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The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes

Notch is a key signalling pathway playing multiple and varied functions during development. Notch regulates the selection of cells with a neurogenic fate and maintains a pool of yet uncommitted precursors through lateral inhibition, both in insects and in vertebrates. Here, we explore the functions...

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Detalles Bibliográficos
Autores principales: Gazave, Eve, Lemaître, Quentin I. B., Balavoine, Guillaume
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5356439/
https://www.ncbi.nlm.nih.gov/pubmed/28148821
http://dx.doi.org/10.1098/rsob.160242
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author Gazave, Eve
Lemaître, Quentin I. B.
Balavoine, Guillaume
author_facet Gazave, Eve
Lemaître, Quentin I. B.
Balavoine, Guillaume
author_sort Gazave, Eve
collection PubMed
description Notch is a key signalling pathway playing multiple and varied functions during development. Notch regulates the selection of cells with a neurogenic fate and maintains a pool of yet uncommitted precursors through lateral inhibition, both in insects and in vertebrates. Here, we explore the functions of Notch in the annelid Platynereis dumerilii (Lophotrochozoa). Conserved components of the pathway are identified and a scenario for their evolution in metazoans is proposed. Unexpectedly, neither Notch nor its ligands are expressed in the neurogenic epithelia of the larva at the time when massive neurogenesis begins. Using chemical inhibitors and neural markers, we demonstrate that Notch plays no major role in the general neurogenesis of larvae. Instead, we find Notch components expressed in nascent chaetal sacs, the organs that produce the annelid bristles. Impairing Notch signalling induces defects in chaetal sac formation, abnormalities in chaetae producing cells and a change of identity of chaeta growth accessory cells. This is the first bilaterian species in which the early neurogenesis processes appear to occur without a major involvement of the Notch pathway. Instead, Notch is co-opted to pattern annelid-specific organs, likely through a lateral inhibition process. These features reinforce the view that Notch signalling has been recruited multiple times in evolution due to its remarkable ‘toolkit’ nature.
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spelling pubmed-53564392017-03-29 The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes Gazave, Eve Lemaître, Quentin I. B. Balavoine, Guillaume Open Biol Research Notch is a key signalling pathway playing multiple and varied functions during development. Notch regulates the selection of cells with a neurogenic fate and maintains a pool of yet uncommitted precursors through lateral inhibition, both in insects and in vertebrates. Here, we explore the functions of Notch in the annelid Platynereis dumerilii (Lophotrochozoa). Conserved components of the pathway are identified and a scenario for their evolution in metazoans is proposed. Unexpectedly, neither Notch nor its ligands are expressed in the neurogenic epithelia of the larva at the time when massive neurogenesis begins. Using chemical inhibitors and neural markers, we demonstrate that Notch plays no major role in the general neurogenesis of larvae. Instead, we find Notch components expressed in nascent chaetal sacs, the organs that produce the annelid bristles. Impairing Notch signalling induces defects in chaetal sac formation, abnormalities in chaetae producing cells and a change of identity of chaeta growth accessory cells. This is the first bilaterian species in which the early neurogenesis processes appear to occur without a major involvement of the Notch pathway. Instead, Notch is co-opted to pattern annelid-specific organs, likely through a lateral inhibition process. These features reinforce the view that Notch signalling has been recruited multiple times in evolution due to its remarkable ‘toolkit’ nature. The Royal Society 2017-02-01 /pmc/articles/PMC5356439/ /pubmed/28148821 http://dx.doi.org/10.1098/rsob.160242 Text en © 2017 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Gazave, Eve
Lemaître, Quentin I. B.
Balavoine, Guillaume
The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes
title The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes
title_full The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes
title_fullStr The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes
title_full_unstemmed The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes
title_short The Notch pathway in the annelid Platynereis: insights into chaetogenesis and neurogenesis processes
title_sort notch pathway in the annelid platynereis: insights into chaetogenesis and neurogenesis processes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5356439/
https://www.ncbi.nlm.nih.gov/pubmed/28148821
http://dx.doi.org/10.1098/rsob.160242
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