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The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA

Multiple myeloma, the second most frequent hematologic tumor after lymphomas, is an incurable cancer. Recent sequencing efforts have identified the ribonuclease DIS3 as one of the most frequently mutated genes in this disease. DIS3 represents the catalytic subunit of the exosome, a macromolecular co...

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Autores principales: Segalla, Simona, Pivetti, Silvia, Todoerti, Katia, Chudzik, Malgorzata Agata, Giuliani, Erica Claudia, Lazzaro, Federico, Volta, Viviana, Lazarevic, Dejan, Musco, Giovanna, Muzi-Falconi, Marco, Neri, Antonino, Biffo, Stefano, Tonon, Giovanni
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
RNA
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4446438/
https://www.ncbi.nlm.nih.gov/pubmed/25925570
http://dx.doi.org/10.1093/nar/gkv387
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author Segalla, Simona
Pivetti, Silvia
Todoerti, Katia
Chudzik, Malgorzata Agata
Giuliani, Erica Claudia
Lazzaro, Federico
Volta, Viviana
Lazarevic, Dejan
Musco, Giovanna
Muzi-Falconi, Marco
Neri, Antonino
Biffo, Stefano
Tonon, Giovanni
author_facet Segalla, Simona
Pivetti, Silvia
Todoerti, Katia
Chudzik, Malgorzata Agata
Giuliani, Erica Claudia
Lazzaro, Federico
Volta, Viviana
Lazarevic, Dejan
Musco, Giovanna
Muzi-Falconi, Marco
Neri, Antonino
Biffo, Stefano
Tonon, Giovanni
author_sort Segalla, Simona
collection PubMed
description Multiple myeloma, the second most frequent hematologic tumor after lymphomas, is an incurable cancer. Recent sequencing efforts have identified the ribonuclease DIS3 as one of the most frequently mutated genes in this disease. DIS3 represents the catalytic subunit of the exosome, a macromolecular complex central to the processing, maturation and surveillance of various RNAs. miRNAs are an evolutionarily conserved class of small noncoding RNAs, regulating gene expression at post-transcriptional level. Ribonucleases, including Drosha, Dicer and XRN2, are involved in the processing and stability of miRNAs. However, the role of DIS3 on the regulation of miRNAs remains largely unknown. Here we found that DIS3 regulates the levels of the tumor suppressor let-7 miRNAs without affecting other miRNA families. DIS3 facilitates the maturation of let-7 miRNAs by reducing in the cytoplasm the RNA stability of the pluripotency factor LIN28B, a inhibitor of let-7 processing. DIS3 inactivation, through the increase of LIN28B and the reduction of mature let-7, enhances the translation of let-7 targets such as MYC and RAS leading to enhanced tumorigenesis. Our study establishes that the ribonuclease DIS3, targeting LIN28B, sustains the maturation of let-7 miRNAs and suggests the increased translation of critical oncogenes as one of the biological outcomes of DIS3 inactivation.
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spelling pubmed-44464382015-06-15 The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA Segalla, Simona Pivetti, Silvia Todoerti, Katia Chudzik, Malgorzata Agata Giuliani, Erica Claudia Lazzaro, Federico Volta, Viviana Lazarevic, Dejan Musco, Giovanna Muzi-Falconi, Marco Neri, Antonino Biffo, Stefano Tonon, Giovanni Nucleic Acids Res RNA Multiple myeloma, the second most frequent hematologic tumor after lymphomas, is an incurable cancer. Recent sequencing efforts have identified the ribonuclease DIS3 as one of the most frequently mutated genes in this disease. DIS3 represents the catalytic subunit of the exosome, a macromolecular complex central to the processing, maturation and surveillance of various RNAs. miRNAs are an evolutionarily conserved class of small noncoding RNAs, regulating gene expression at post-transcriptional level. Ribonucleases, including Drosha, Dicer and XRN2, are involved in the processing and stability of miRNAs. However, the role of DIS3 on the regulation of miRNAs remains largely unknown. Here we found that DIS3 regulates the levels of the tumor suppressor let-7 miRNAs without affecting other miRNA families. DIS3 facilitates the maturation of let-7 miRNAs by reducing in the cytoplasm the RNA stability of the pluripotency factor LIN28B, a inhibitor of let-7 processing. DIS3 inactivation, through the increase of LIN28B and the reduction of mature let-7, enhances the translation of let-7 targets such as MYC and RAS leading to enhanced tumorigenesis. Our study establishes that the ribonuclease DIS3, targeting LIN28B, sustains the maturation of let-7 miRNAs and suggests the increased translation of critical oncogenes as one of the biological outcomes of DIS3 inactivation. Oxford University Press 2015-05-26 2015-04-29 /pmc/articles/PMC4446438/ /pubmed/25925570 http://dx.doi.org/10.1093/nar/gkv387 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle RNA
Segalla, Simona
Pivetti, Silvia
Todoerti, Katia
Chudzik, Malgorzata Agata
Giuliani, Erica Claudia
Lazzaro, Federico
Volta, Viviana
Lazarevic, Dejan
Musco, Giovanna
Muzi-Falconi, Marco
Neri, Antonino
Biffo, Stefano
Tonon, Giovanni
The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA
title The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA
title_full The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA
title_fullStr The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA
title_full_unstemmed The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA
title_short The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA
title_sort ribonuclease dis3 promotes let-7 mirna maturation by degrading the pluripotency factor lin28b mrna
topic RNA
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4446438/
https://www.ncbi.nlm.nih.gov/pubmed/25925570
http://dx.doi.org/10.1093/nar/gkv387
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