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Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona

Neurogenesis is a complex sequence of cellular processes and behaviors driven by the coordinated expression of conserved effectors. The bipolar tail neurons (BTNs) of Ciona develop according to a highly dynamic, yet highly stereotyped developmental program and thus could serve as an accessible model...

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Autores principales: Kim, Kwantae, Gibboney, Susanne, Razy-Krajka, Florian, Lowe, Elijah K., Wang, Wei, Stolfi, Alberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7324659/
https://www.ncbi.nlm.nih.gov/pubmed/32656209
http://dx.doi.org/10.3389/fcell.2020.00477
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author Kim, Kwantae
Gibboney, Susanne
Razy-Krajka, Florian
Lowe, Elijah K.
Wang, Wei
Stolfi, Alberto
author_facet Kim, Kwantae
Gibboney, Susanne
Razy-Krajka, Florian
Lowe, Elijah K.
Wang, Wei
Stolfi, Alberto
author_sort Kim, Kwantae
collection PubMed
description Neurogenesis is a complex sequence of cellular processes and behaviors driven by the coordinated expression of conserved effectors. The bipolar tail neurons (BTNs) of Ciona develop according to a highly dynamic, yet highly stereotyped developmental program and thus could serve as an accessible model system for neurogenesis, including underlying cell behaviors like neuronal delamination, migration, and polarized axon outgrowth. Here we investigate both the upstream events that shape BTN neurogenesis through spatiotemporal regulation of the conserved proneural factor Neurog, spatiotemporal, and the gene expression profile of differentiating BTNs downstream of Neurog activity. We show that, although early FGF signaling is required for Neurog expression and BTN specification, Fgf8/17/18 is expressed in tail tip cells at later stages and suppresses sustained Neurog expression in the anterior BTN (aBTN) lineage, such that only one cell (the one furthest from the source of Fgf8/17/18) maintains Neurog expression and becomes a neuron. Curiously, Fgf8/17/18 might not affect neurogenesis of the posterior BTNs (pBTNs), which are in direct contact with the Fgf8/17/18-expressing cells. Finally, to profile gene expression associated with BTN neurogenesis we performed RNAseq of isolated BTN lineage cells in which BTN neurogenesis was enhanced or suppressed by perturbing Neurog function. This allowed us to identify several candidate genes that might play conserved roles in neurogenesis and neuronal migration in other animals, including mammals.
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spelling pubmed-73246592020-07-10 Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona Kim, Kwantae Gibboney, Susanne Razy-Krajka, Florian Lowe, Elijah K. Wang, Wei Stolfi, Alberto Front Cell Dev Biol Cell and Developmental Biology Neurogenesis is a complex sequence of cellular processes and behaviors driven by the coordinated expression of conserved effectors. The bipolar tail neurons (BTNs) of Ciona develop according to a highly dynamic, yet highly stereotyped developmental program and thus could serve as an accessible model system for neurogenesis, including underlying cell behaviors like neuronal delamination, migration, and polarized axon outgrowth. Here we investigate both the upstream events that shape BTN neurogenesis through spatiotemporal regulation of the conserved proneural factor Neurog, spatiotemporal, and the gene expression profile of differentiating BTNs downstream of Neurog activity. We show that, although early FGF signaling is required for Neurog expression and BTN specification, Fgf8/17/18 is expressed in tail tip cells at later stages and suppresses sustained Neurog expression in the anterior BTN (aBTN) lineage, such that only one cell (the one furthest from the source of Fgf8/17/18) maintains Neurog expression and becomes a neuron. Curiously, Fgf8/17/18 might not affect neurogenesis of the posterior BTNs (pBTNs), which are in direct contact with the Fgf8/17/18-expressing cells. Finally, to profile gene expression associated with BTN neurogenesis we performed RNAseq of isolated BTN lineage cells in which BTN neurogenesis was enhanced or suppressed by perturbing Neurog function. This allowed us to identify several candidate genes that might play conserved roles in neurogenesis and neuronal migration in other animals, including mammals. Frontiers Media S.A. 2020-06-23 /pmc/articles/PMC7324659/ /pubmed/32656209 http://dx.doi.org/10.3389/fcell.2020.00477 Text en Copyright © 2020 Kim, Gibboney, Razy-Krajka, Lowe, Wang and Stolfi. http://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
Kim, Kwantae
Gibboney, Susanne
Razy-Krajka, Florian
Lowe, Elijah K.
Wang, Wei
Stolfi, Alberto
Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona
title Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona
title_full Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona
title_fullStr Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona
title_full_unstemmed Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona
title_short Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona
title_sort regulation of neurogenesis by fgf signaling and neurogenin in the invertebrate chordate ciona
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7324659/
https://www.ncbi.nlm.nih.gov/pubmed/32656209
http://dx.doi.org/10.3389/fcell.2020.00477
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