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A localization screen reveals translation factories and widespread co-translational RNA targeting

Racha Chouaib, Adham Safieddine, Xavier Pichon, Arthur Imbert, Oh Sung Kwon, Aubin Samacoits, Abdel-Meneem Traboulsi, Marie-Cécile Robert, Nikolay Tsanov, Emeline Coleno, Ina Poser, Christophe Zimmer, Anthony Hyman, Hervé Le Hir, Kazem Zibara, Marion Peter, Florian Mueller, View ORCID ProfileThomas Walter, View ORCID ProfileEdouard Bertrand
doi: https://doi.org/10.1101/2020.05.20.106989
Racha Chouaib
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
3ER045, PRASE, DSST, Lebanese University, Beirut, Lebanon
11Biology Department, Faculty of Sciences-I, Lebanese University, Beirut, Lebanon
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Adham Safieddine
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
3ER045, PRASE, DSST, Lebanese University, Beirut, Lebanon
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Xavier Pichon
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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Arthur Imbert
4MINES ParisTech, PSL-Research University, CBIO-Centre for Computational Biology, 77300 Fontainebleau, France
5Institut Curie, 75248 Paris Cedex, France
6INSERM, U900, 75248 Paris Cedex, France
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Oh Sung Kwon
7Institut de biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University, 46 rue d’Ulm, 75005, Paris, France
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Aubin Samacoits
8Unité Imagerie et Modélisation, Institut Pasteur and CNRS UMR 3691, 28 rue du Docteur Roux, 75015 Paris; France
9C3BI, USR 3756 IP CNRS – Paris, France
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Abdel-Meneem Traboulsi
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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Marie-Cécile Robert
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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Nikolay Tsanov
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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Emeline Coleno
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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Ina Poser
10MPI-CBG, Pfotenhauer Str. 108, 01307 Dresden, Germany
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Christophe Zimmer
8Unité Imagerie et Modélisation, Institut Pasteur and CNRS UMR 3691, 28 rue du Docteur Roux, 75015 Paris; France
9C3BI, USR 3756 IP CNRS – Paris, France
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Anthony Hyman
10MPI-CBG, Pfotenhauer Str. 108, 01307 Dresden, Germany
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Hervé Le Hir
7Institut de biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University, 46 rue d’Ulm, 75005, Paris, France
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Kazem Zibara
3ER045, PRASE, DSST, Lebanese University, Beirut, Lebanon
11Biology Department, Faculty of Sciences-I, Lebanese University, Beirut, Lebanon
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Marion Peter
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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Florian Mueller
8Unité Imagerie et Modélisation, Institut Pasteur and CNRS UMR 3691, 28 rue du Docteur Roux, 75015 Paris; France
9C3BI, USR 3756 IP CNRS – Paris, France
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  • For correspondence: muellerf.research@gmail.com thomas.walter@mines-paristech.fr edouard.bertrand@igmm.cnrs.fr
Thomas Walter
4MINES ParisTech, PSL-Research University, CBIO-Centre for Computational Biology, 77300 Fontainebleau, France
5Institut Curie, 75248 Paris Cedex, France
6INSERM, U900, 75248 Paris Cedex, France
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  • ORCID record for Thomas Walter
  • For correspondence: muellerf.research@gmail.com thomas.walter@mines-paristech.fr edouard.bertrand@igmm.cnrs.fr
Edouard Bertrand
1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, Montpellier, France
2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, Montpellier, France
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  • ORCID record for Edouard Bertrand
  • For correspondence: muellerf.research@gmail.com thomas.walter@mines-paristech.fr edouard.bertrand@igmm.cnrs.fr
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Summary

Local translation allows a spatial control of gene expression. Here, we performed a dual protein/mRNA localization screen, using smFISH on 523 human cell lines expressing GFP-tagged genes. A total of 32 mRNAs displayed specific cytoplasmic localizations, and we observed local translation at unexpected locations, including cytoplasmic protrusions, cell edges, endosomes, Golgi, the nuclear envelope and centrosomes, the latter being cell cycle dependent. Quantitation of mRNA distribution and automatic pattern classification revealed a high degree of localization heterogeneity between cells. Surprisingly, mRNA localization frequently required ongoing translation, indicating widespread co-translational RNA targeting. Interestingly, while P-body accumulation was frequent (15 mRNAs), four mRNAs accumulated in foci that were distinct structures. These foci lacked the mature protein, but nascent polypeptide imaging showed that they were specialized translation factories. For β-catenin, foci formation was regulated by Wnt, relied on APC-dependent polysome aggregation, and led to nascent protein degradation. Thus, translation factories uniquely regulate nascent protein metabolism and create a fine granular compartmentalization of translation.

Competing Interest Statement

The authors have declared no competing interest.

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A localization screen reveals translation factories and widespread co-translational RNA targeting
Racha Chouaib, Adham Safieddine, Xavier Pichon, Arthur Imbert, Oh Sung Kwon, Aubin Samacoits, Abdel-Meneem Traboulsi, Marie-Cécile Robert, Nikolay Tsanov, Emeline Coleno, Ina Poser, Christophe Zimmer, Anthony Hyman, Hervé Le Hir, Kazem Zibara, Marion Peter, Florian Mueller, Thomas Walter, Edouard Bertrand
bioRxiv 2020.05.20.106989; doi: https://doi.org/10.1101/2020.05.20.106989
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A localization screen reveals translation factories and widespread co-translational RNA targeting
Racha Chouaib, Adham Safieddine, Xavier Pichon, Arthur Imbert, Oh Sung Kwon, Aubin Samacoits, Abdel-Meneem Traboulsi, Marie-Cécile Robert, Nikolay Tsanov, Emeline Coleno, Ina Poser, Christophe Zimmer, Anthony Hyman, Hervé Le Hir, Kazem Zibara, Marion Peter, Florian Mueller, Thomas Walter, Edouard Bertrand
bioRxiv 2020.05.20.106989; doi: https://doi.org/10.1101/2020.05.20.106989

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