Gcn4 misregulation reveals a direct role for the evolutionary conserved $$\mathrm{EKC/KEOPS}$$ in the t6A modification of t$$\mathrm{RNA}$$s
Abstract
The EKC/KEOPS complex is universally conserved in Archaea and Eukarya and has been implicated in several cellular processes, including transcription, telomere homeostasis and genomic instability. However, the molecular function of the complex has remained elusive so far. We analyzed the transcriptome of EKC/KEOPS mutants and observed a specific profile that is highly enriched in targets of the Gcn4p transcriptional activator. GCN4 expression was found to be activated at the translational level in mutants via the defective recognition of the inhibitory upstream ORFs (uORFs) present in its leader. We show that EKC/KEOPS mutants are defective for the N6-threonylcarbamoyl adenosine modification at position 37 (t6A37) of tRNAs decoding ANN codons, which affects initiation at the inhibitory uORFs and provokes Gcn4 de-repression. Structural modeling reveals similarities between Kae1 and bacterial enzymes involved in carbamoylation reactions analogous to t6A37 formation, supporting a direct role for the EKC in tRNA modification. These findings are further supported by strong genetic interactions of EKC mutants with a translation initiation factor and with threonine biosynthesis genes. Overall, our data provide a novel twist to understanding the primary function of the EKC/KEOPS and its impact on several essential cellular functions like transcription and telomere homeostasis.
- Authors:
-
- Centre National de la Recherche Scientifique (CNRS), Gif sur Yvette (France). LEA Laboratory of Nuclear RNA metabolism; Aarhus University (Denmark); University Paris-Sud, Orsay (France)
- Utrecht University (Netherlands). University Medical Center
- Centre National de la Recherche Scientifique (CNRS), Gif sur Yvette (France). LEA Laboratory of Nuclear RNA metabolism; Aarhus University (Denmark); University of Padova (Italy)
- University of Florida, Gainesville, FL (United States)
- Centre National de la Recherche Scientifique (CNRS), Gif sur Yvette (France). LEA Laboratory of Nuclear RNA metabolism
- University Paris-Sud, Orsay (France)
- Institute Pasteur, CNRS, Paris (France). Unite de Genetique des Interactions Macromoleculaires
- Centre National de la Recherche Scientifique (CNRS), Gif sur Yvette (France). LEA Laboratory of Nuclear RNA metabolism; Aarhus University (Denmark)
- Publication Date:
- Research Org.:
- Univ. of Florida, Gainesville, FL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Centre National pour la Recherche Scientifique (CNRS); Agence Nationale pour la Recherche (ANR); Netherlands Organization of Scientific Research (NWO); Netherlands Bioinformatics Centre (NBIC); National Institutes of Health (NIH)
- OSTI Identifier:
- 1904624
- Grant/Contract Number:
- FG02-07ER64498; ANR-09-BLAN-0349-03; ANR-08-JCJC-0019-01; 021.002.035; 817.02.015; 050.71.057; 911.06.009; 016.108.607; R01 GM70641-01
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 39; Journal Issue: 14; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Daugeron, Marie-Claire, Lenstra, Tineke L., Frizzarin, Martina, El Yacoubi, Basma, Liu, Xipeng, Baudin-Baillieu, Agnès, Lijnzaad, Philip, Decourty, Laurence, Saveanu, Cosmin, Jacquier, Alain, Holstege, Frank C. P., de Crécy-Lagard, Valérie, van Tilbeurgh, Herman, and Libri, Domenico. Gcn4 misregulation reveals a direct role for the evolutionary conserved $\mathrm{EKC/KEOPS}$ in the t6A modification of t$\mathrm{RNA}$s. United States: N. p., 2011.
Web. doi:10.1093/nar/gkr178.
Daugeron, Marie-Claire, Lenstra, Tineke L., Frizzarin, Martina, El Yacoubi, Basma, Liu, Xipeng, Baudin-Baillieu, Agnès, Lijnzaad, Philip, Decourty, Laurence, Saveanu, Cosmin, Jacquier, Alain, Holstege, Frank C. P., de Crécy-Lagard, Valérie, van Tilbeurgh, Herman, & Libri, Domenico. Gcn4 misregulation reveals a direct role for the evolutionary conserved $\mathrm{EKC/KEOPS}$ in the t6A modification of t$\mathrm{RNA}$s. United States. https://doi.org/10.1093/nar/gkr178
Daugeron, Marie-Claire, Lenstra, Tineke L., Frizzarin, Martina, El Yacoubi, Basma, Liu, Xipeng, Baudin-Baillieu, Agnès, Lijnzaad, Philip, Decourty, Laurence, Saveanu, Cosmin, Jacquier, Alain, Holstege, Frank C. P., de Crécy-Lagard, Valérie, van Tilbeurgh, Herman, and Libri, Domenico. Fri .
"Gcn4 misregulation reveals a direct role for the evolutionary conserved $\mathrm{EKC/KEOPS}$ in the t6A modification of t$\mathrm{RNA}$s". United States. https://doi.org/10.1093/nar/gkr178. https://www.osti.gov/servlets/purl/1904624.
@article{osti_1904624,
title = {Gcn4 misregulation reveals a direct role for the evolutionary conserved $\mathrm{EKC/KEOPS}$ in the t6A modification of t$\mathrm{RNA}$s},
author = {Daugeron, Marie-Claire and Lenstra, Tineke L. and Frizzarin, Martina and El Yacoubi, Basma and Liu, Xipeng and Baudin-Baillieu, Agnès and Lijnzaad, Philip and Decourty, Laurence and Saveanu, Cosmin and Jacquier, Alain and Holstege, Frank C. P. and de Crécy-Lagard, Valérie and van Tilbeurgh, Herman and Libri, Domenico},
abstractNote = {The EKC/KEOPS complex is universally conserved in Archaea and Eukarya and has been implicated in several cellular processes, including transcription, telomere homeostasis and genomic instability. However, the molecular function of the complex has remained elusive so far. We analyzed the transcriptome of EKC/KEOPS mutants and observed a specific profile that is highly enriched in targets of the Gcn4p transcriptional activator. GCN4 expression was found to be activated at the translational level in mutants via the defective recognition of the inhibitory upstream ORFs (uORFs) present in its leader. We show that EKC/KEOPS mutants are defective for the N6-threonylcarbamoyl adenosine modification at position 37 (t6A37) of tRNAs decoding ANN codons, which affects initiation at the inhibitory uORFs and provokes Gcn4 de-repression. Structural modeling reveals similarities between Kae1 and bacterial enzymes involved in carbamoylation reactions analogous to t6A37 formation, supporting a direct role for the EKC in tRNA modification. These findings are further supported by strong genetic interactions of EKC mutants with a translation initiation factor and with threonine biosynthesis genes. Overall, our data provide a novel twist to understanding the primary function of the EKC/KEOPS and its impact on several essential cellular functions like transcription and telomere homeostasis.},
doi = {10.1093/nar/gkr178},
journal = {Nucleic Acids Research},
number = 14,
volume = 39,
place = {United States},
year = {Fri Apr 01 00:00:00 EDT 2011},
month = {Fri Apr 01 00:00:00 EDT 2011}
}
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