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YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis
YAP1 fusion-positive supratentorial ependymomas predominantly occur in infants, but the molecular mechanisms of oncogenesis are unknown. Here we show YAP1-MAMLD1 fusions are sufficient to drive malignant transformation in mice, and the resulting tumors share histo-molecular characteristics of human...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6718408/ https://www.ncbi.nlm.nih.gov/pubmed/31477715 http://dx.doi.org/10.1038/s41467-019-11884-5 |
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author | Pajtler, Kristian W. Wei, Yiju Okonechnikov, Konstantin Silva, Patricia B. G. Vouri, Mikaella Zhang, Lei Brabetz, Sebastian Sieber, Laura Gulley, Melissa Mauermann, Monika Wedig, Tatjana Mack, Norman Imamura Kawasawa, Yuka Sharma, Tanvi Zuckermann, Marc Andreiuolo, Felipe Holland, Eric Maass, Kendra Körkel-Qu, Huiqin Liu, Hai-Kun Sahm, Felix Capper, David Bunt, Jens Richards, Linda J. Jones, David T. W. Korshunov, Andrey Chavez, Lukas Lichter, Peter Hoshino, Mikio Pfister, Stefan M. Kool, Marcel Li, Wei Kawauchi, Daisuke |
author_facet | Pajtler, Kristian W. Wei, Yiju Okonechnikov, Konstantin Silva, Patricia B. G. Vouri, Mikaella Zhang, Lei Brabetz, Sebastian Sieber, Laura Gulley, Melissa Mauermann, Monika Wedig, Tatjana Mack, Norman Imamura Kawasawa, Yuka Sharma, Tanvi Zuckermann, Marc Andreiuolo, Felipe Holland, Eric Maass, Kendra Körkel-Qu, Huiqin Liu, Hai-Kun Sahm, Felix Capper, David Bunt, Jens Richards, Linda J. Jones, David T. W. Korshunov, Andrey Chavez, Lukas Lichter, Peter Hoshino, Mikio Pfister, Stefan M. Kool, Marcel Li, Wei Kawauchi, Daisuke |
author_sort | Pajtler, Kristian W. |
collection | PubMed |
description | YAP1 fusion-positive supratentorial ependymomas predominantly occur in infants, but the molecular mechanisms of oncogenesis are unknown. Here we show YAP1-MAMLD1 fusions are sufficient to drive malignant transformation in mice, and the resulting tumors share histo-molecular characteristics of human ependymomas. Nuclear localization of YAP1-MAMLD1 protein is mediated by MAMLD1 and independent of YAP1-Ser127 phosphorylation. Chromatin immunoprecipitation-sequencing analyses of human YAP1-MAMLD1-positive ependymoma reveal enrichment of NFI and TEAD transcription factor binding site motifs in YAP1-bound regulatory elements, suggesting a role for these transcription factors in YAP1-MAMLD1-driven tumorigenesis. Mutation of the TEAD binding site in the YAP1 fusion or repression of NFI targets prevents tumor induction in mice. Together, these results demonstrate that the YAP1-MAMLD1 fusion functions as an oncogenic driver of ependymoma through recruitment of TEADs and NFIs, indicating a rationale for preclinical studies to block the interaction between YAP1 fusions and NFI and TEAD transcription factors. |
format | Online Article Text |
id | pubmed-6718408 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-67184082019-09-04 YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis Pajtler, Kristian W. Wei, Yiju Okonechnikov, Konstantin Silva, Patricia B. G. Vouri, Mikaella Zhang, Lei Brabetz, Sebastian Sieber, Laura Gulley, Melissa Mauermann, Monika Wedig, Tatjana Mack, Norman Imamura Kawasawa, Yuka Sharma, Tanvi Zuckermann, Marc Andreiuolo, Felipe Holland, Eric Maass, Kendra Körkel-Qu, Huiqin Liu, Hai-Kun Sahm, Felix Capper, David Bunt, Jens Richards, Linda J. Jones, David T. W. Korshunov, Andrey Chavez, Lukas Lichter, Peter Hoshino, Mikio Pfister, Stefan M. Kool, Marcel Li, Wei Kawauchi, Daisuke Nat Commun Article YAP1 fusion-positive supratentorial ependymomas predominantly occur in infants, but the molecular mechanisms of oncogenesis are unknown. Here we show YAP1-MAMLD1 fusions are sufficient to drive malignant transformation in mice, and the resulting tumors share histo-molecular characteristics of human ependymomas. Nuclear localization of YAP1-MAMLD1 protein is mediated by MAMLD1 and independent of YAP1-Ser127 phosphorylation. Chromatin immunoprecipitation-sequencing analyses of human YAP1-MAMLD1-positive ependymoma reveal enrichment of NFI and TEAD transcription factor binding site motifs in YAP1-bound regulatory elements, suggesting a role for these transcription factors in YAP1-MAMLD1-driven tumorigenesis. Mutation of the TEAD binding site in the YAP1 fusion or repression of NFI targets prevents tumor induction in mice. Together, these results demonstrate that the YAP1-MAMLD1 fusion functions as an oncogenic driver of ependymoma through recruitment of TEADs and NFIs, indicating a rationale for preclinical studies to block the interaction between YAP1 fusions and NFI and TEAD transcription factors. Nature Publishing Group UK 2019-09-02 /pmc/articles/PMC6718408/ /pubmed/31477715 http://dx.doi.org/10.1038/s41467-019-11884-5 Text en © The Author(s) 2019 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 Pajtler, Kristian W. Wei, Yiju Okonechnikov, Konstantin Silva, Patricia B. G. Vouri, Mikaella Zhang, Lei Brabetz, Sebastian Sieber, Laura Gulley, Melissa Mauermann, Monika Wedig, Tatjana Mack, Norman Imamura Kawasawa, Yuka Sharma, Tanvi Zuckermann, Marc Andreiuolo, Felipe Holland, Eric Maass, Kendra Körkel-Qu, Huiqin Liu, Hai-Kun Sahm, Felix Capper, David Bunt, Jens Richards, Linda J. Jones, David T. W. Korshunov, Andrey Chavez, Lukas Lichter, Peter Hoshino, Mikio Pfister, Stefan M. Kool, Marcel Li, Wei Kawauchi, Daisuke YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis |
title | YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis |
title_full | YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis |
title_fullStr | YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis |
title_full_unstemmed | YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis |
title_short | YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis |
title_sort | yap1 subgroup supratentorial ependymoma requires tead and nuclear factor i-mediated transcriptional programmes for tumorigenesis |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6718408/ https://www.ncbi.nlm.nih.gov/pubmed/31477715 http://dx.doi.org/10.1038/s41467-019-11884-5 |
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