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The MicroRNA Landscape of MYCN-Amplified Neuroblastoma

MYCN gene amplification and upregulated expression are major hallmarks in the progression of high-risk neuroblastoma. MYCN expression and function in modulating gene synthesis in neuroblastoma is controlled at virtually every level, including poorly understood regulation at the post-transcriptional...

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Autores principales: Misiak, Danny, Hagemann, Sven, Bell, Jessica L., Busch, Bianca, Lederer, Marcell, Bley, Nadine, Schulte, Johannes H., Hüttelmaier, Stefan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8138323/
https://www.ncbi.nlm.nih.gov/pubmed/34026620
http://dx.doi.org/10.3389/fonc.2021.647737
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author Misiak, Danny
Hagemann, Sven
Bell, Jessica L.
Busch, Bianca
Lederer, Marcell
Bley, Nadine
Schulte, Johannes H.
Hüttelmaier, Stefan
author_facet Misiak, Danny
Hagemann, Sven
Bell, Jessica L.
Busch, Bianca
Lederer, Marcell
Bley, Nadine
Schulte, Johannes H.
Hüttelmaier, Stefan
author_sort Misiak, Danny
collection PubMed
description MYCN gene amplification and upregulated expression are major hallmarks in the progression of high-risk neuroblastoma. MYCN expression and function in modulating gene synthesis in neuroblastoma is controlled at virtually every level, including poorly understood regulation at the post-transcriptional level. MYCN modulates the expression of various microRNAs including the miR-17-92 cluster. MYCN mRNA expression itself is subjected to the control by miRNAs, most prominently the miR-17-92 cluster that balances MYCN expression by feed-back regulation. This homeostasis seems disturbed in neuroblastoma where MYCN upregulation coincides with severely increased expression of the miR-17-92 cluster. In the presented study, we applied high-throughput next generation sequencing to unravel the miRNome in a cohort of 97 neuroblastomas, representing all clinical stages. Aiming to reveal the MYCN-dependent miRNome, we evaluate miRNA expression in MYCN-amplified as well as none amplified tumor samples. In correlation with survival data analysis of differentially expressed miRNAs, we present various putative oncogenic as well as tumor suppressive miRNAs in neuroblastoma. Using microRNA trapping by RNA affinity purification, we provide a comprehensive view of MYCN-regulatory miRNAs in neuroblastoma-derived cells, confirming a pivotal role of the miR-17-92 cluster and moderate association by the let-7 miRNA family. Attempting to decipher how MYCN expression escapes elevated expression of inhibitory miRNAs, we present evidence that RNA-binding proteins like the IGF2 mRNA binding protein 1 reduce miRNA-directed downregulation of MYCN in neuroblastoma. Our findings emphasize the potency of post-transcriptional regulation of MYCN in neuroblastoma and unravel new avenues to pursue inhibition of this potent oncogene.
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spelling pubmed-81383232021-05-22 The MicroRNA Landscape of MYCN-Amplified Neuroblastoma Misiak, Danny Hagemann, Sven Bell, Jessica L. Busch, Bianca Lederer, Marcell Bley, Nadine Schulte, Johannes H. Hüttelmaier, Stefan Front Oncol Oncology MYCN gene amplification and upregulated expression are major hallmarks in the progression of high-risk neuroblastoma. MYCN expression and function in modulating gene synthesis in neuroblastoma is controlled at virtually every level, including poorly understood regulation at the post-transcriptional level. MYCN modulates the expression of various microRNAs including the miR-17-92 cluster. MYCN mRNA expression itself is subjected to the control by miRNAs, most prominently the miR-17-92 cluster that balances MYCN expression by feed-back regulation. This homeostasis seems disturbed in neuroblastoma where MYCN upregulation coincides with severely increased expression of the miR-17-92 cluster. In the presented study, we applied high-throughput next generation sequencing to unravel the miRNome in a cohort of 97 neuroblastomas, representing all clinical stages. Aiming to reveal the MYCN-dependent miRNome, we evaluate miRNA expression in MYCN-amplified as well as none amplified tumor samples. In correlation with survival data analysis of differentially expressed miRNAs, we present various putative oncogenic as well as tumor suppressive miRNAs in neuroblastoma. Using microRNA trapping by RNA affinity purification, we provide a comprehensive view of MYCN-regulatory miRNAs in neuroblastoma-derived cells, confirming a pivotal role of the miR-17-92 cluster and moderate association by the let-7 miRNA family. Attempting to decipher how MYCN expression escapes elevated expression of inhibitory miRNAs, we present evidence that RNA-binding proteins like the IGF2 mRNA binding protein 1 reduce miRNA-directed downregulation of MYCN in neuroblastoma. Our findings emphasize the potency of post-transcriptional regulation of MYCN in neuroblastoma and unravel new avenues to pursue inhibition of this potent oncogene. Frontiers Media S.A. 2021-05-07 /pmc/articles/PMC8138323/ /pubmed/34026620 http://dx.doi.org/10.3389/fonc.2021.647737 Text en Copyright © 2021 Misiak, Hagemann, Bell, Busch, Lederer, Bley, Schulte and Hüttelmaier 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 Oncology
Misiak, Danny
Hagemann, Sven
Bell, Jessica L.
Busch, Bianca
Lederer, Marcell
Bley, Nadine
Schulte, Johannes H.
Hüttelmaier, Stefan
The MicroRNA Landscape of MYCN-Amplified Neuroblastoma
title The MicroRNA Landscape of MYCN-Amplified Neuroblastoma
title_full The MicroRNA Landscape of MYCN-Amplified Neuroblastoma
title_fullStr The MicroRNA Landscape of MYCN-Amplified Neuroblastoma
title_full_unstemmed The MicroRNA Landscape of MYCN-Amplified Neuroblastoma
title_short The MicroRNA Landscape of MYCN-Amplified Neuroblastoma
title_sort microrna landscape of mycn-amplified neuroblastoma
topic Oncology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8138323/
https://www.ncbi.nlm.nih.gov/pubmed/34026620
http://dx.doi.org/10.3389/fonc.2021.647737
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