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A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport

Local translation allows for a spatial control of gene expression. Here, we use high-throughput smFISH to screen centrosomal protein-coding genes, and we describe 8 human mRNAs accumulating at centrosomes. These mRNAs localize at different stages during cell cycle with a remarkable choreography, ind...

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Autores principales: Safieddine, Adham, Coleno, Emeline, Salloum, Soha, Imbert, Arthur, Traboulsi, Abdel-Meneem, Kwon, Oh Sung, Lionneton, Frederic, Georget, Virginie, Robert, Marie-Cécile, Gostan, Thierry, Lecellier, Charles-Henri, Chouaib, Racha, Pichon, Xavier, Le Hir, Hervé, Zibara, Kazem, Mueller, Florian, Walter, Thomas, Peter, Marion, Bertrand, Edouard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7921559/
https://www.ncbi.nlm.nih.gov/pubmed/33649340
http://dx.doi.org/10.1038/s41467-021-21585-7
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author Safieddine, Adham
Coleno, Emeline
Salloum, Soha
Imbert, Arthur
Traboulsi, Abdel-Meneem
Kwon, Oh Sung
Lionneton, Frederic
Georget, Virginie
Robert, Marie-Cécile
Gostan, Thierry
Lecellier, Charles-Henri
Chouaib, Racha
Pichon, Xavier
Le Hir, Hervé
Zibara, Kazem
Mueller, Florian
Walter, Thomas
Peter, Marion
Bertrand, Edouard
author_facet Safieddine, Adham
Coleno, Emeline
Salloum, Soha
Imbert, Arthur
Traboulsi, Abdel-Meneem
Kwon, Oh Sung
Lionneton, Frederic
Georget, Virginie
Robert, Marie-Cécile
Gostan, Thierry
Lecellier, Charles-Henri
Chouaib, Racha
Pichon, Xavier
Le Hir, Hervé
Zibara, Kazem
Mueller, Florian
Walter, Thomas
Peter, Marion
Bertrand, Edouard
author_sort Safieddine, Adham
collection PubMed
description Local translation allows for a spatial control of gene expression. Here, we use high-throughput smFISH to screen centrosomal protein-coding genes, and we describe 8 human mRNAs accumulating at centrosomes. These mRNAs localize at different stages during cell cycle with a remarkable choreography, indicating a finely regulated translational program at centrosomes. Interestingly, drug treatments and reporter analyses reveal a common translation-dependent localization mechanism requiring the nascent protein. Using ASPM and NUMA1 as models, single mRNA and polysome imaging reveals active movements of endogenous polysomes towards the centrosome at the onset of mitosis, when these mRNAs start localizing. ASPM polysomes associate with microtubules and localize by either motor-driven transport or microtubule pulling. Remarkably, the Drosophila orthologs of the human centrosomal mRNAs also localize to centrosomes and also require translation. These data identify a conserved family of centrosomal mRNAs that localize by active polysome transport mediated by nascent proteins.
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spelling pubmed-79215592021-03-12 A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport Safieddine, Adham Coleno, Emeline Salloum, Soha Imbert, Arthur Traboulsi, Abdel-Meneem Kwon, Oh Sung Lionneton, Frederic Georget, Virginie Robert, Marie-Cécile Gostan, Thierry Lecellier, Charles-Henri Chouaib, Racha Pichon, Xavier Le Hir, Hervé Zibara, Kazem Mueller, Florian Walter, Thomas Peter, Marion Bertrand, Edouard Nat Commun Article Local translation allows for a spatial control of gene expression. Here, we use high-throughput smFISH to screen centrosomal protein-coding genes, and we describe 8 human mRNAs accumulating at centrosomes. These mRNAs localize at different stages during cell cycle with a remarkable choreography, indicating a finely regulated translational program at centrosomes. Interestingly, drug treatments and reporter analyses reveal a common translation-dependent localization mechanism requiring the nascent protein. Using ASPM and NUMA1 as models, single mRNA and polysome imaging reveals active movements of endogenous polysomes towards the centrosome at the onset of mitosis, when these mRNAs start localizing. ASPM polysomes associate with microtubules and localize by either motor-driven transport or microtubule pulling. Remarkably, the Drosophila orthologs of the human centrosomal mRNAs also localize to centrosomes and also require translation. These data identify a conserved family of centrosomal mRNAs that localize by active polysome transport mediated by nascent proteins. Nature Publishing Group UK 2021-03-01 /pmc/articles/PMC7921559/ /pubmed/33649340 http://dx.doi.org/10.1038/s41467-021-21585-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Safieddine, Adham
Coleno, Emeline
Salloum, Soha
Imbert, Arthur
Traboulsi, Abdel-Meneem
Kwon, Oh Sung
Lionneton, Frederic
Georget, Virginie
Robert, Marie-Cécile
Gostan, Thierry
Lecellier, Charles-Henri
Chouaib, Racha
Pichon, Xavier
Le Hir, Hervé
Zibara, Kazem
Mueller, Florian
Walter, Thomas
Peter, Marion
Bertrand, Edouard
A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport
title A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport
title_full A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport
title_fullStr A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport
title_full_unstemmed A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport
title_short A choreography of centrosomal mRNAs reveals a conserved localization mechanism involving active polysome transport
title_sort choreography of centrosomal mrnas reveals a conserved localization mechanism involving active polysome transport
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7921559/
https://www.ncbi.nlm.nih.gov/pubmed/33649340
http://dx.doi.org/10.1038/s41467-021-21585-7
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