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Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains

The embryonic ectoderm is composed of four domains: neural plate, neural crest, pre-placodal region (PPR) and epidermis. Their formation is initiated during early gastrulation by dorsal-ventral and anterior-posterior gradients of signaling factors that first divide the embryonic ectoderm into neural...

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Autores principales: Klein, Steven L., Tavares, Andre L. P., Peterson, Meredith, Sullivan, Charles H., Moody, Sally A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8859430/
https://www.ncbi.nlm.nih.gov/pubmed/35198557
http://dx.doi.org/10.3389/fcell.2022.786052
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author Klein, Steven L.
Tavares, Andre L. P.
Peterson, Meredith
Sullivan, Charles H.
Moody, Sally A.
author_facet Klein, Steven L.
Tavares, Andre L. P.
Peterson, Meredith
Sullivan, Charles H.
Moody, Sally A.
author_sort Klein, Steven L.
collection PubMed
description The embryonic ectoderm is composed of four domains: neural plate, neural crest, pre-placodal region (PPR) and epidermis. Their formation is initiated during early gastrulation by dorsal-ventral and anterior-posterior gradients of signaling factors that first divide the embryonic ectoderm into neural and non-neural domains. Next, the neural crest and PPR domains arise, either via differential competence of the neural and non-neural ectoderm (binary competence model) or via interactions between the neural and non-neural ectoderm tissues to produce an intermediate neural border zone (NB) (border state model) that subsequently separates into neural crest and PPR. Many previous gain- and loss-of-function experiments demonstrate that numerous TFs are expressed in initially overlapping zones that gradually resolve into patterns that by late neurula stages are characteristic of each of the four domains. Several of these studies suggested that this is accomplished by a combination of repressive TF interactions and competence to respond to local signals. In this study, we ectopically expressed TFs that at neural plate stages are characteristic of one domain in a different domain to test whether they act cell autonomously as repressors. We found that almost all tested TFs caused reduced expression of the other TFs. At gastrulation these effects were strictly within the lineage-labeled cells, indicating that the effects were cell autonomous, i.e., due to TF interactions within individual cells. Analysis of previously published single cell RNAseq datasets showed that at the end of gastrulation, and continuing to neural tube closure stages, many ectodermal cells express TFs characteristic of more than one neural plate stage domain, indicating that different TFs have the opportunity to interact within the same cell. At neurula stages repression was observed both in the lineage-labeled cells and in adjacent cells not bearing detectable lineage label, suggesting that cell-to-cell signaling has begun to contribute to the separation of the domains. Together, these observations directly demonstrate previous suggestions in the literature that the segregation of embryonic ectodermal domains initially involves cell autonomous, repressive TF interactions within an individual cell followed by the subsequent advent of non-cell autonomous signaling to neighbors.
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spelling pubmed-88594302022-02-22 Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains Klein, Steven L. Tavares, Andre L. P. Peterson, Meredith Sullivan, Charles H. Moody, Sally A. Front Cell Dev Biol Cell and Developmental Biology The embryonic ectoderm is composed of four domains: neural plate, neural crest, pre-placodal region (PPR) and epidermis. Their formation is initiated during early gastrulation by dorsal-ventral and anterior-posterior gradients of signaling factors that first divide the embryonic ectoderm into neural and non-neural domains. Next, the neural crest and PPR domains arise, either via differential competence of the neural and non-neural ectoderm (binary competence model) or via interactions between the neural and non-neural ectoderm tissues to produce an intermediate neural border zone (NB) (border state model) that subsequently separates into neural crest and PPR. Many previous gain- and loss-of-function experiments demonstrate that numerous TFs are expressed in initially overlapping zones that gradually resolve into patterns that by late neurula stages are characteristic of each of the four domains. Several of these studies suggested that this is accomplished by a combination of repressive TF interactions and competence to respond to local signals. In this study, we ectopically expressed TFs that at neural plate stages are characteristic of one domain in a different domain to test whether they act cell autonomously as repressors. We found that almost all tested TFs caused reduced expression of the other TFs. At gastrulation these effects were strictly within the lineage-labeled cells, indicating that the effects were cell autonomous, i.e., due to TF interactions within individual cells. Analysis of previously published single cell RNAseq datasets showed that at the end of gastrulation, and continuing to neural tube closure stages, many ectodermal cells express TFs characteristic of more than one neural plate stage domain, indicating that different TFs have the opportunity to interact within the same cell. At neurula stages repression was observed both in the lineage-labeled cells and in adjacent cells not bearing detectable lineage label, suggesting that cell-to-cell signaling has begun to contribute to the separation of the domains. Together, these observations directly demonstrate previous suggestions in the literature that the segregation of embryonic ectodermal domains initially involves cell autonomous, repressive TF interactions within an individual cell followed by the subsequent advent of non-cell autonomous signaling to neighbors. Frontiers Media S.A. 2022-02-07 /pmc/articles/PMC8859430/ /pubmed/35198557 http://dx.doi.org/10.3389/fcell.2022.786052 Text en Copyright © 2022 Klein, Tavares, Peterson, Sullivan and Moody. https://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
Klein, Steven L.
Tavares, Andre L. P.
Peterson, Meredith
Sullivan, Charles H.
Moody, Sally A.
Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains
title Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains
title_full Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains
title_fullStr Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains
title_full_unstemmed Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains
title_short Repressive Interactions Between Transcription Factors Separate Different Embryonic Ectodermal Domains
title_sort repressive interactions between transcription factors separate different embryonic ectodermal domains
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8859430/
https://www.ncbi.nlm.nih.gov/pubmed/35198557
http://dx.doi.org/10.3389/fcell.2022.786052
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