E4F1 COORDINATES PYRUVATE METABOLISM AND THE ACTIVITY OF THE ELONGATOR COMPLEX TO ENSURE TRANSLATION FIDELITY DURING BRAIN DEVELOPMENT
Pyruvate metabolism defects lead to severe neuropathies such as the Leigh syndrome (LS) but the molecular mechanisms underlying neuronal cell death remain poorly understood. Here, we unravel a connection between pyruvate metabolism and the regulation of the epitranscriptome that is relevant to LS pa...
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| Vydáno v: | Nature communications |
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Cold Spring Harbor Laboratory
02.10.2024
Nature Publishing Group |
| Vydání: | 1.2 |
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| ISSN: | 2041-1723, 2692-8205, 2041-1723 |
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| Abstract | Pyruvate metabolism defects lead to severe neuropathies such as the Leigh syndrome (LS) but the molecular mechanisms underlying neuronal cell death remain poorly understood. Here, we unravel a connection between pyruvate metabolism and the regulation of the epitranscriptome that is relevant to LS pathogenesis. We identified the transcription factor E4F1 as a key coordinator of AcetylCoenzyme A (AcCoA) production by the pyruvate dehydrogenase complex (PDC) and its utilization as an essential co-factor by the Elongator complex to acetylate tRNAs at the wobble position uridine 34 (U34). E4F1-mediated direct transcriptional regulation of Dlat and Elp3, two genes encoding key subunits of the PDC and of the Elongator complex, respectively, ensured proper translation fidelity and cell survival in the central nervous system (CNS) during mouse embryonic development. Furthermore, analysis of PDH-deficient cells highlighted a crosstalk linking the PDC to ELP3 expression that is perturbed in LS patients. |
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| AbstractList | Pyruvate metabolism defects lead to severe neuropathies such as the Leigh syndrome (LS) but the molecular mechanisms underlying neuronal cell death remain poorly understood. Here, we unravel a connection between pyruvate metabolism and the regulation of the epitranscriptome that is relevant to LS pathogenesis. We identified the transcription factor E4F1 as a key coordinator of AcetylCoenzyme A (AcCoA) production by the pyruvate dehydrogenase complex (PDC) and its utilization as an essential co-factor by the Elongator complex to acetylate tRNAs at the wobble position uridine 34 (U34). E4F1-mediated direct transcriptional regulation of Dlat and Elp3, two genes encoding key subunits of the PDC and of the Elongator complex, respectively, ensured proper translation fidelity and cell survival in the central nervous system (CNS) during mouse embryonic development. Furthermore, analysis of PDH-deficient cells highlighted a crosstalk linking the PDC to ELP3 expression that is perturbed in LS patients. SUMMARY Pyruvate metabolism defects lead to severe neuropathies such as the Leigh syndrome (LS) but the molecular mechanisms underlying neuronal cell death remain poorly understood. Here, we unravel a connection between pyruvate metabolism and the regulation of the epitranscriptome that is relevant to LS pathogenesis. We identified the transcription factor E4F1 as a key coordinator of AcetylCoenzyme A (AcCoA) production by the pyruvate dehydrogenase complex (PDC) and its utilization as an essential co-factor by the Elongator complex to acetylate tRNAs at the wobble position uridine 34 (U 34 ). E4F1-mediated direct transcriptional regulation of Dlat and Elp3 , two genes encoding key subunits of the PDC and of the Elongator complex, respectively, ensured proper translation fidelity and cell survival in the central nervous system (CNS) during mouse embryonic development. Furthermore, analysis of PDH-deficient cells highlighted a crosstalk linking the PDC to ELP3 expression that is perturbed in LS patients. |
| Author | Claude, Sardet Nelly, Pirot Lucille, Stuani Mélanie, Rousseau Yoan, Buscail Pierre, Close Laurent, Le Cam Michela, Di Michele Laura, Papon Aurore, Attina Pierre-François, Roux Pierrick, Dupré Betty, Encislai Justine, Guégan Javier, Florido Hugo, Mathieu Lucie, Rubio Daniele, Ghezzi Tania, Sorg Carole, Ferraro Peyret Vincent, Compan Céline, Jahanault-Tagliani Adeline, Torro Alexandre, David Giuseppe, Arena Sophie, Laguesse Christophe, Hirtz Morane, Houdeville Francesca, Rapino Geneviève, Rodier Hanna, Kulyk Armelle, Choquet Floriant, Bellvert Cédric, Chaveroux Elise, Lebigot Olivia, Wendling Andrea, Legati Imène, Tabet Matthieu, Lacroix Maryse, Fuentes Henri-Alexandre, Michaud Laurent, Nguyen Carlo, De Blasio Francois-Xavier, Frenois Fabrice, Ango |
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| Cites_doi | 10.1016/j.bbagrm.2017.11.006 10.1016/j.cell.2014.04.046 10.1038/s41586-018-0243-7 10.1038/s41588-017-0026-3 10.1371/journal.pone.0089020 10.1016/j.cmet.2024.05.002 10.3390/ijms21218209 10.1038/s41467-021-22254-5 10.1126/scitranslmed.aan0457 10.1093/hmg/ddr393 10.1016/j.cmet.2024.07.022 |
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| Keywords | pyruvate metabolism translation Leigh syndrome E4F1 Elongator complex integrated stress response |
| Language | English |
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| Notes | Competing Interest Statement: The authors have declared no competing interest. |
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| Snippet | Pyruvate metabolism defects lead to severe neuropathies such as the Leigh syndrome (LS) but the molecular mechanisms underlying neuronal cell death remain... SUMMARY Pyruvate metabolism defects lead to severe neuropathies such as the Leigh syndrome (LS) but the molecular mechanisms underlying neuronal cell death... |
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| Title | E4F1 COORDINATES PYRUVATE METABOLISM AND THE ACTIVITY OF THE ELONGATOR COMPLEX TO ENSURE TRANSLATION FIDELITY DURING BRAIN DEVELOPMENT |
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