Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles.

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Version: Final published version
License: CC BY 4.0
Serval ID
serval:BIB_ECE3D90701DA
Type
Article: article from journal or magazin.
Collection
Publications
Institution
Title
Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles.
Journal
PLoS Biology
Author(s)
Le Martelot G., Canella D., Symul L., Migliavacca E., Gilardi F., Liechti R., Martin O., Harshman K., Delorenzi M., Desvergne B., Herr W., Deplancke B., Schibler U., Rougemont J., Guex N., Hernandez N., Naef F.
Working group(s)
CycliX Consortium
Contributor(s)
Hernandez N., Delorenzi M., Deplancke B., Desvergne B., Guex N., Herr W., Naef F., Rougemont J., Schibler U., Deplancke B., Guex N., Herr W., Guex N., Andersin T., Cousin P., Gilardi F., Gos P., Le Martelot G., Lammers F., Canella D., Gilardi F., Raghav S., Fabbretti R., Fortier A., Long L., Vlegel V., Xenarios I., Migliavacca E., Praz V., Guex N., Naef F., Rougemont J., David F., Jarosz Y., Kuznetsov D., Liechti R., Martin O., Delafontaine J., Sinclair L., Cajan J., Krier I., Leleu M., Migliavacca E., Molina N., Naldi A., Rey G., Symul L., Guex N., Naef F., Rougemont J., Bernasconi D., Delorenzi M.
ISSN
1545-7885 (Electronic)
ISSN-L
1544-9173
Publication state
Published
Issued date
2012
Peer-reviewed
Oui
Volume
10
Number
11
Pages
e1001442
Language
english
Abstract
Interactions of cell-autonomous circadian oscillators with diurnal cycles govern the temporal compartmentalization of cell physiology in mammals. To understand the transcriptional and epigenetic basis of diurnal rhythms in mouse liver genome-wide, we generated temporal DNA occupancy profiles by RNA polymerase II (Pol II) as well as profiles of the histone modifications H3K4me3 and H3K36me3. We used these data to quantify the relationships of phases and amplitudes between different marks. We found that rhythmic Pol II recruitment at promoters rather than rhythmic transition from paused to productive elongation underlies diurnal gene transcription, a conclusion further supported by modeling. Moreover, Pol II occupancy preceded mRNA accumulation by 3 hours, consistent with mRNA half-lives. Both methylation marks showed that the epigenetic landscape is highly dynamic and globally remodeled during the 24-hour cycle. While promoters of transcribed genes had tri-methylated H3K4 even at their trough activity times, tri-methylation levels reached their peak, on average, 1 hour after Pol II. Meanwhile, rhythms in tri-methylation of H3K36 lagged transcription by 3 hours. Finally, modeling profiles of Pol II occupancy and mRNA accumulation identified three classes of genes: one showing rhythmicity both in transcriptional and mRNA accumulation, a second class with rhythmic transcription but flat mRNA levels, and a third with constant transcription but rhythmic mRNAs. The latter class emphasizes widespread temporally gated posttranscriptional regulation in the mouse liver.
Keywords
Animals, Chromatin Assembly and Disassembly, Chromatin Immunoprecipitation, Circadian Rhythm, DNA Methylation, Epigenesis, Genetic, Half-Life, Histones/genetics, Histones/metabolism, Kinetics, Liver/cytology, Liver/metabolism, Male, Mice, Mice, Inbred C57BL, Models, Genetic, Promoter Regions, Genetic, RNA Polymerase II/genetics, RNA Polymerase II/metabolism, RNA Processing, Post-Transcriptional, RNA, Messenger/analysis, RNA, Messenger/metabolism, Reverse Transcriptase Polymerase Chain Reaction, Time Factors, Transcription Initiation Site, Transcription, Genetic, Transcriptome
Pubmed
Web of science
Open Access
Yes
Create date
13/08/2013 12:11
Last modification date
18/10/2023 6:10
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