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

Adham Safieddine (), Emeline Coleno, Soha Salloum, Arthur Imbert, Abdel-Meneem Traboulsi, Oh Sung Kwon, Frederic Lionneton, Virginie Georget, Marie-Cécile Robert, Thierry Gostan, Charles-Henri Lecellier, Racha Chouaib, Xavier Pichon, Hervé Hir, Kazem Zibara, Florian Mueller, Thomas Walter, Marion Peter and Edouard Bertrand ()
Additional contact information
Adham Safieddine: University of Montpellier, CNRS
Emeline Coleno: University of Montpellier, CNRS
Soha Salloum: University of Montpellier, CNRS
Arthur Imbert: MINES ParisTech, PSL-Research University, CBIO-Centre for Computational Biology
Abdel-Meneem Traboulsi: University of Montpellier, CNRS
Oh Sung Kwon: PSL Research University
Frederic Lionneton: BioCampus Montpellier
Virginie Georget: BioCampus Montpellier
Marie-Cécile Robert: University of Montpellier, CNRS
Thierry Gostan: University of Montpellier, CNRS
Charles-Henri Lecellier: University of Montpellier, CNRS
Racha Chouaib: University of Montpellier, CNRS
Xavier Pichon: University of Montpellier, CNRS
Hervé Hir: PSL Research University
Kazem Zibara: Lebanese University
Florian Mueller: Imaging and Modeling Unit, Institut Pasteur, UMR 3691 CNRS, C3BI USR 3756 IP CNRS
Thomas Walter: MINES ParisTech, PSL-Research University, CBIO-Centre for Computational Biology
Marion Peter: University of Montpellier, CNRS
Edouard Bertrand: University of Montpellier, CNRS

Nature Communications, 2021, vol. 12, issue 1, 1-21

Abstract: Abstract 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.

Date: 2021
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DOI: 10.1038/s41467-021-21585-7

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