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Journal articles
A Dual Protein-mRNA Localization Screen Reveals Compartmentalized Translation and Widespread Co-translational RNA Targeting
Racha Chouaib
1, 2
Adham Safieddine
1, 2
Xavier Pichon
1
Arthur Imbert
3, 4
Oh Sung Kwon
5
Aubin Samacoits
6, 7
Abdel-Meneem Traboulsi
1
Marie-Cécile Robert
1
Nikolay Tsanov
1
Emeline Coleno
1
Ina Poser
8
Christophe Zimmer
6, 7
Anthony Hyman
8
Hervé Le Hir
5
Kazem Zibara
2
Marion Peter
1
Florian Mueller
6, 7, *
Thomas Walter
3, 4, *
Edouard Bertrand
1, 9, *
*
Corresponding author
Racha Chouaib 1, 2
Author
Adham Safieddine 1, 2
Author
Xavier Pichon 1
Author
Arthur Imbert 3, 4
Author
Oh Sung Kwon 5
Author
Aubin Samacoits 6, 7
Author
Abdel-Meneem Traboulsi 1
Author
Marie-Cécile Robert 1
Author
Nikolay Tsanov 1
Author
Emeline Coleno 1
Author
Ina Poser 8
Author
Christophe Zimmer 6, 7
Author IdHAL : christophe-zimmer ORCID : https://orcid.org/0000-0001-9910-1589
Anthony A. Hyman 8
Author
Hervé Le Hir 5
Author IdHAL : herve-le-hir ORCID : https://orcid.org/0000-0001-7964-9221
Kazem Zibara 2
Author
Marion Peter 1
Author IdHAL : marion-peter ResearcherId : http://www.researcherid.com/rid/Y-5024-2019 ORCID : https://orcid.org/0000-0002-5720-4798
Florian Mueller 6, 7
Correspondent author
Thomas Walter 3, 4
Correspondent author IdHAL : thomas-walter ORCID : https://orcid.org/0000-0001-7419-7879
Edouard Bertrand 1, 9
Correspondent author IdHAL : edouard-bertrand ORCID : https://orcid.org/0000-0002-9642-7994
1
IGMM - Institut de Génétique Moléculaire de Montpellier (1919 Route de Mende - 34293 Montpellier Cedex 5 - France)
- UM - Université de Montpellier (163 rue Auguste Broussonnet - 34090 Montpellier - France)
- CNRS - Centre National de la Recherche Scientifique : UMR5535 (France)
2
ER045-PRASE - Laboratory of Stem Cells [Lebanese, Beirut] (Beirut - Lebanon)
- LU - Lebanese University [Beirut] ( P.O. Box 6573/14 Badaro, Museum, Beirut - Lebanon)
3
CBIO - Centre de Bioinformatique (35 rue Saint-Honoré 77300 Fontainebleau, France - France)
- MINES ParisTech - École nationale supérieure des mines de Paris (60, boulevard Saint-Michel 75006 Paris - France)
- PSL - Université Paris sciences et lettres (60 rue Mazarine 75006 Paris - France)
4
Cancer et génome: Bioinformatique, biostatistiques et épidémiologie d'un système complexe (26 rue d'Ulm - 75248 Paris cedex 05 - France)
- Institut Curie [Paris] ( 26 rue d'Ulm - 75248 Paris - France)
- MINES ParisTech - École nationale supérieure des mines de Paris (60, boulevard Saint-Michel 75006 Paris - France)
- PSL - Université Paris sciences et lettres (60 rue Mazarine 75006 Paris - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U900 (101, rue de Tolbiac, 75013 Paris - France)
5
IBENS - Institut de biologie de l'ENS Paris (UMR 8197/1024) (46, Rue d’Ulm
75005 Paris - France)
- Département de Biologie - ENS Paris (Département de Biologie
ENS Ulm
46 rue d 'Ulm
75005 Paris - France)
- ENS Paris - École normale supérieure - Paris (45, Rue d'Ulm - 75230 Paris cedex 05 - France)
- PSL - Université Paris sciences et lettres (60 rue Mazarine 75006 Paris - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale (101, rue de Tolbiac, 75013 Paris - France)
- CNRS - Centre National de la Recherche Scientifique (France)
- ENS Paris - École normale supérieure - Paris (45, Rue d'Ulm - 75230 Paris cedex 05 - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U1024 (101, rue de Tolbiac, 75013 Paris - France)
- CNRS - Centre National de la Recherche Scientifique : UMR8197 (France)
6
Imagerie et Modélisation - Imaging and Modeling (Département Biologie computationnelle,
Département de Biologie cellulaire et Infection,
25-28, rue du docteur Roux, 75724 Paris Cedex 15 - France)
- Institut Pasteur [Paris] (25-28, rue du docteur Roux, 75724 Paris cedex 15 - France)
- CNRS - Centre National de la Recherche Scientifique : UMR3691 (France)
7
C3BI - Centre de Bioinformatique, Biostatistique et Biologie Intégrative (25-28 rue du docteur Roux, 75724 Paris cedex 15 - France)
- Institut Pasteur [Paris] (25-28, rue du docteur Roux, 75724 Paris cedex 15 - France)
- CNRS - Centre National de la Recherche Scientifique : USR3756 (France)
8
MPI-CBG - Max Planck Institute of Molecular Cell Biology and Genetics (D-01307 Dresden, Germany - Germany)
- Max-Planck-Gesellschaft (Jägerstrasse, 10-11, D-10117 Berlin - Germany)
9
Equipe labellisée Ligue contre le Cancer (France)
Abstract : Local translation allows 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. 32 mRNAs displayed specific cytoplasmic localizations with local translation at unexpected locations, including cytoplasmic protrusions, cell edges, endosomes, Golgi, the nuclear envelope, and centrosomes, the latter being cell-cycle-dependent. Automated classification of mRNA localization patterns revealed a high degree of intercellular heterogeneity. 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.
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Journal articles
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https://hal-pasteur.archives-ouvertes.fr/pasteur-02925687
Contributor : Christophe Zimmer <>
Submitted on : Monday, November 16, 2020 - 8:26:26 PM
Last modification on : Wednesday, January 20, 2021 - 2:58:01 PM
Contributor : Christophe Zimmer <>
Submitted on : Monday, November 16, 2020 - 8:26:26 PM
Last modification on : Wednesday, January 20, 2021 - 2:58:01 PM
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Distributed under a Creative Commons Attribution - NonCommercial 4.0 International License
Identifiers
- HAL Id : pasteur-02925687, version 1
- DOI : 10.1016/j.devcel.2020.07.010
- PUBMED : 32783880
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PASTEUR | PSL | BS | UNIV-MONTPELLIER | CURIE | FNCLCC | PARISTECH | ENSMP_CBIO | CNRS | ENS-PARIS | ENSMP | INSTITUT-TELECOM | PRAIRIE-IA
Citation
Racha Chouaib, Adham Safieddine, Xavier Pichon, Arthur Imbert, Oh Sung Kwon, et al.. A Dual Protein-mRNA Localization Screen Reveals Compartmentalized Translation and Widespread Co-translational RNA Targeting. Developmental Cell, Elsevier, 2020, 54, pp.773 - 791.e5. ⟨10.1016/j.devcel.2020.07.010⟩. ⟨pasteur-02925687⟩
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