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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
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.
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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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