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Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs

Cell cycle progression requires control of the abundance of several proteins and RNAs over space and time to properly transit from one phase to the next and to ensure faithful genomic inheritance in daughter cells. The proteasome, the main protein degradation system of the cell, facilitates the esta...

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Autores principales: Cáceres‐Gutiérrez, Rodrigo E., Andonegui, Marco A., Oliva‐Rico, Diego A., González‐Barrios, Rodrigo, Luna, Fernando, Arriaga‐Canon, Cristian, López‐Saavedra, Alejandro, Prada, Diddier, Castro, Clementina, Parmentier, Laurent, Díaz‐Chávez, José, Alfaro‐Mora, Yair, Navarro‐Delgado, Erick I., Fabian‐Morales, Eunice, Tran, Bao, Shetty, Jyoti, Zhao, Yongmei, Alcaraz, Nicolas, De la Rosa, Carlos, Reyes, José L., Hédouin, Sabrine, Hubé, Florent, Francastel, Claire, Herrera, Luis A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9299679/
https://www.ncbi.nlm.nih.gov/pubmed/34739170
http://dx.doi.org/10.1111/febs.16261
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author Cáceres‐Gutiérrez, Rodrigo E.
Andonegui, Marco A.
Oliva‐Rico, Diego A.
González‐Barrios, Rodrigo
Luna, Fernando
Arriaga‐Canon, Cristian
López‐Saavedra, Alejandro
Prada, Diddier
Castro, Clementina
Parmentier, Laurent
Díaz‐Chávez, José
Alfaro‐Mora, Yair
Navarro‐Delgado, Erick I.
Fabian‐Morales, Eunice
Tran, Bao
Shetty, Jyoti
Zhao, Yongmei
Alcaraz, Nicolas
De la Rosa, Carlos
Reyes, José L.
Hédouin, Sabrine
Hubé, Florent
Francastel, Claire
Herrera, Luis A.
author_facet Cáceres‐Gutiérrez, Rodrigo E.
Andonegui, Marco A.
Oliva‐Rico, Diego A.
González‐Barrios, Rodrigo
Luna, Fernando
Arriaga‐Canon, Cristian
López‐Saavedra, Alejandro
Prada, Diddier
Castro, Clementina
Parmentier, Laurent
Díaz‐Chávez, José
Alfaro‐Mora, Yair
Navarro‐Delgado, Erick I.
Fabian‐Morales, Eunice
Tran, Bao
Shetty, Jyoti
Zhao, Yongmei
Alcaraz, Nicolas
De la Rosa, Carlos
Reyes, José L.
Hédouin, Sabrine
Hubé, Florent
Francastel, Claire
Herrera, Luis A.
author_sort Cáceres‐Gutiérrez, Rodrigo E.
collection PubMed
description Cell cycle progression requires control of the abundance of several proteins and RNAs over space and time to properly transit from one phase to the next and to ensure faithful genomic inheritance in daughter cells. The proteasome, the main protein degradation system of the cell, facilitates the establishment of a proteome specific to each phase of the cell cycle. Its activity also strongly influences transcription. Here, we detected the upregulation of repetitive RNAs upon proteasome inhibition in human cancer cells using RNA‐seq. The effect of proteasome inhibition on centromeres was remarkable, especially on α‐Satellite RNAs. We showed that α‐Satellite RNAs fluctuate along the cell cycle and interact with members of the cohesin ring, suggesting that these transcripts may take part in the regulation of mitotic progression. Next, we forced exogenous overexpression and used gapmer oligonucleotide targeting to demonstrate that α‐Sat RNAs have regulatory roles in mitosis. Finally, we explored the transcriptional regulation of α‐Satellite DNA. Through in silico analyses, we detected the presence of CCAAT transcription factor‐binding motifs within α‐Satellite centromeric arrays. Using high‐resolution three‐dimensional immuno‐FISH and ChIP‐qPCR, we showed an association between the α‐Satellite upregulation and the recruitment of the transcription factor NFY‐A to the centromere upon MG132‐induced proteasome inhibition. Together, our results show that the proteasome controls α‐Satellite RNAs associated with the regulation of mitosis.
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spelling pubmed-92996792022-07-21 Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs Cáceres‐Gutiérrez, Rodrigo E. Andonegui, Marco A. Oliva‐Rico, Diego A. González‐Barrios, Rodrigo Luna, Fernando Arriaga‐Canon, Cristian López‐Saavedra, Alejandro Prada, Diddier Castro, Clementina Parmentier, Laurent Díaz‐Chávez, José Alfaro‐Mora, Yair Navarro‐Delgado, Erick I. Fabian‐Morales, Eunice Tran, Bao Shetty, Jyoti Zhao, Yongmei Alcaraz, Nicolas De la Rosa, Carlos Reyes, José L. Hédouin, Sabrine Hubé, Florent Francastel, Claire Herrera, Luis A. FEBS J Original Articles Cell cycle progression requires control of the abundance of several proteins and RNAs over space and time to properly transit from one phase to the next and to ensure faithful genomic inheritance in daughter cells. The proteasome, the main protein degradation system of the cell, facilitates the establishment of a proteome specific to each phase of the cell cycle. Its activity also strongly influences transcription. Here, we detected the upregulation of repetitive RNAs upon proteasome inhibition in human cancer cells using RNA‐seq. The effect of proteasome inhibition on centromeres was remarkable, especially on α‐Satellite RNAs. We showed that α‐Satellite RNAs fluctuate along the cell cycle and interact with members of the cohesin ring, suggesting that these transcripts may take part in the regulation of mitotic progression. Next, we forced exogenous overexpression and used gapmer oligonucleotide targeting to demonstrate that α‐Sat RNAs have regulatory roles in mitosis. Finally, we explored the transcriptional regulation of α‐Satellite DNA. Through in silico analyses, we detected the presence of CCAAT transcription factor‐binding motifs within α‐Satellite centromeric arrays. Using high‐resolution three‐dimensional immuno‐FISH and ChIP‐qPCR, we showed an association between the α‐Satellite upregulation and the recruitment of the transcription factor NFY‐A to the centromere upon MG132‐induced proteasome inhibition. Together, our results show that the proteasome controls α‐Satellite RNAs associated with the regulation of mitosis. John Wiley and Sons Inc. 2021-11-18 2022-04 /pmc/articles/PMC9299679/ /pubmed/34739170 http://dx.doi.org/10.1111/febs.16261 Text en © 2021 The Authors. The FEBS Journal published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Original Articles
Cáceres‐Gutiérrez, Rodrigo E.
Andonegui, Marco A.
Oliva‐Rico, Diego A.
González‐Barrios, Rodrigo
Luna, Fernando
Arriaga‐Canon, Cristian
López‐Saavedra, Alejandro
Prada, Diddier
Castro, Clementina
Parmentier, Laurent
Díaz‐Chávez, José
Alfaro‐Mora, Yair
Navarro‐Delgado, Erick I.
Fabian‐Morales, Eunice
Tran, Bao
Shetty, Jyoti
Zhao, Yongmei
Alcaraz, Nicolas
De la Rosa, Carlos
Reyes, José L.
Hédouin, Sabrine
Hubé, Florent
Francastel, Claire
Herrera, Luis A.
Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs
title Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs
title_full Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs
title_fullStr Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs
title_full_unstemmed Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs
title_short Proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐Satellite RNAs
title_sort proteasome inhibition alters mitotic progression through the upregulation of centromeric α‐satellite rnas
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9299679/
https://www.ncbi.nlm.nih.gov/pubmed/34739170
http://dx.doi.org/10.1111/febs.16261
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