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2. ATF4 couples MYC-dependent translational activity to bioenergetic demands during tumour progression

Author

Tameire, Feven, Verginadis, Ioannis I, Leli, Nektaria Maria, Polte, Christine, Conn, Crystal S, Ojha, Rani, Salas Salinas, Carlo, Chinga, Frank, Monroy, Alexandra M, Fu, Weixuan, Wang, Paul, Kossenkov, Andrew, Ye, Jiangbin, Amaravadi, Ravi K, Ignatova, Zoya, Fuchs, Serge Y, Diehl, J Alan, Ruggero, Davide, and Koumenis, Constantinos

Subjects
Biochemistry and Cell Biology, Biological Sciences, Genetics, Aetiology, 2.1 Biological and endogenous factors, Cancer, Activating Transcription Factor 4, Adaptor Proteins, Signal Transducing, Animals, Cell Cycle Proteins, Endoplasmic Reticulum Stress, Genes, myc, Humans, Mechanistic Target of Rapamycin Complex 1, Mice, Transgenic, Phosphoproteins, Phosphorylation, Protein Biosynthesis, TOR Serine-Threonine Kinases, Transcriptional Activation, Medical and Health Sciences, Developmental Biology, Biochemistry and cell biology
Abstract

The c-Myc oncogene drives malignant progression and induces robust anabolic and proliferative programmes leading to intrinsic stress. The mechanisms enabling adaptation to MYC-induced stress are not fully understood. Here we reveal an essential role for activating transcription factor 4 (ATF4) in survival following MYC activation. MYC upregulates ATF4 by activating general control nonderepressible 2 (GCN2) kinase through uncharged transfer RNAs. Subsequently, ATF4 co-occupies promoter regions of over 30 MYC-target genes, primarily those regulating amino acid and protein synthesis, including eukaryotic translation initiation factor 4E-binding protein 1 (4E-BP1), a negative regulator of translation. 4E-BP1 relieves MYC-induced proteotoxic stress and is essential to balance protein synthesis. 4E-BP1 activity is negatively regulated by mammalian target of rapamycin complex 1 (mTORC1)-dependent phosphorylation and inhibition of mTORC1 signalling rescues ATF4-deficient cells from MYC-induced endoplasmic reticulum stress. Acute deletion of ATF4 significantly delays MYC-driven tumour progression and increases survival in mouse models. Our results establish ATF4 as a cellular rheostat of MYC activity, which ensures that enhanced translation rates are compatible with survival and tumour progression.

Published
2019

8. Additional file 1 of Not1 and Not4 inversely determine mRNA solubility that sets the dynamics of co-translational events

Author

Allen, George, Weiss, Benjamin, Panasenko, Olesya O., Huch, Susanne, Villanyi, Zoltan, Albert, Benjamin, Dilg, Daniel, Zagatti, Marina, Schaughency, Paul, Liao, Susan E., Corden, Jeff, Polte, Christine, Shore, David, Ignatova, Zoya, Pelechano, Vicent, and Collart, Martine A.

Abstract

Additional file 1: Additional figures and figure legends in a single pdf file with: Figure S1. Comparison of mRNAs that are more or less soluble. Figure S2. mRNAs that are more or less soluble upon Not1 and Not4 depletion are enriched for different GO-terms. Figure S3. Comparison of RDO changes between mutants and RNA pools. Figure S4. Quality control of the Not4 PAR-CLIP. Table S5. List of strains and plasmids.

Published
2023
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10. Additional file 6 of Not1 and Not4 inversely determine mRNA solubility that sets the dynamics of co-translational events

Author

Allen, George, Weiss, Benjamin, Panasenko, Olesya O., Huch, Susanne, Villanyi, Zoltan, Albert, Benjamin, Dilg, Daniel, Zagatti, Marina, Schaughency, Paul, Liao, Susan E., Corden, Jeff, Polte, Christine, Shore, David, Ignatova, Zoya, Pelechano, Vicent, and Collart, Martine A.

Abstract

Additional file 6. A separate pdf file entitled: Uncropped blots. Related to Figure S2A.

Published
2023
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12. Author Correction: ATF4 couples MYC-dependent translational activity to bioenergetic demands during tumour progression

Author

Tameire, Feven, Verginadis, Ioannis I., Leli, Nektaria Maria, Polte, Christine, Conn, Crystal S., Ojha, Rani, Salinas, Carlo Salas, Chinga, Frank, Monroy, Alexandra. M., Fu, Weixuan, Wang, Paul, Kossenkov, Andrew, Ye, Jiangbin, Amaravadi, Ravi K., Ignatova, Zoya, Fuchs, Serge Y., Diehl, J. Alan, Ruggero, Davide, and Koumenis, Constantinos

Published
2019
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13. Not1 and Not4 inversely determine mRNA solubility that sets the dynamics of co-translational events

Author

Allen, George, primary, Weiss, Benjamin, additional, Panasenko, Olesya, additional, Huch, Susanne, additional, Villanyi, Zoltan, additional, Albert, Benjamin, additional, Dilg, Daniel, additional, Zagatti, Marina, additional, Schaughency, Paul, additional, Liao, Susan E., additional, Corden, Jeff, additional, Polte, Christine, additional, Shore, David, additional, Ignatova, Zoya, additional, Pelechano, Vicent, additional, and Collart, Martine A., additional

Published
2022
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15. RqcH and RqcP catalyze processive poly-alanine synthesis in a reconstituted ribosome-associated quality control system

Author

Takada, Hiraku, Crowe-Mcauliffe, Caillan, Polte, Christine, Sidorova, Zhanna Yu, Murina, Victoriia, Atkinson, Gemma C, Konevega, Andrey L, Ignatova, Zoya, Wilson, Daniel N, and Hauryliuk, Vasili

Subjects
Ribosomal Proteins, RNA, Transfer, AcademicSubjects/SCI00010, RNA and RNA-protein complexes, DNA Helicases, Biochemistry and Molecular Biology, Ribosome Subunits, Large, Bacterial, Peptides, Ribosomes, Biokemi och molekylärbiologi, Bacillus subtilis
Abstract

In the cell, stalled ribosomes are rescued through ribosome-associated protein quality-control (RQC) pathways. After splitting of the stalled ribosome, a C-terminal polyalanine ‘tail’ is added to the unfinished polypeptide attached to the tRNA on the 50S ribosomal subunit. In Bacillus subtilis, polyalanine tailing is catalyzed by the NEMF family protein RqcH, in cooperation with RqcP. However, the mechanistic details of this process remain unclear. Here we demonstrate that RqcH is responsible for tRNAAla selection during RQC elongation, whereas RqcP lacks any tRNA specificity. The ribosomal protein uL11 is crucial for RqcH, but not RqcP, recruitment to the 50S subunit, and B. subtilis lacking uL11 are RQC-deficient. Through mutational mapping, we identify critical residues within RqcH and RqcP that are important for interaction with the P-site tRNA and/or the 50S subunit. Additionally, we have reconstituted polyalanine-tailing in vitro and can demonstrate that RqcH and RqcP are necessary and sufficient for processivity in a minimal system. Moreover, the in vitro reconstituted system recapitulates our in vivo findings by reproducing the importance of conserved residues of RqcH and RqcP for functionality. Collectively, our findings provide mechanistic insight into the role of RqcH and RqcP in the bacterial RQC pathway.

Published
2021

16. Not4 and Not5 modulate translation elongation by Rps7A ubiquitination, Rli1 moonlighting, and condensates that exclude eIF5A

Author

Allen, George Edward, Panasenko, Olesya, Villanyi, Zoltan, Zagatti, Marina, Weiss, Benjamin, Pagliazzo, Lucile, Huch, Susanne, Polte, Christine, Zahoran, Szabolcs, Hughes, Christopher S., Pelechano, Vicent, Ignatova, Zoya, and Collart, Martine

Subjects
Saccharomyces cerevisiae Proteins, Ubiquitin-Protein Ligases, Translation elongation, Peptide Chain Elongation, Translational, Saccharomyces cerevisiae, Not1, ddc:590, Peptide Initiation Factors, Gene Expression Regulation, Fungal, RNA, Messenger, Eukaryotic Initiation Factor-5, Not5, Not4, ddc:616, Ubiquitination, RNA-Binding Proteins, RNA, Fungal, Ribosome Subunits, Small, Repressor Proteins, Condensates, Rli1, Codon optimality, EIF5A, ATP-Binding Cassette Transporters, Ribosomes, Signal Transduction, Transcription Factors
Abstract

In this work, we show that Not4 and Not5 from the Ccr4-Not complex modulate translation elongation dynamics and change ribosome A-site dwelling occupancy in a codon-dependent fashion. These codon-specific changes in not5Δ cells are very robust and independent of codon position within the mRNA, the overall mRNA codon composition, or changes of mRNA expression levels. They inversely correlate with codon-specific changes in cells depleted for eIF5A and positively correlate with those in cells depleted for ribosome-recycling factor Rli1. Not5 resides in punctate loci, co-purifies with ribosomes and Rli1, but not with eIF5A, and limits mRNA solubility. Overexpression of wild-type or non-complementing Rli1 and loss of Rps7A ubiquitination enable Not4 E3 ligase-dependent translation of polyarginine stretches. We propose that Not4 and Not5 modulate translation elongation dynamics to produce a soluble proteome by Rps7A ubiquitination, dynamic condensates that limit mRNA solubility and exclude eIF5A, and a moonlighting function of Rli1.

Published
2020

18. Structural basis of resistance to lincosamide, streptogramin A, and pleuromutilin antibiotics by ABCF ATPases in Gram-positive pathogens

Author

Crowe-McAuliffe, Caillan, primary, Murina, Victoriia, additional, Turnbull, Kathryn Jane, additional, Kasari, Marje, additional, Mohamad, Merianne, additional, Polte, Christine, additional, Takada, Hiraku, additional, Vaitkevicius, Karolis, additional, Johansson, Jörgen, additional, Ignatova, Zoya, additional, Atkinson, Gemma C., additional, O’Neill, Alex J., additional, Hauryliuk, Vasili, additional, and Wilson, Daniel N., additional

Published
2020
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19. Structural basis for bacterial ribosome quality control

Author

Crowe-McAuliffe, Caillan, primary, Takada, Hiraku, additional, Murina, Victoriia, additional, Polte, Christine, additional, Kasvandik, Sergo, additional, Tenson, Tanel, additional, Ignatova, Zoya, additional, Atkinson, Gemma C., additional, Wilson, Daniel N., additional, and Hauryliuk, Vasili, additional

Published
2020
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20. eIF3 Associates with 80S Ribosomes to Promote Translation Elongation, Mitochondrial Homeostasis, and Muscle Health

Author

Lin, Yingying, primary, Li, Fajin, additional, Huang, Linlu, additional, Polte, Christine, additional, Duan, Haoran, additional, Fang, Jianhuo, additional, Sun, Li, additional, Xing, Xudong, additional, Tian, Guiyou, additional, Cheng, Yabin, additional, Ignatova, Zoya, additional, Yang, Xuerui, additional, and Wolf, Dieter A., additional

Published
2020
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21. Not4 and Not5 Modulate Translation Elongation Dynamics Via Rli1 and Rps7a Ubiquitination, and Condensates that Exclude eIF5A

Author

Allen, George E., primary, Panasenko, Olesya O., additional, Villanyi, Zoltan, additional, Zagatti, Marina, additional, Weiss, Benjamin, additional, Pagilazzo, Lucile, additional, Polte, Christine, additional, Zahoran, Szabolcs, additional, Hughes, Christopher S., additional, Ignatova, Zoya, additional, and Collart, Martine, additional

Published
2020
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23. Additional file 1: of Assessing cell-specific effects of genetic variations using tRNA microarrays

Author

Polte, Christine, Wedemeyer, Daniel, Oliver, Kathryn, Wagner, Johannes, Bijvelds, Marcel, Mahoney, John, Jonge, Hugo, Sorscher, Eric, and Ignatova, Zoya

Abstract

Figure S1. Biological replicates of the comparative tRNA microarrays are highly reproducible. a-e Data for HBE (a), organoids (b), CFBE41o- (c), FRT (d) and HNE from a male (NL124) or female (NL117) individual (e) are shown as fold-enrichment (gradient ruler at the bottom) of tRNAs compared with HEK293 cells. Global reproducibility between each two replicates was assessed by Kolmogorov-Smirnov test (for all arrays pâ â Ľâ 0.9, i.e. very similar). The reproducibility for each tRNA probe was assessed by variability analysis of each two replicates and is presented as coefficient of variance. tRNA isoacceptors are depicted with their anticodon and corresponding amino acid; Meti-CAU, initiator tRNAMet pairing to the AUG codon. Figure S2. Correlation of tRNA abundance between tested models. a Pairwise correlation of tRNA isoacceptor abundancies. For iPSCs, only the zero time point was considered. R, Pearson correlation coefficient. b Correlation of tRNA isoacceptor abundancies for iPCSs over the course of differentiation. Stem cells at days 5, 10, 15 and 21 (gradient ruler) were compared to non-differentiated cells at time zero. Figure S3. Standard deviations of computed ribosome occupancies per codon among models. In these calculations, only the zero time point was considered for iPSCs. (DOCX 1932 kb)

Published
2019
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25. BAD-LAMP controls TLR9 trafficking and signalling in human plasmacytoid dendritic cells

Author

Argüello, Rafael, Reverendo, Marisa, Mendes, Andreia, Gatti, Evelina, Pierre, Philippe, Polte, Christine, Valečka, Jan, Camosseto, Voahirana, Auphan-Anezin, Nathalie, Ignatova, Zoya, Simoes, Marisa Reverendo, Torres, Adrian, de Pouplana, Lluis Ribas, van de Pavert, Serge, Combes, Alexis, N’guessan, Prudence, Mussard, Julie, Caux, Christophe, Bendriss-Vermare, Nathalie, Centre d'Immunologie de Marseille - Luminy (CIML), Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Aix Marseille Université (AMU), Institut National de la Santé et de la Recherche Médicale (INSERM), Centre National de la Recherche Scientifique (CNRS), Institut de l'Ouest : Droit et Europe (IODE), Université de Rennes (UR)-Centre National de la Recherche Scientifique (CNRS), Universität Hamburg (UHH), Centre de Recherche en Cancérologie de Marseille (CRCM), Aix Marseille Université (AMU)-Institut Paoli-Calmettes, Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Physiopathologie, cibles et thérapies de la polyarthrite rhumatoïde (Li2P), Université Paris 13 (UP13)-Université Sorbonne Paris Cité (USPC)-UFR Santé, Médecine et Biologie Humaine-Institut National de la Santé et de la Recherche Médicale (INSERM), Centre de Recherche en Cancérologie de Lyon (UNICANCER/CRCL), Centre Léon Bérard [Lyon]-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Paoli-Calmettes, Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Aix Marseille Université (AMU), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM), and Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)

Subjects
[SDV.IMM]Life Sciences [q-bio]/Immunology, hemic and immune systems, [SDV.BC.BC]Life Sciences [q-bio]/Cellular Biology/Subcellular Processes [q-bio.SC]
Abstract

International audience; Toll-like receptors (TLR) are essential components of the innate immune system. Several accessory proteins, such as UNC93B1, are required for transport and activation of nucleic acid sensing Toll-like receptors in endosomes. Here, we show that BAD-LAMP (LAMP5) controls TLR9 trafficking to LAMP1+ late endosomes in human plasmacytoid dendritic cells (pDC), leading to NF-κB activation and TNF production upon DNA detection. An inducible VAMP3+/LAMP2+/LAMP1− endolysosome compartment exists in pDCs from which TLR9 activation triggers type I interferon expression. BAD-LAMP-silencing enhances TLR9 retention in this compartment and consequent downstream signalling events. Conversely, sustained BAD-LAMP expression in pDCs contributes to their lack of type I interferon production after exposure to a TGF-β-positive microenvironment or isolation from human breast tumours. Hence, BAD-LAMP limits interferon expression in pDCs indirectly, by promoting TLR9 sorting to late endosome compartments at steady state and in response to immunomodulatory cues.

Published
2017

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