Diurnal regulation of RNA polymerase III transcription is under the control of both the feeding–fasting response and the circadian clock
- François Mange1,
- Viviane Praz1,2,
- Eugenia Migliavacca1,2,6,
- Ian M. Willis3,
- Frédéric Schütz1,4,
- Nouria Hernandez1,
- the CycliX Consortium5,
- Nouria Hernandez7,
- Mauro Delorenzi8,9,10,
- Bart Deplancke11,
- Béatrice Desvergne7,
- Nicolas Guex12,
- Winship Herr7,
- Felix Naef11,
- Jacques Rougemont13,
- Ueli Schibler14,
- Teemu Andersin14,15,
- Pascal Cousin7,
- Federica Gilardi7,
- Fabienne Lammers7,
- François Mange7,
- Dominic Villeneuve7,
- Fabrice David8,13,
- Roberto Fabbretti12,
- Philippe Jacquet8,13,
- Irina Krier11,
- Dmitry Kuznetsov12,
- Marion Leleu8,13,
- Robin Liechti12,
- Olivier Martin12,
- Eugenia Migliavacca7,12,16,
- Aurélien Naldi7,17,
- Viviane Praz7,8,
- Leonor Rib7,
- Jonathan Sobel11,
- Volker Vlegel12 and
- Ioannis Xenarios7,8,12
- 1Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, 1015 Lausanne, Switzerland;
- 2Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;
- 3Department of Biochemistry, Albert Einstein College of Medicine, Bronx, New York 10461, USA;
- 4Bioinformatics Core Facility, Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
- 7Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, 1015 Lausanne, Switzerland
- 8Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
- 9Bioinformatics Core Facility, Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
- 10Department of Oncology and Ludwig Center for Cancer Research, Faculty of Biology and Medicine, University of Lausanne, 1011 Lausanne, Switzerland
- 11Interfaculty Institute of Bioengineering, School of Life Sciences, Ecole polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland
- 12Vital IT, Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
- 13Bioinformatics and Biostatistics Core Facility, School of Life Sciences, Ecole polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland
- 14Department of Molecular Biology, Faculty of Sciences, University of Geneva, 1211 Geneva, Switzerland
- Corresponding author: nouria.hernandez{at}unil.ch
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↵5 A complete list of Consortium authors appears at the end of this article.
Abstract
RNA polymerase III (Pol III) synthesizes short noncoding RNAs, many of which are essential for translation. Accordingly, Pol III activity is tightly regulated with cell growth and proliferation by factors such as MYC, RB1, TRP53, and MAF1. MAF1 is a repressor of Pol III transcription whose activity is controlled by phosphorylation; in particular, it is inactivated through phosphorylation by the TORC1 kinase complex, a sensor of nutrient availability. Pol III regulation is thus sensitive to environmental cues, yet a diurnal profile of Pol III transcription activity is so far lacking. Here, we first use gene expression arrays to measure mRNA accumulation during the diurnal cycle in the livers of (1) wild-type mice, (2) arrhythmic Arntl knockout mice, (3) mice fed at regular intervals during both night and day, and (4) mice lacking the Maf1 gene, and so provide a comprehensive view of the changes in cyclic mRNA accumulation occurring in these different systems. We then show that Pol III occupancy of its target genes rises before the onset of the night, stays high during the night, when mice normally ingest food and when translation is known to be increased, and decreases in daytime. Whereas higher Pol III occupancy during the night reflects a MAF1-dependent response to feeding, the rise of Pol III occupancy before the onset of the night reflects a circadian clock-dependent response. Thus, Pol III transcription during the diurnal cycle is regulated both in response to nutrients and by the circadian clock, which allows anticipatory Pol III transcription.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.217521.116.
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Freely available online through the Genome Research Open Access option.
- Received November 11, 2016.
- Accepted March 17, 2017.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
