Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors

The organizer is one of the earliest structures to be established during vertebrate development and is crucial to subsequent patterning of the embryo. We have previously shown that the SoxB1 transcription factor, Sox3, plays a central role as a transcriptional repressor of zebrafish organizer gene e...

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Main Authors: Kuo, Cheng-Liang, Lam, Chi Man, Hewitt, Jane E., Scotting, Paul J.
Format: Article
Published: Public Library of Science 2013
Online Access:https://eprints.nottingham.ac.uk/2318/
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author Kuo, Cheng-Liang
Lam, Chi Man
Hewitt, Jane E.
Scotting, Paul J.
author_facet Kuo, Cheng-Liang
Lam, Chi Man
Hewitt, Jane E.
Scotting, Paul J.
author_sort Kuo, Cheng-Liang
building Nottingham Research Data Repository
collection Online Access
description The organizer is one of the earliest structures to be established during vertebrate development and is crucial to subsequent patterning of the embryo. We have previously shown that the SoxB1 transcription factor, Sox3, plays a central role as a transcriptional repressor of zebrafish organizer gene expression. Recent data suggest that Fgf signaling has a positive influence on organizer formation, but its role remains to be fully elucidated. In order to better understand how Fgf signaling fits into the complex regulatory network that determines when and where the organizer forms, the relationship between the positive effects of Fgf signaling and the repressive effects of the SoxB1 factors must be resolved. This study demonstrates that both fgf3 and fgf8 are required for expression of the organizer genes, gsc and chd, and that SoxB1 factors (Sox3, and the zebrafish specific factors, Sox19a and Sox19b) can repress the expression of both fgf3 and fgf8. However, we also find that these SoxB1 factors inhibit the expression of gsc and chd independently of their repression of fgf expression. We show that ectopic expression of organizer genes induced solely by the inhibition of SoxB1 function is dependent upon the activation of fgf expression. These data allow us to describe a comprehensive signaling network in which the SoxB1 factors restrict organizer formation by inhibiting Fgf, Nodal and Wnt signaling, as well as independently repressing the targets of that signaling. The organizer therefore forms only where Nodal-induced Fgf signaling overlaps with Wnt signaling and the SoxB1 proteins are absent.
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spelling nottingham-23182020-05-04T16:35:44Z https://eprints.nottingham.ac.uk/2318/ Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors Kuo, Cheng-Liang Lam, Chi Man Hewitt, Jane E. Scotting, Paul J. The organizer is one of the earliest structures to be established during vertebrate development and is crucial to subsequent patterning of the embryo. We have previously shown that the SoxB1 transcription factor, Sox3, plays a central role as a transcriptional repressor of zebrafish organizer gene expression. Recent data suggest that Fgf signaling has a positive influence on organizer formation, but its role remains to be fully elucidated. In order to better understand how Fgf signaling fits into the complex regulatory network that determines when and where the organizer forms, the relationship between the positive effects of Fgf signaling and the repressive effects of the SoxB1 factors must be resolved. This study demonstrates that both fgf3 and fgf8 are required for expression of the organizer genes, gsc and chd, and that SoxB1 factors (Sox3, and the zebrafish specific factors, Sox19a and Sox19b) can repress the expression of both fgf3 and fgf8. However, we also find that these SoxB1 factors inhibit the expression of gsc and chd independently of their repression of fgf expression. We show that ectopic expression of organizer genes induced solely by the inhibition of SoxB1 function is dependent upon the activation of fgf expression. These data allow us to describe a comprehensive signaling network in which the SoxB1 factors restrict organizer formation by inhibiting Fgf, Nodal and Wnt signaling, as well as independently repressing the targets of that signaling. The organizer therefore forms only where Nodal-induced Fgf signaling overlaps with Wnt signaling and the SoxB1 proteins are absent. Public Library of Science 2013-02-28 Article PeerReviewed Kuo, Cheng-Liang, Lam, Chi Man, Hewitt, Jane E. and Scotting, Paul J. (2013) Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors. PLoS ONE, 8 (2). ISSN 1932-6203 http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0057698 doi:10.1371/journal.pone.0057698 doi:10.1371/journal.pone.0057698
spellingShingle Kuo, Cheng-Liang
Lam, Chi Man
Hewitt, Jane E.
Scotting, Paul J.
Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors
title Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors
title_full Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors
title_fullStr Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors
title_full_unstemmed Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors
title_short Formation of the embryonic organizer is restricted by the competitive influences of Fgf signaling and the SoxB1 transcription factors
title_sort formation of the embryonic organizer is restricted by the competitive influences of fgf signaling and the soxb1 transcription factors
url https://eprints.nottingham.ac.uk/2318/
https://eprints.nottingham.ac.uk/2318/
https://eprints.nottingham.ac.uk/2318/