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The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon
Dorsal-ventral patterning of the mammalian telencephalon is fundamental to the formation of distinct functional regions including the neocortex and ganglionic eminence. While Bone morphogenetic protein (BMP), Wnt, and Sonic hedgehog (Shh) signaling are known to determine regional identity along the...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Nature Publishing Group UK
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7658352/ https://www.ncbi.nlm.nih.gov/pubmed/33177537 http://dx.doi.org/10.1038/s41467-020-19556-5 |
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author | Eto, Hikaru Kishi, Yusuke Yakushiji-Kaminatsui, Nayuta Sugishita, Hiroki Utsunomiya, Shun Koseki, Haruhiko Gotoh, Yukiko |
author_facet | Eto, Hikaru Kishi, Yusuke Yakushiji-Kaminatsui, Nayuta Sugishita, Hiroki Utsunomiya, Shun Koseki, Haruhiko Gotoh, Yukiko |
author_sort | Eto, Hikaru |
collection | PubMed |
description | Dorsal-ventral patterning of the mammalian telencephalon is fundamental to the formation of distinct functional regions including the neocortex and ganglionic eminence. While Bone morphogenetic protein (BMP), Wnt, and Sonic hedgehog (Shh) signaling are known to determine regional identity along the dorsoventral axis, how the region-specific expression of these morphogens is established remains unclear. Here we show that the Polycomb group (PcG) protein Ring1 contributes to the ventralization of the mouse telencephalon. Deletion of Ring1b or both Ring1a and Ring1b in neuroepithelial cells induces ectopic expression of dorsal genes, including those for BMP and Wnt ligands, as well as attenuated expression of the gene for Shh, a key morphogen for ventralization, in the ventral telencephalon. We observe PcG protein–mediated trimethylation of histone 3 at lysine-27 and binding of Ring1B at BMP and Wnt ligand genes specifically in the ventral region. Furthermore, forced activation of BMP or Wnt signaling represses Shh expression. Our results thus indicate that PcG proteins suppress BMP and Wnt signaling in a region-specific manner and thereby allow proper Shh expression and development of the ventral telencephalon. |
format | Online Article Text |
id | pubmed-7658352 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-76583522020-11-17 The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon Eto, Hikaru Kishi, Yusuke Yakushiji-Kaminatsui, Nayuta Sugishita, Hiroki Utsunomiya, Shun Koseki, Haruhiko Gotoh, Yukiko Nat Commun Article Dorsal-ventral patterning of the mammalian telencephalon is fundamental to the formation of distinct functional regions including the neocortex and ganglionic eminence. While Bone morphogenetic protein (BMP), Wnt, and Sonic hedgehog (Shh) signaling are known to determine regional identity along the dorsoventral axis, how the region-specific expression of these morphogens is established remains unclear. Here we show that the Polycomb group (PcG) protein Ring1 contributes to the ventralization of the mouse telencephalon. Deletion of Ring1b or both Ring1a and Ring1b in neuroepithelial cells induces ectopic expression of dorsal genes, including those for BMP and Wnt ligands, as well as attenuated expression of the gene for Shh, a key morphogen for ventralization, in the ventral telencephalon. We observe PcG protein–mediated trimethylation of histone 3 at lysine-27 and binding of Ring1B at BMP and Wnt ligand genes specifically in the ventral region. Furthermore, forced activation of BMP or Wnt signaling represses Shh expression. Our results thus indicate that PcG proteins suppress BMP and Wnt signaling in a region-specific manner and thereby allow proper Shh expression and development of the ventral telencephalon. Nature Publishing Group UK 2020-11-11 /pmc/articles/PMC7658352/ /pubmed/33177537 http://dx.doi.org/10.1038/s41467-020-19556-5 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Article Eto, Hikaru Kishi, Yusuke Yakushiji-Kaminatsui, Nayuta Sugishita, Hiroki Utsunomiya, Shun Koseki, Haruhiko Gotoh, Yukiko The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon |
title | The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon |
title_full | The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon |
title_fullStr | The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon |
title_full_unstemmed | The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon |
title_short | The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon |
title_sort | polycomb group protein ring1 regulates dorsoventral patterning of the mouse telencephalon |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7658352/ https://www.ncbi.nlm.nih.gov/pubmed/33177537 http://dx.doi.org/10.1038/s41467-020-19556-5 |
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