing histo- and immunochemical labelling of catecholamines, serotonin, FMRFamide related peptides, and acetylated tubulin. The first neuron differentiates at the posterior extremity of the protrochophore, reacts to the antibodies against both serotonin and FMRFamide. Then its fibres run forwards along the ventral side. Soon, more neurons appear at the apical extreme, and their basal neurites form the basel structure of the developing brain (cerebral neuropil and circumesophageal connectives). Initial development of the nervous system starts in two rudiments: anterior and posterior. At the nectochaete stage, segmental ganglia start to differentiate in the anterior-to-posterior direction, and the first structures of the stomatogastric and peripheral nervous system appear. All connectives including the unpaired ventral cord develop from initially paired nerves. CONCLUSIONS: We present a detailed description of Platynereis dumerilii neuronal development based on anti-acetylated tubulin, serotonin, and FMRFamide-like immunostaining as well as catecholamine histofluorescence. The development of the nervous system starts from peripheral pioneer neurons at both the posterior and anterior poles of the larva, and their neurites form a scaffold upon which the adult central nervous system develops. The anterior-to-posterior mode of the ventral ganglia development challenges the primary heteronomy concept. Comparison with the development of Mollusca reveals substantial similarities with early neuronal development in larval Solenogastres. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-017-0211-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-54454942017-05-30 Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida) Starunov, Viktor V. Voronezhskaya, Elena E. Nezlin, Leonid P. Front Zool Research BACKGROUND: The structure and development of the nervous system in Lophotrochozoa has long been recognized as one of the most important subjects for phylogenetic and evolutionary discussion. Many recent papers have presented comprehensive data on the structure and development of catecholaminergic, serotonergic and FMRFamidergic parts of the nervous system. However, relatively few papers contain detailed descriptions of the nervous system in Annelida, one of the largest taxa of Lophotrochozoa. The polychaete species Platynereis dumerilii has recently become one of the more popular model animals in evolutionary and developmental biology. The goal of the present study was to provide a detailed description of its neuronal development. The data obtained will contribute to a better understanding of the basic features of neuronal development in polychaetes. RESULTS: We have studied the development of the nervous system in P. dumerilii utilizing histo- and immunochemical labelling of catecholamines, serotonin, FMRFamide related peptides, and acetylated tubulin. The first neuron differentiates at the posterior extremity of the protrochophore, reacts to the antibodies against both serotonin and FMRFamide. Then its fibres run forwards along the ventral side. Soon, more neurons appear at the apical extreme, and their basal neurites form the basel structure of the developing brain (cerebral neuropil and circumesophageal connectives). Initial development of the nervous system starts in two rudiments: anterior and posterior. At the nectochaete stage, segmental ganglia start to differentiate in the anterior-to-posterior direction, and the first structures of the stomatogastric and peripheral nervous system appear. All connectives including the unpaired ventral cord develop from initially paired nerves. CONCLUSIONS: We present a detailed description of Platynereis dumerilii neuronal development based on anti-acetylated tubulin, serotonin, and FMRFamide-like immunostaining as well as catecholamine histofluorescence. The development of the nervous system starts from peripheral pioneer neurons at both the posterior and anterior poles of the larva, and their neurites form a scaffold upon which the adult central nervous system develops. The anterior-to-posterior mode of the ventral ganglia development challenges the primary heteronomy concept. Comparison with the development of Mollusca reveals substantial similarities with early neuronal development in larval Solenogastres. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-017-0211-3) contains supplementary material, which is available to authorized users. BioMed Central 2017-05-25 /pmc/articles/PMC5445494/ /pubmed/28559917 http://dx.doi.org/10.1186/s12983-017-0211-3 Text en © The Author(s). 2017 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
Starunov, Viktor V.
Voronezhskaya, Elena E.
Nezlin, Leonid P.
Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)
title Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)
title_full Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)
title_fullStr Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)
title_full_unstemmed Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)
title_short Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida)
title_sort development of the nervous system in platynereis dumerilii (nereididae, annelida)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5445494/
https://www.ncbi.nlm.nih.gov/pubmed/28559917
http://dx.doi.org/10.1186/s12983-017-0211-3
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